58 results on '"Donal T. Manahan"'
Search Results
2. Thermal sensitivities of respiration and protein synthesis differ among larval families of the Pacific oyster, Crassostrea gigas
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Melissa B. DellaTorre, Francis T. C. Pan, Andrew W. Griffith, Ning Li, and Donal T. Manahan
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Physiology ,Larva ,Protein Biosynthesis ,Respiration ,Insect Science ,Temperature ,Animals ,Animal Science and Zoology ,Crassostrea ,Aquatic Science ,Molecular Biology ,Ecology, Evolution, Behavior and Systematics - Abstract
Understanding the mechanisms of biological responses to environmental change is a central theme in comparative and evolutionary physiology. Here, we analyzed variation in physiological responses to temperature, using 21 full-sibling larval families of the Pacific oyster, Crassostrea gigas. Pedigrees were confirmed with genetic markers for adult broodstock obtained from our breeding program. From these 21 larval families, 41 determinations of thermal sensitivity (Q10 values) were assayed for larvae of different sizes. For respiration, thermal sensitivity was consistent within a larval family during growth, but showed significant differences among families. Different Q10 values were evident among 21 larval families, with family accounting for 87% of variation. Specifically, four larval families maintained an increased thermal sensitivity for respiration (Q10 of 3). This physiology would confer resilience to rising temperature by matching the increased energy demand of protein synthesis (Q10 of 3 previously reported). For protein synthesis, differences in Q10 values were also observed. Notably, a family was identified that had a decreased thermal sensitivity for protein synthesis (Q10 of 1.7 cf. Q10 of 3 for other families), conferring an optimal energy allocation with rising temperature. Different thermal sensitivities across families for respiration (energy supply) and protein synthesis (energy demand) were integrated into models of energy allocation at the whole-organism level. The outcome of these analyses provides insights into the physiological bases of optimal energy allocation with rising temperature. These transgenerational (egg-to-egg) experiments highlight approaches to dissect components of phenotypic variance to address long-standing questions of genetic adaptation and physiological resilience to environmental change.
- Published
- 2022
3. Differing thermal sensitivities of physiological processes alter ATP allocation
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Francis T. C. Pan, Scott L. Applebaum, and Donal T. Manahan
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0106 biological sciences ,Bioenergetics ,Physiology ,Q10 ,Aquatic Science ,01 natural sciences ,03 medical and health sciences ,Adenosine Triphosphate ,Respiration ,Protein biosynthesis ,Animals ,Crassostrea ,Molecular Biology ,Ecology, Evolution, Behavior and Systematics ,Ion transporter ,030304 developmental biology ,chemistry.chemical_classification ,0303 health sciences ,Glycine transport ,biology ,010604 marine biology & hydrobiology ,Temperature ,Pacific oyster ,biology.organism_classification ,Amino acid ,chemistry ,Insect Science ,Larva ,Biophysics ,Animal Science and Zoology ,Energy Metabolism - Abstract
Changes in environmental temperature impact rate processes at all levels of biological organization. Yet, the thermal sensitivity of specific physiological processes that impact allocation of the ATP pool within a species is less well understood. In this study of developmental stages of the Pacific oyster, Crassostrea gigas, thermal sensitivities were measured for growth, survivorship, protein synthesis, respiration, and transport of amino acids and ions. At warmer temperatures, larvae grew faster but suffered increased mortality. An analysis of temperature sensitivity (Q10 values) revealed that protein synthesis, the major ATP-consuming process in larvae of C. gigas, is more sensitive to temperature change (Q10 value of 2.9±0.18) than is metabolic rate (Q10 of 2.0±0.15). Ion transport by Na+/K+-ATPase measured in vivo has a Q10 value of 2.1±0.09. The corresponding value for glycine transport is 2.4±0.23. Differing thermal responses for protein synthesis and respiration result in a disproportional increase in the allocation of available ATP to protein synthesis with rising temperature. A bioenergetic model is presented illustrating how changes in growth and temperature impact allocation of the ATP pool. Over an environmentally relevant temperature range for this species, the proportion of the ATP pool allocated to protein synthesis increases from 35% to 65%. The greater energy demand to support protein synthesis with increasing temperature will compromise energy availability to support other essential physiological processes. Defining the tradeoffs of ATP demand will provide insights into understanding the adaptive capacity of organisms to respond to various scenarios of environmental change.
- Published
- 2020
4. Shifting Balance of Protein Synthesis and Degradation Sets a Threshold for Larval Growth Under Environmental Stress
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Donal T. Manahan, Scott L. Applebaum, Christina A. Frieder, and T-C Francis Pan
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0106 biological sciences ,Biology ,Protein degradation ,010603 evolutionary biology ,01 natural sciences ,pCO2 ,chemistry.chemical_compound ,Downregulation and upregulation ,Stress, Physiological ,Protein biosynthesis ,Animals ,Seawater ,Crassostrea ,010604 marine biology & hydrobiology ,Ocean acidification ,Marine invertebrates ,Carbon Dioxide ,Hydrogen-Ion Concentration ,chemistry ,Larva ,Protein Biosynthesis ,Proteolysis ,Available energy ,Biophysics ,Energy Metabolism ,General Agricultural and Biological Sciences ,Adenosine triphosphate - Abstract
Exogenous environmental factors alter growth rates, yet information remains scant on the biochemical mechanisms and energy trade-offs that underlie variability in the growth of marine invertebrates. Here we study the biochemical bases for differential growth and energy utilization (as adenosine triphosphate [ATP] equivalents) during larval growth of the bivalve Crassostrea gigas exposed to increasing levels of experimental ocean acidification (control, middle, and high pCO2, corresponding to ∼400, ∼800, and ∼1100 µatm, respectively). Elevated pCO2 hindered larval ability to accrete both shell and whole-body protein content. This negative impact was not due to an inability to synthesize protein per se, because size-specific rates of protein synthesis were upregulated at both middle and high pCO2 treatments by as much as 45% relative to control pCO2. Rather, protein degradation rates increased with increasing pCO2. At control pCO2, 89% of cellular energy (ATP equivalents) utilization was accounted for by just 2 processes in larvae, with protein synthesis accounting for 66% and sodium-potassium transport accounting for 23%. The energetic demand necessitated by elevated protein synthesis rates could be accommodated either by reallocating available energy from within the existing ATP pool or by increasing the production of total ATP. The former strategy was observed at middle pCO2, while the latter strategy was observed at high pCO2. Increased pCO2 also altered sodium-potassium transport, but with minimal impact on rates of ATP utilization relative to the impact observed for protein synthesis. Quantifying the actual energy costs and trade-offs for maintaining physiological homeostasis in response to stress will help to reveal the mechanisms of resilience thresholds to environmental change.
- Published
- 2018
5. Metabolic cost of calcification in bivalve larvae under experimental ocean acidification
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T.-C. Francis Pan, Scott L. Applebaum, Donal T. Manahan, Dennis Hedgecock, and Christina A. Frieder
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0106 biological sciences ,Larva ,010504 meteorology & atmospheric sciences ,Ecology ,010604 marine biology & hydrobiology ,fungi ,Ocean acidification ,Aquatic Science ,Biology ,Oceanography ,medicine.disease ,01 natural sciences ,Metabolic cost ,medicine ,Ecology, Evolution, Behavior and Systematics ,0105 earth and related environmental sciences ,Calcification - Abstract
Physiological increases in energy expenditure frequently occur in response to environmental stress. Although energy limitation is often invoked as a basis for decreased calcification under ocean acidification, energy-relevant measurements related to this process are scant. In this study we focus on first-shell (prodissoconch I) formation in larvae of the Pacific oyster, Crassostrea gigas. The energy cost of calcification was empirically derived to be ≤ 1.1 µJ (ng CaCO3)−1. Regardless of the saturation state of aragonite (2.77 vs. 0.77), larvae utilize the same amount of total energy to complete first-shell formation. Even though there was a 56% reduction of shell mass and an increase in dissolution at aragonite undersaturation, first-shell formation is not energy limited because sufficient endogenous reserves are available to meet metabolic demand. Further studies were undertaken on larvae from genetic crosses of pedigreed lines to test for variance in response to aragonite undersaturation. Larval families show variation in response to ocean acidification, with loss of shell size ranging from no effect to 28%. These differences show that resilience to ocean acidification may exist among genotypes. Combined studies of bioenergetics and genetics are promising approaches for understanding climate change impacts on marine organisms that undergo calcification.
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- 2016
6. A scientific name for Pacific oysters
- Author
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Ryan B. Carnegie, B. L. Bayne, Roger Mann, Sylvie Lapegue, Chris Langdon, Maureen K. Krause, Ximing Guo, Eric N. Powell, Pierre Boudry, Dennis Hedgecock, Jonathan P. Davis, M. Anglès d'Auriac, Thierry Backeljau, Sandra E. Shumway, Donal T. Manahan, Peter G. Beninger, Norwegian Institute for Water Research (NIVA), Royal Belgian Institute of Natural Sciences (RBINS), Mer, molécules et santé EA 2160 (MMS), Université de Nantes - UFR des Sciences Pharmaceutiques et Biologiques, Université de Nantes (UN)-Université de Nantes (UN)-Le Mans Université (UM)-Université de Nantes - UFR des Sciences et des Techniques (UN UFR ST), Université de Nantes (UN)-Université de Nantes (UN), Laboratoire des Sciences de l'Environnement Marin (LEMAR) (LEMAR), Institut de Recherche pour le Développement (IRD)-Institut Français de Recherche pour l'Exploitation de la Mer (IFREMER)-Université de Brest (UBO)-Institut Universitaire Européen de la Mer (IUEM), Institut de Recherche pour le Développement (IRD)-Institut national des sciences de l'Univers (INSU - CNRS)-Université de Brest (UBO)-Centre National de la Recherche Scientifique (CNRS)-Institut national des sciences de l'Univers (INSU - CNRS)-Université de Brest (UBO)-Centre National de la Recherche Scientifique (CNRS)-Centre National de la Recherche Scientifique (CNRS), Institut Français de Recherche pour l'Exploitation de la Mer - Brest (IFREMER Centre de Bretagne), Institut Français de Recherche pour l'Exploitation de la Mer (IFREMER), Virginia Institute of Marine Science (VIMS), Rutgers University [Newark], Rutgers University System (Rutgers), University of Southern California (USC), Hofstra University [Hempstead], Oregon State University (OSU), Laboratoire de Génétique et Pathologie des Mollusques Marins, 17390 La Tremblade, France. (LGPMM), Santé, Génétique et Microbiologie des Mollusques (IFREMER SG2M), Institut Français de Recherche pour l'Exploitation de la Mer - Atlantique (IFREMER Atlantique), Institut Français de Recherche pour l'Exploitation de la Mer (IFREMER)-Institut Français de Recherche pour l'Exploitation de la Mer (IFREMER)-Institut Français de Recherche pour l'Exploitation de la Mer - Atlantique (IFREMER Atlantique), Institut Français de Recherche pour l'Exploitation de la Mer (IFREMER)-Institut Français de Recherche pour l'Exploitation de la Mer (IFREMER), University of Southern Mississippi (USM), University of Connecticut (UCONN), Le Mans Université (UM)-Université de Nantes - UFR des Sciences et des Techniques (UN UFR ST), Université de Nantes (UN)-Université de Nantes (UN)-Université de Nantes - UFR des Sciences Pharmaceutiques et Biologiques, Institut de Recherche pour le Développement (IRD)-Institut national des sciences de l'Univers (INSU - CNRS)-Université de Brest (UBO)-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD)-Institut national des sciences de l'Univers (INSU - CNRS)-Université de Brest (UBO)-Centre National de la Recherche Scientifique (CNRS)-Centre National de la Recherche Scientifique (CNRS), Laboratoire de Génétique et Pathologie des Mollusques Marins (LGPMM), and Santé, Génétique et Microbiologie des Mollusques (SGMM)
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0303 health sciences ,biology ,ACL ,letter ,010501 environmental sciences ,Aquatic Science ,Pacific oyster ,biology.organism_classification ,01 natural sciences ,Fishery ,03 medical and health sciences ,Crassostrea ,[SDE.BE]Environmental Sciences/Biodiversity and Ecology ,Biology ,030304 developmental biology ,0105 earth and related environmental sciences - Abstract
WOS:000447083800041; International audience
- Published
- 2019
7. The Proposed Dropping of the Genus Crassostrea for All Pacific Cupped Oysters and Its Replacement by a New Genus Magallana: A Dissenting View
- Author
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Roger Mann, T. Backeljau, R. Bohn, Michael J. Ahrens, B. L. Bayne, Sylvie Lapegue, Donal T. Manahan, Eric N. Powell, Chris Langdon, Ximing Guo, Sandra E. Shumway, José L. Sánchez, Jonathan P. Davis, Peter G. Beninger, Pierre Boudry, M. Anglès d'Auriac, Timothy J. Green, Dennis Hedgecock, Daniel I. Speiser, L. Perez-Paralle, Maureen K. Krause, Chunbo Li, Ana M. Ibarra, Haiyan Wang, Peter R. Kingsley-Smith, Paul D. Rawson, Standish K. Allen, Virginia Institute of Marine Science (VIMS), Royal Belgian Institute of Natural Sciences (RBINS), Université de Nantes (UN), Laboratoire des Sciences de l'Environnement Marin (LEMAR) (LEMAR), Institut de Recherche pour le Développement (IRD)-Institut Français de Recherche pour l'Exploitation de la Mer (IFREMER)-Université de Brest (UBO)-Institut Universitaire Européen de la Mer (IUEM), Institut de Recherche pour le Développement (IRD)-Institut national des sciences de l'Univers (INSU - CNRS)-Université de Brest (UBO)-Centre National de la Recherche Scientifique (CNRS)-Institut national des sciences de l'Univers (INSU - CNRS)-Université de Brest (UBO)-Centre National de la Recherche Scientifique (CNRS)-Centre National de la Recherche Scientifique (CNRS), Institut Français de Recherche pour l'Exploitation de la Mer - Brest (IFREMER Centre de Bretagne), Institut Français de Recherche pour l'Exploitation de la Mer (IFREMER), University of Southern California (USC), Macquarie University, Rutgers University System (Rutgers), Centro de Investigaciones Biologicas del Noroeste [Mexico] (CONACYT-CIBNOR), Consejo Nacional de Ciencia y Tecnología [Mexico] (CONACYT), Hofstra University [Hempstead], Oregon State University (OSU), Chinese Academy of Sciences [Beijing] (CAS), Universidade de Santiago de Compostela [Spain] (USC ), University of Maine, University of South Carolina [Columbia], University of Connecticut (UCONN), Institut de Recherche pour le Développement (IRD)-Institut national des sciences de l'Univers (INSU - CNRS)-Université de Brest (UBO)-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD)-Institut national des sciences de l'Univers (INSU - CNRS)-Université de Brest (UBO)-Centre National de la Recherche Scientifique (CNRS)-Centre National de la Recherche Scientifique (CNRS), Institut Universitaire Européen de la Mer (IUEM), and Institut de Recherche pour le Développement (IRD)-Institut national des sciences de l'Univers (INSU - CNRS)-Université de Brest (UBO)-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD)-Institut national des sciences de l'Univers (INSU - CNRS)-Université de Brest (UBO)-Centre National de la Recherche Scientifique (CNRS)-Institut Français de Recherche pour l'Exploitation de la Mer (IFREMER)-Centre National de la Recherche Scientifique (CNRS)-Université de Brest (UBO)
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0106 biological sciences ,Genus Crassostrea ,ACL ,010604 marine biology & hydrobiology ,Zoology ,Aquatic Science ,Biology ,Ostras ,biology.organism_classification ,010603 evolutionary biology ,01 natural sciences ,Animales marinos ,Aquatic organisms ,taxonomy ,classification ,Dissenting opinion ,Genus ,Crassostrea ,Taxonomy (biology) ,14. Life underwater ,[SDE.BE]Environmental Sciences/Biodiversity and Ecology - Abstract
The World Register of Marine Species (WoRMS) currently registers all Pacific cupped oysters that were formerly members of the genus Crassostrea in a new genus, Magallana. Magallana gigas is designated as an ‘‘accepted name,’’ whereas a search for Crassostrea gigas results in the message ‘‘no matching results found.’’ This has caused dismay among many biologists, aquaculturists, and other stakeholders with an interest in the Pacific and other oysters. This note, which is authored by 27 interested scientists, presents a dissenting view and a rebuttal of the proposed change of genus.
- Published
- 2017
8. Predicting phenotypic variation in growth and metabolism of marine invertebrate larvae
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Donal T. Manahan, T.-C. Francis Pan, Scott L. Applebaum, and Brian A. Lentz
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0106 biological sciences ,0301 basic medicine ,Ecophysiology ,Larva ,biology ,Ecology ,010604 marine biology & hydrobiology ,Zoology ,Metabolism ,Marine invertebrates ,Aquatic Science ,Pacific oyster ,biology.organism_classification ,01 natural sciences ,Enzyme assay ,03 medical and health sciences ,030104 developmental biology ,Respiration ,biology.protein ,Ecology, Evolution, Behavior and Systematics ,Ion transporter - Abstract
Understanding the mechanisms that establish variation in growth and metabolism is fundamental in evolutionary and physiological ecology. Although a genetic basis is frequently invoked to explain variation in performance, it remains challenging to study such processes in marine animals due to the lack of genetically-enabled “model” organisms. The Pacific oyster Crassostrea gigas is a species for which pedigreed genetic lines have been established. In this study, a series of larval families was produced by crossbreeding pedigreed lines to yield large-volume larval cultures to provide sufficient biomass for biochemical and physiological analyses. Major phenotypic contrasts in larval growth rate were evident. A primary goal of this study was to investigate the physiological bases for this variation in growth and to identify biomarkers that are predictive of growth potential. To that end, measurements were undertaken to define the relationship between rates of growth, respiration, and ion transport by the sodium-potassium pump (in vivo Na+,K+-ATPase activity). The relationship of respiration and ion transport during larval growth showed that, on average, 17% of total energy demand was allocated to support ion transport. Further analyses of total Na+,K+-ATPase activity (in vitro enzyme assay) revealed that 41% of the total metabolic rate could be accounted for by this single process if all of the enzyme was physiologically active. Significant biological variation was evident, however, when size-specific comparisons were made across different larval families. These differences were up to (i) 2.2-fold in ion transport rates; (ii) 2.8-fold in the allocation of energy to support the metabolic demand of ion transport; (iii) 3.5-fold in total enzyme activity; (iv) 3.9-fold in the physiologically active fraction of total enzyme; and (v) 3.1-fold in gene expression. These differences among families highlight the need to distinguish genetic from environmental causes of biological variation. Notably, for inferences of physiological changes based upon molecular biological analyses, the measured rates of ion transport were not predicted from concurrent measurements of gene expression or enzyme activity. Size-corrected rates of ion transport were predictive of variation in growth rates among different larval families, supporting the application of physiological rates of ion transport as a predictor of growth differences. Evolutionary variation in physiological performance has important implications for understanding the ecology of larval forms. Developing physiological indices will be of value in predicting growth and metabolism and corresponding survival of larval forms of different genotypes in response to environmental change.
- Published
- 2016
9. Metabolic Cost of Protein Synthesis in Larvae of the Pacific Oyster (Crassostrea gigas) Is Fixed Across Genotype, Phenotype, and Environmental Temperature
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James Lee, Donal T. Manahan, and Scott L. Applebaum
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0106 biological sciences ,Genotype ,Zoology ,Environment ,Biology ,010603 evolutionary biology ,01 natural sciences ,Genetic variation ,Animals ,Crassostrea ,Shellfish ,Ecology ,Catabolism ,010604 marine biology & hydrobiology ,fungi ,Temperature ,Aquatic animal ,Pacific oyster ,biology.organism_classification ,Phenotype ,Larva ,Energy Metabolism ,General Agricultural and Biological Sciences - Abstract
The energy made available through catabolism of specific biochemical reserves is constant using standard thermodynamic conversion equivalents (e.g., 24.0 J mg protein(-1)). In contrast, measurements reported for the energy cost of synthesis of specific biochemical constituents are highly variable. In this study, we measured the metabolic cost of protein synthesis and determined whether this cost was influenced by genotype, phenotype, or environment. We focused on larval stages of the Pacific oyster Crassostrea gigas, a species that offers several experimental advantages: availability of genetically pedigreed lines, manipulation of ploidy, and tractability of larval forms for in vivo studies of physiological processes. The cost of protein synthesis was measured in larvae of C. gigas for 1) multiple genotypes, 2) phenotypes with different growth rates, and 3) different environmental temperatures. For all treatments, the cost of protein synthesis was within a narrow range--near the theoretical minimum--with a fixed cost (mean ± one standard error, n = 21) of 2.1 ± 0.2 J (mg protein synthesized)(-1) We conclude that there is no genetic variation in the metabolic cost of protein synthesis, thereby simplifying bioenergetic models. Protein synthesis is a major component of larval metabolism in C. gigas, accounting for more than half the metabolic rate in diploid (59%) and triploid larvae (54%). These results provide measurements of metabolic cost of protein synthesis in larvae of C. gigas, an indicator species for impacts of ocean change, and provide a quantitative basis for evaluating the cost of resilience.
- Published
- 2016
10. Sources of Energy for Increased Metabolic Demand During Metamorphosis of the Abalone Haliotis rufescens (Mollusca)
- Author
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Donal T. Manahan, Fraser Shilling, and Ove Hoegh-Guldberg
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Larva ,Haliotis rufescens ,Abalone ,Ecology ,media_common.quotation_subject ,Marine larval ecology ,fungi ,Biology ,biology.organism_classification ,Animal science ,Juvenile ,Seawater ,Metamorphosis ,General Agricultural and Biological Sciences ,Mollusca ,media_common - Abstract
Pelagic, lecithotrophic (nonfeeding) larvae of the red abalone (Haliotis rufescens) settle and subsequently metamorphose into benthic juveniles capable of feeding on particulate food. Thus, metamorphosis must be fueled by either endogenous reserves or a nonparticulate food source such as dissolved organic material (DOM) in seawater. The metabolic rates (measured as oxygen consumption) of abalone larvae were found to increase by an average of 3- to 5-fold from the larva to early juvenile stage. The total cost of development from embryo to juvenile measured for three cultures ranged from 41.6 mJ to 55.0 mJ. Meeting this cost would require 1.3 to 1.7 {mu}g of biomass (ash-free dry mass), which is similar to the initial biomass of the spawned oocyte at 1.36 +/- 0.04 {mu}g (mean of four cultures). However, there was no net loss of biomass during development from the oocyte to the juvenile. The uptake of alanine and glucose from seawater by larvae and juveniles could provide one-third of the organic material required to supply metabolism, even if the transporters were only operating at 20% of their maximum capacity throughout development. For larvae undergoing metamorphosis (between 6- and 9-days-old) the proportion of total metabolic demand supplied using aerobically catabolized biomass was only 39%. The higher metabolic rates of metamorphosis are met only in part by consuming stored endogenous reserves. Concomitant with an increase in mass-specific metabolic rate during metamorphosis, the maximal capacity (Jmax) for the transport of dissolved alanine from seawater increased 3-fold, from 61.2 +/- 1.9 (SE) to 182.0 +/- 49 pmol alanine individual-1 h-1. The majority (range: 61% to 100%) of the energy requirements of larval and early juvenile development of H. rufescens could be supplied by input of DOM from the environment. Measurements of transport rates of amino acids and sugars by these animals, and calculations of the energy input from these substrates, indicate that the cumulative transport of DOM from seawater during development to the early juvenile stage could supply an amount of energy equivalent to the initial maternal endowment of energy reserves to the oocyte of this lecithotrophic species.
- Published
- 2017
11. Experimental ocean acidification alters the allocation of metabolic energy
- Author
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T.-C. Francis Pan, Donal T. Manahan, and Scott L. Applebaum
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Male ,Time Factors ,Environmental change ,Oceans and Seas ,ved/biology.organism_classification_rank.species ,Gene Expression ,pCO2 ,chemistry.chemical_compound ,biology.animal ,Animals ,Seawater ,14. Life underwater ,Model organism ,Strongylocentrotus purpuratus ,Sea urchin ,Ion transporter ,Analysis of Variance ,Multidisciplinary ,biology ,Ecology ,ved/biology ,Age Factors ,Proteins ,Ocean acidification ,Carbon Dioxide ,Hydrogen-Ion Concentration ,Biological Sciences ,biology.organism_classification ,Cell biology ,chemistry ,13. Climate action ,Larva ,Carbon dioxide ,Female ,Sodium-Potassium-Exchanging ATPase ,Energy Metabolism ,Acids - Abstract
Energy is required to maintain physiological homeostasis in response to environmental change. Although responses to environmental stressors frequently are assumed to involve high metabolic costs, the biochemical bases of actual energy demands are rarely quantified. We studied the impact of a near-future scenario of ocean acidification [800 µatm partial pressure of CO2 (pCO2)] during the development and growth of an important model organism in developmental and environmental biology, the sea urchin Strongylocentrotus purpuratus. Size, metabolic rate, biochemical content, and gene expression were not different in larvae growing under control and seawater acidification treatments. Measurements limited to those levels of biological analysis did not reveal the biochemical mechanisms of response to ocean acidification that occurred at the cellular level. In vivo rates of protein synthesis and ion transport increased ∼50% under acidification. Importantly, the in vivo physiological increases in ion transport were not predicted from total enzyme activity or gene expression. Under acidification, the increased rates of protein synthesis and ion transport that were sustained in growing larvae collectively accounted for the majority of available ATP (84%). In contrast, embryos and prefeeding and unfed larvae in control treatments allocated on average only 40% of ATP to these same two processes. Understanding the biochemical strategies for accommodating increases in metabolic energy demand and their biological limitations can serve as a quantitative basis for assessing sublethal effects of global change. Variation in the ability to allocate ATP differentially among essential functions may be a key basis of resilience to ocean acidification and other compounding environmental stressors.
- Published
- 2015
12. Biochemical bases of growth variation during development: a study of protein turnover in pedigreed families of bivalve larvae (
- Author
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T-C Francis, Pan, Scott L, Applebaum, Christina A, Frieder, and Donal T, Manahan
- Subjects
Adenosine Triphosphate ,Phenotype ,Genotype ,Animal Shells ,Larva ,Protein Biosynthesis ,Animals ,Crassostrea - Abstract
Animal size is a highly variable trait regulated by complex interactions between biological and environmental processes. Despite the importance of understanding the mechanistic bases of growth, predicting size variation in early stages of development remains challenging. Pedigreed lines of the Pacific oyster (
- Published
- 2017
13. Addressing Grand Challenges In Organismal Biology: The Need For Synthesis
- Author
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Patsy S. Dickinson, Daniel Grünbaum, Billie J. Swalla, Dianna K. Padilla, James H. Marden, Thomas L. Daniel, Cheryl Hayashi, Donal T. Manahan, and Brian Tsukimura
- Subjects
Engineering ethics ,Computational biology ,General Agricultural and Biological Sciences ,Grand Challenges - Abstract
This is a pre-copyedited, author-produced PDF of an article accepted for publication in BioScience following peer review. The version of record [Padilla, Dianna K., etc. (2014) Addressing Grand Challenges In Organismal Biology: The Need For Synthesis. BioScience 64: 1178–1187] is available online at: http://dx.doi.org/10.1093/biosci/biu164.
- Published
- 2014
14. Expression of amino acid transporter genes in developmental stages and adult tissues of Antarctic echinoderms
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Donal T. Manahan, Charles S. Capron, Scott L. Applebaum, and David W. Ginsburg
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chemistry.chemical_classification ,biology ,Ecology ,Zoology ,Odontaster validus ,Marine invertebrates ,biology.organism_classification ,Solute carrier family ,Amino acid ,chemistry ,biology.animal ,Gene family ,Sterechinus neumayeri ,Amino acid transporter ,General Agricultural and Biological Sciences ,Sea urchin - Abstract
Epithelial cells in the body wall of adult and developmental stages of marine invertebrates absorb dissolved organic material directly from seawater. Despite over a century of study, little is known about the molecular biological mechanisms responsible for this transport process. Previous studies on embryonic and larval Antarctic echinoderms show that amino acid uptake could provide an important supplement of metabolic substrates. In the present study, partial cDNA sequences of 11 putative amino acid transporter genes were isolated from six species of Antarctic echinoderms including the Antarctic sea stars Acodontaster hodgsoni, Diplasterias brucei, Odontaster meridionalis, Odontaster validus, and Perknaster fuscus, and the Antarctic sea urchin Sterechinus neumayeri. Conserved domains of cDNA-deduced amino acid sequences characterized these genes as being members of a family of amino acid transporters (solute carrier family 6). Expression of these genes was detected throughout embryonic and larval development of two species that have contrasting developmental modes (A. hodgsoni: lecithotrophic; O. meridionalis: planktotrophic). In all six species studied, the expression of amino acid transporter genes was detected in tube feet and digestive organs of adult animals, demonstrating that members of a single amino acid transporter gene family are expressed during the entire life history of a marine invertebrate. The identification of these genes is an important step toward developing a mechanistic understanding of amino acid transport capacities in Antarctic marine invertebrates.
- Published
- 2013
15. Ribosomal Analysis of Rapid Rates of Protein Synthesis in the Antarctic Sea Urchin Sterechinus neumayeri
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Donal T. Manahan, Robert E. Maxson, and Douglas A. Pace
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High rate ,chemistry.chemical_classification ,biology ,Arctic Regions ,Peptide ,Ribosomal RNA ,biology.organism_classification ,Ribosome ,Biochemistry ,chemistry ,Protein Biosynthesis ,Sea Urchins ,biology.animal ,Botany ,Protein biosynthesis ,Animals ,Sterechinus neumayeri ,Elongation ,General Agricultural and Biological Sciences ,Ribosomes ,Sea urchin - Abstract
Previous research has shown that developing stages of the Antarctic sea urchin Sterechinus neumayeri have high rates of protein synthesis that are comparable to those of similar species living in much warmer waters. Direct measurements of the biosynthetic capacities of isolated ribosomes have not been reported for marine organisms living in the extreme-cold environment of Antarctica. Such measurements are required for a mechanistic understanding of how the critical and highly complex processes involved in protein synthesis are regulated in animals living in the coldest marine environment on Earth (-1 degrees C). We tested the hypothesis that high rates of protein synthesis in the cold are a direct result of high biosynthetic capacities of ribosomes engaged in protein synthesis. Our results show that the rate at which ribosomes manufacture proteins (i.e., the peptide elongation rate) at -1 degrees C is surprisingly similar to rates measured in other sea urchin species at temperatures that are over 15 degrees C warmer. Average peptide elongation rates for a range of developmental stages of the Antarctic sea urchin were 0.36 codons s(-1) (+/- 0.05, SE). On the basis of subcellular rate determinations of ribosomal activity, we calculated stage-specific rates of protein synthesis for blastulae and gastrulae to be 3.7 and 6.5 ng protein h(-1), respectively. These findings support the conclusion that the high rates of biosynthesis previously reported for the Antarctic sea urchin are an outcome of high ribosomal activities.
- Published
- 2010
16. Developmental physiology of Antarctic asteroids with different life-history modes
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Donal T. Manahan and David W. Ginsburg
- Subjects
Larva ,Low protein ,Ecology ,Context (language use) ,Aquatic Science ,Biology ,biology.organism_classification ,Sedimentary depositional environment ,Echinoderm ,Botany ,Respiration ,Temperate climate ,Biological dispersal ,Ecology, Evolution, Behavior and Systematics - Abstract
Rates of respiration and protein synthesis were measured during embryonic and larval development of Antarctic asteroids with different life-history modes (non-feeding and feeding larvae: Acodontaster hodgsoni, Porania antarctica, Odontaster meridionalis). Patterns of respiration for these species all show an increase during embryogenesis, with subsequent maintenance of routine respiration (“starvation resistance”), even in the absence of food for ~4 months (O. meridionalis). Fractional rates of protein synthesis (i.e., rate per unit mass of whole-body protein content) in the Antarctic larvae are essentially identical to those of temperate species. Larvae of O. meridionalis had an average fractional synthesis rate of 0.52% ± 0.05 h−1 at −1.0°C, which is comparable to the temperate asteroid Asterina miniata at 0.53% ± 0.14 h−1 at 15°C. For embryos of the asteroids A. hodgsoni and P. antarctica, fractional rates of protein synthesis (~0.2% h−1) also are comparable to those reported for embryos of temperate echinoderm species. While rates of synthesis are high, rates of protein deposition are relatively low (percent of protein synthesized that is retained for growth). During a ~4 month growth period for larvae of O. meridionalis, the average protein depositional efficiency was 5.2%. This contrasts with higher rates of depositional efficiency reported for similar developmental stages of temperate echinoderm species. The biological significance of maintaining high rates of macromolecular synthesis for species with low rates of cell division and low protein depositional efficiencies is intriguing in the context of understanding the mechanistic bases of extended life spans and dispersal potential in response to changing Antarctic environments.
- Published
- 2009
17. Efficiencies and costs of larval growth in different food environments (Asteroidea: Asterina miniata)
- Author
-
Douglas A. Pace and Donal T. Manahan
- Subjects
Biomass (ecology) ,Larva ,Ecology ,fungi ,Energetics ,Energy balance ,Aquatic Science ,Biology ,biology.organism_classification ,Metabolic efficiency ,Animal science ,Echinoderm ,Protein biosynthesis ,Asterina miniata ,Ecology, Evolution, Behavior and Systematics - Abstract
The ocean is a nutritionally heterogeneous environment. For feeding larval forms, food variability has significant consequences for growth and later recruitment success. In this study, the physiological and biochemical responses to a range of different food concentrations (unfed, 4, 20, and 40 algal cells μl− 1) were examined in larvae of the asteroid, Asterina miniata. Measurements of growth, protein synthesis rates, and the energetic cost of protein synthesis were made. Under conditions of rapid growth, protein comprised a larger percent (66%) of a larva's organic biomass compared to similar-aged, slower-growing larvae (26%). Larvae fed at the highest food concentration tested (40 algal cells μl− 1) had a protein depositional efficiency of 80% (± 16%), a value 3-fold higher than larvae fed 20 algal cells μl− 1 (28% ± 11%). Also, faster-growing larvae required 3-fold less energy per unit mass of protein growth. Larvae fed 40 algal cells μl− 1 deposited protein at a respiratory cost of 65 ± 11 pmol O2 h− 1 (μg protein)− 1; larvae fed 20 algal cells μl− 1 had a cost of 192 ± 47 pmol O2 h− 1 (μg protein)− 1. While there were differences in the cost to deposit protein (i.e., protein growth, the balance of synthesis and degradation), there were no differences in the energetic cost of protein synthesis for all food concentrations tested. The energetic cost of protein synthesis was fixed at 13.8 (± 0.92) Joules (mg protein synthesized)− 1 and was independent of developmental stage, growth rates, and large changes (58-fold) in protein synthesis rates. A major conclusion from this study is that larvae grown in high-food environments not only grew faster, but did so for considerably less energy. Defining the complex relationships of food availability and metabolic efficiency will provide more accurate predictions of larval growth under variable food conditions in the ocean.
- Published
- 2007
18. Variation among females in egg lipid content and developmental success of echinoderms from McMurdo Sound, Antarctica
- Author
-
Michael S. Moore and Donal T. Manahan
- Subjects
Herbivore ,geography ,geography.geographical_feature_category ,biology ,Ecology ,Embryo ,Blastula ,biology.organism_classification ,biology.animal ,Lipid content ,embryonic structures ,Sterechinus neumayeri ,Omnivore ,General Agricultural and Biological Sciences ,Sea urchin ,Sound (geography) - Abstract
Egg lipid and protein content of different females of Antarctic echinoderms in McMurdo Sound, Antarctica, were measured to assess variation among females and developmental success. Egg triacylglycerol content of the Antarctic sea urchin Sterechinus neumayeri, when less than 70 ng, correlated with embryos that failed to develop past the 4-day-old blastula stage. In contrast asteroids (Odontaster meridionalis, O. validus, Acodontaster hodgsoni) all produced eggs that developed normally, even with variable egg lipid content. This difference might be related to dietary sources for more herbivorous sea urchins compared to more omnivorous and predatory asteroids. Low egg lipid content, with resulting poor embryonic survivorship, suggests that herbivorous sea urchins may be under unusual levels of nutritional stress in McMurdo Sound during the time frame studied (2004–2005). This nutritional stress might be related to the presence of large icebergs, known to have reduced primary production in the Ross Sea area.
- Published
- 2007
19. Food availability and physiological state of sea urchin larvae (Strongylocentrotus purpuratus)
- Author
-
A. J. Green, Donal T. Manahan, Eli Meyer, and Michael S. Moore
- Subjects
animal structures ,Ecology ,Physiological condition ,fungi ,Marine invertebrates ,Aquatic Science ,Biology ,biology.organism_classification ,Strongylocentrotus purpuratus ,Nutrient ,Biochemistry ,biology.animal ,parasitic diseases ,Respiration ,Glycine ,biology.protein ,Citrate synthase ,Sea urchin ,Ecology, Evolution, Behavior and Systematics - Abstract
Food availability is highly variable in the ocean. Many species of marine invertebrates have a larval form that depends upon exogenous nutrients for growth, yet there are few biochemical and physiological indices for determining changes in the nutritional status of larvae. In this study, the effects of food availability on biochemical compositions and metabolic processes of larvae of the sea urchin, Strongylocentrotus purpuratus, were determined. Larvae were cultured under different food concentrations (fed-to-excess and unfed) and a suite of biological processes assayed, ranging from measurements at the level of the whole organism to that of specific molecules. These data were normalized to DNA content (an index of cell number) to allow comparisons of physiological rates in larvae of different sizes. Changes in the following were measured during larval growth: free amino acid pool, protein, lipid classes (cholesterol, free fatty acids, hydrocarbons, phospholipids, triacylglycerol), enzyme activities (Na+, K+-ATPase and citrate synthase), and respiration rates. In growing larvae, the two key components that showed differential cell-specific content relative to unfed larvae were glycine in the free amino acid pool and phospholipids. Additionally, several lipid classes were detectable only in fed larvae (cholesterols, free fatty acids, and hydrocarbons). While triacylglycerols were present in eggs and utilized during pre-feeding development, they were not re-accumulated at detectable levels in feeding larvae. Respiration rates, protein content, and enzyme activities were all similar on a cell-specific basis, showing that these variables did not provide useful indices of differences in physiological state between fed and unfed larvae. In contrast, measurements of the cell-specific content of glycine and certain lipid classes did provide useful indices of physiological state of larvae. Application of these indices could potentially allow for determinations of nutritional state of larvae in the ocean.
- Published
- 2007
20. Transcriptomic analysis of growth heterosis in larval Pacific oysters ( Crassostrea gigas )
- Author
-
Donal T. Manahan, Christian D. Haudenschild, Shannon Decola, Dennis Hedgecock, Ben Bowen, Eli Meyer, and Jing-Zhong Lin
- Subjects
Ribosomal Proteins ,Genetics ,Candidate gene ,Genome ,Multidisciplinary ,biology ,Heterosis ,Reciprocal cross ,Molecular Sequence Data ,Growth ,Biological Sciences ,Pacific oyster ,biology.organism_classification ,Massively parallel signature sequencing ,Gene Expression Regulation ,Larva ,Hybrid Vigor ,Animals ,Crassostrea ,RNA, Messenger ,Underdominance ,Hybrid - Abstract
Compared with understanding of biological shape and form, knowledge is sparse regarding what regulates growth and body size of a species. For example, the genetic and physiological causes of heterosis (hybrid vigor) have remained elusive for nearly a century. Here, we investigate gene-expression patterns underlying growth heterosis in the Pacific oyster ( Crassostrea gigas ) in two partially inbred ( f = 0.375) and two hybrid larval populations produced by a reciprocal cross between the two inbred families. We cloned cDNA and generated 4.5 M sequence tags with massively parallel signature sequencing. The sequences contain 23,274 distinct signatures that are expressed at statistically nonzero levels and show a highly positively skewed distribution with median and modal counts of 9.25 million and 3 transcripts per million, respectively. For nearly half of these signatures, expression level depends on genotype and is predominantly nonadditive (hybrids deviate from the inbred average). Statistical contrasts suggest ≈350 candidate genes for growth heterosis that exhibit concordant nonadditive expression in reciprocal hybrids; this represents only ≈1.5% of the >20,000 transcripts. Patterns of gene expression, which include dominance for low expression and even underdominance of expression, are more complex than predicted from classical dominant or overdominant explanations of heterosis. Preliminary identification of ribosomal proteins among candidate genes supports the suggestion from previous studies that efficiency of protein metabolism plays a role in growth heterosis.
- Published
- 2007
21. Genetically Determined Variation in Developmental Physiology of Bivalve Larvae (Crassostrea gigas)
- Author
-
T.-C. Francis Pan, Scott L. Applebaum, and Donal T. Manahan
- Subjects
Genetics ,Genome ,biology ,Physiology ,Ecology ,Gene Expression Profiling ,Glycine ,Genetic Variation ,Pacific oyster ,biology.organism_classification ,Biochemistry ,Protein Transport ,Larva ,Genetic variation ,Gene expression ,Gene family ,Crassostrea ,Animals ,Animal Science and Zoology ,Amino acid transporter ,Gene ,Crosses, Genetic - Abstract
Understanding the complex interactions that regulate growth and form is a central question in developmental physiology. We used experimental crosses of pedigreed lines of the Pacific oyster, Crassostrea gigas, to investigate genetically determined variations in larval growth and nutrient transport. We show that (i) transport rates at 10 and 100 μM glycine scale differentially with size; (ii) size-specific maximum transport capacity (Jmax) is genetically determined; and (iii) Jmax serves as an early predictive index of subsequent growth rate. This relationship between genetically determined Jmax and growth suggests the potential use of transporter genes as biomarkers of growth potential. Analysis of the genome of C. gigas revealed 23 putative amino acid transporter genes. The complexity of gene families that underpin physiological traits has additional precedents in this species and others and warrants caution in the use of gene expression as a biomarker for physiological state. Direct in vivo measurements of physiological processes using species with defined genotypes are required to understand genetically determined variance of nutrient flux and other processes that regulate development and growth.
- Published
- 2015
22. Physiological bases of genetically determined variation in growth of marine invertebrate larvae: A study of growth heterosis in the bivalve Crassostrea gigas
- Author
-
Donal T. Manahan, Patrick K. K. Leong, Dennis Hedgecock, Douglas A. Pace, Adam G. Marsh, and Allison J. Green
- Subjects
Larva ,Oyster ,biology ,Ecology ,fungi ,Marine invertebrates ,Aquatic Science ,Plankton ,Pacific oyster ,biology.organism_classification ,biology.animal ,Crassostrea ,Growth rate ,Mollusca ,Ecology, Evolution, Behavior and Systematics - Abstract
Many species of marine animals have larval stages whose rates of growth in the plankton are regulated by complex combinations of biological and environmental factors. In this study, we focus on the physiological bases that underlie endogenous variation in growth potential of larvae. Our approach was based on experimental crosses of gravid adults from pedigreed families of the Pacific oyster, Crassostrea gigas. This produced large numbers of larvae with different growth rates when reared under similar environmental conditions of food and temperature. A total of 35 larval families were reared to test hypotheses regarding the physiological bases of growth variation. Growth rate of these larval families varied over a five-fold range, from 3.4 (± 0.5, S.E.) to 17.6 (± 0.6) μm day− 1. The suite of integrated measurements applied to study growth variation included size, biochemical compositions, rates of particulate and dissolved nutrient acquisition, absorption efficiencies, respiration rates and enzyme activities. We show that a complex set of physiological processes regulated differences in genetically determined growth rates of larvae. One-half of the energy required for faster growth came from an enhanced, size-specific feeding ability. Differences in absorption rates were not significant for slow- and fast-growing larvae, nor were differences in size-specific respiration rates. Metabolic processes accounted for the additional 50% of the energy “savings” required to explain enhanced growth rates. We propose that different protein depositional efficiencies could account for this energy saving. Quantitative analyses of the endogenous physiological factors that cause variation in growth rate will allow for a more sophisticated understanding of growth, survival and recruitment potential of larvae.
- Published
- 2006
23. Physiological recovery from prolonged ‘starvation’ in larvae of the Pacific oyster Crassostrea gigas
- Author
-
Amy L. Moran and Donal T. Manahan
- Subjects
Starvation ,Oyster ,Larva ,animal structures ,genetic structures ,biology ,Ecology ,fungi ,Zoology ,Veliger ,Aquatic Science ,Pacific oyster ,biology.organism_classification ,Bivalvia ,biology.animal ,parasitic diseases ,medicine ,Crassostrea ,medicine.symptom ,human activities ,Mollusca ,Ecology, Evolution, Behavior and Systematics - Abstract
Previous studies of energy metabolism in larvae have described a developmental “point of no return” (PNR), a time by which larvae of planktotrophic marine species must feed in order to survive and grow. This study investigated the effects of long-term food deprivation on developing larvae of the oyster Crassostrea gigas with the goal of providing a biochemical and metabolic description of larvae at the PNR in this species. Mortality of unfed larvae was low for the first 14 days without the addition of phytoplankton foods. Even after 33 days without food, larvae were still swimming. Unfed larvae did not lose their ability to capture and digest algal cells when provided with food after 33 days. Growth, metabolic rate and biochemical constituents all increased at the same or greater rates in larvae whose feeding was delayed for 5, 8, 11, 14 or 17 days compared to larvae fed at 2 days old, when feeding was possible. These results show that larvae of C . gigas can survive long feeding delays while maintaining a constant rate of metabolism. These results suggest that oyster larvae have the capacity to survive ‘starvation’ using alternative sources of energy. If there is a “point of no return” beyond which larvae of C . gigas must feed on microalgae to survive, our findings suggest this point may be set by the availability of detrital material or dissolved organic carbon that can fuel maintenance metabolism for extended periods equivalent to over four times the predicted lifespan.
- Published
- 2004
24. Separating the nature and nurture of the allocation of energy in response to global change
- Author
-
T.-C. Francis Pan, Scott L. Applebaum, Donal T. Manahan, and Dennis Hedgecock
- Subjects
Research program ,education.field_of_study ,Aquatic Organisms ,Environmental change ,business.industry ,Ecology ,Energy (esotericism) ,Climate Change ,Systems Biology ,Environmental resource management ,Population ,Adaptation, Biological ,Global change ,Plant Science ,Biology ,Environmental stress ,Models, Biological ,Nature versus nurture ,Models, Animal ,Animals ,Animal Science and Zoology ,business ,education ,Energy Metabolism ,Grand Challenges - Abstract
Synopsis Understanding and predicting biological stability and change in the face of rapid anthropogenic modifications of ecosystems and geosystems are grand challenges facing environmental and life scientists. Physiologically, organisms withstand environmental stress through changes in biochemical regulation that maintain homeostasis, which necessarily demands tradeoffs in the use of metabolic energy. Evolutionarily, in response to environmentally forced energetic tradeoffs, populations adapt based on standing genetic variation in the ability of individual organisms to reallocate metabolic energy. Combined study of physiology and genetics, separating ‘‘Nature and Nurture,’’ is, thus, the key to understanding the potential for evolutionary adaptation to future global change. To understand biological responses to global change, we need experimentally tractable model species that have the well-developed physiological, genetic, and genomic resources necessary for partitioning variance in the allocation of metabolic energy into its causal components. Model species allow for discovery and for experimental manipulation of relevant phenotypic contrasts and enable a systems-biology approach that integrates multiple levels of analyses to map genotypic-to-phenotypic variation. Here, we illustrate how combined physiological and genetic studies that focus on energy metabolism in developmental stages of a model marine organism contribute to an understanding of the potential to adapt to environmental change. This integrative research program provides insights that can be readily incorporated into individual-based ecological models of population persistence under global change.
- Published
- 2014
25. Larval dispersal potential of the tubeworm Riftia pachyptila at deep-sea hydrothermal vents
- Author
-
Donal T. Manahan, Craig M. Young, Lauren S. Mullineaux, and Adam G. Marsh
- Subjects
Pachyptila ,geography ,Larva ,Multidisciplinary ,geography.geographical_feature_category ,biology ,Siboglinidae ,Ecology ,Reproduction ,Fauna ,Ephemeral key ,fungi ,biology.organism_classification ,Invertebrates ,Oceanography ,Volcano ,Animals ,Biological dispersal ,Seawater ,Hydrothermal vent - Abstract
Hydrothermal vents are ephemeral because of frequent volcanic and tectonic activities associated with crust formation. Although the larvae of hydrothermal vent fauna can rapidly colonize new vent sites separated by tens to hundreds of kilometres, the mechanisms by which these larvae disperse and recruit are not understood. Here we integrate physiological, developmental and hydrodynamic data to estimate the dispersal potential of larvae of the giant tubeworm Riftia pachyptila. At in situ temperatures and pressures (2 degrees C and 250 atm), we estimate that the metabolic lifespan for a larva of R. pachyptila averages 38 days. In the measured flow regime at a fast-spreading ridge axis (9 degrees 50' N; East Pacific Rise), this lifespan results in potential along-ridge dispersal distances that rarely exceed 100 km. This limited dispersal results not from the physiological performance of the embryos and larvae, but instead from transport limitations imposed by periodic reversals in along-ridge flows and sustained episodes of across-ridge flow. The lifespan presented for these larvae can now be used to predict dispersal under current regimes at other hydrothermal vent sites.
- Published
- 2001
26. Metabolic differences between 'demersal' and 'pelagic' development of the Antarctic sea urchin Sterechinus neumayeri
- Author
-
Donal T. Manahan and Adam G. Marsh
- Subjects
Ecology ,Hatching ,Energetics ,Pelagic zone ,Aquatic Science ,Biology ,biology.organism_classification ,Demersal zone ,Animal science ,Water column ,Dry weight ,biology.animal ,embryonic structures ,Sterechinus neumayeri ,Sea urchin ,Ecology, Evolution, Behavior and Systematics - Abstract
Early development of the Antarctic sea urchin Sterechinus neumayeri was examined under two differ-ent culture regimes: one to simulate development near-bottom (“demersal development”) and the other to simulate the development of embryos in the water column (“pelagic development”). When embryos of both treatments reached the hatching blastula stage at 5 d post-fertilization (−1.5 °C), the blastulae that had undergone demersal development evidenced significant differences (by ANOVA or suitable non-parametric comparison) in the following: a thicker blastoderm layer (12%, P < 0.001), higher ash-free dry weights (19%, P < 0.01), lower mass-specific respiration rates (50%, P < 0.001), higher incorporation rates of 35S-methionine into protein (23%, P < 0.003), and a differential pattern of protein synthesis. When embryos developed demersally, they remained in the jelly-coat material released with the eggs at spawning. Quantitative isolation of this jelly-coat material in S. neumayeri demonstrated that it contained a significant amount of organic matter, 115 ng ash-free dry mass per egg, equivalent to 17% of the egg's initial organic mass. Uptake of external nutrients during embryogenesis may be a significant component of the physiological energetics of this polar invertebrate by allowing the utilization of jelly-coat material released by a female during spawning.
- Published
- 2000
27. Energy metabolism during embryonic development and larval growth of an Antarctic sea urchin
- Author
-
Adam G. Marsh, Patrick K. K. Leong, and Donal T. Manahan
- Subjects
Larva ,biology ,Respiratory rate ,Physiology ,Ecology ,Ontogeny ,fungi ,Energetics ,Embryogenesis ,Zoology ,Aquatic Science ,biology.organism_classification ,Sea Urchins ,Insect Science ,biology.animal ,biology.protein ,Animals ,Citrate synthase ,Sterechinus neumayeri ,Animal Science and Zoology ,Energy Metabolism ,Molecular Biology ,Sea urchin ,Ecology, Evolution, Behavior and Systematics - Abstract
Developmental energetics of an Antarctic sea urchin, Sterechinus neumayeri, were quantified to describe the physiological bases underlying ontogenetic changes in metabolic rate at extreme cold temperatures (−1.5 °C). Rates of development from a four-arm to a six-arm larval stage were not affected by food availability. The respiratory cost of development to the six-arm larval stage (day 60) was 14.0 mJ for fed larvae and 8.2 mJ for unfed larvae. We observed three phases of metabolic regulation during development. During embryogenesis (day 0–22), increasing metabolic rates were proportional to increases in cell numbers. During early larval development (day 22–47), the differences in respiratory rate between fed and unfed larvae were not accounted for by cell number, but by cell-specific metabolic rate (respiratory rate normalized to DNA content). Once an advanced larval stage had been reached (day 47–60), cell-specific respiratory rate and mitochondrial densities (citrate synthase activity normalized to DNA content) were more equivalent between fed and unfed larvae, suggesting that size-specific metabolic rates were determined at a level of physiological regulation that was independent of cell numbers or feeding history.
- Published
- 1999
28. Protein Metabolism in Lecithotrophic Larvae (Gastropoda: Haliotis rufescens)
- Author
-
Jay Vavra and Donal T. Manahan
- Subjects
food.ingredient ,Abalone ,Haliotis rufescens ,fungi ,Protein metabolism ,Protein turnover ,Veliger ,Biology ,biology.organism_classification ,chemistry.chemical_compound ,food ,chemistry ,Biochemistry ,Trochophore ,Protein biosynthesis ,Haliotis ,General Agricultural and Biological Sciences - Abstract
Rates of protein depletion, synthesis, and turn- over were measured in larvae of the abalone Haliotis rufe- scens as an approach to understanding macromolecular me- tabolism during lecithotrophic development. Protein content decreased linearly during development to metamorphic competence, with 34% of the initial protein in eggs depleted during the &day larval life span. Fractional rates of protein synthesis (percentage of total body-protein synthesized per day) decreased during development, from 40% (1 -day-old trochophore larva) to 14% (7-day-old veliger larva). Sepa- ration of proteins by one-dimensional gel electrophoresis showed that protein pools in larvae are dominated by two high-molecular-weight protein classes (88 and 121 kDa). When the proteins of l- and 3-day-old larvae were labeled with a mixture of '?S-methionine and cysteine, the pattern on two-dimensional gels showed that the turnover process (protein synthesis and degradation) involved hundreds of different proteins. The energy gained from loss of protein could account for 20% of the protein turnover rates for trochophore larvae and 79% of the lower turnover costs for late-stage veligers. Lecithotrophic larvae of H. rufescens maintained high biosynthetic activities, with up to 40% of their whole-body protein being turned over each day. Such dynamic processes during development of nonfeeding lar- vae would contribute significantly to maintenance metabo- lism.
- Published
- 1999
29. A method for accurate measurements of the respiration rates of marine invertebrate embryos and larvae
- Author
-
Adam G. Marsh and Donal T. Manahan
- Subjects
Biochemical oxygen demand ,animal structures ,Ecology ,biology ,fungi ,chemistry.chemical_element ,Aquatic Science ,biology.organism_classification ,Oxygen ,Strongylocentrotus purpuratus ,Oxygen tension ,Respirometry ,Animal science ,chemistry ,embryonic structures ,Respiration ,Sterechinus neumayeri ,Seawater ,Ecology, Evolution, Behavior and Systematics - Abstract
Measurements of respiration rates are essential to quantify the energy requirements of embryos and larvae. Here we describe a ')_rBOD' method that employs small (~1 ml) Biological Oxygen Demand (BOD) glass vials in which embryos and larvae are incubated. A decrease in oxygen concen- tration is measured by injecting seawater from each vial into the measurement chamber of a standard polarographic oxygen sensor. This pBOD method was used to measure respiration rates of larvae of the sea urchin Strongylocentrotus purpuratus (at 15°C) and embryos and larvae of 2 Antarctic echino- derms, the sea urchin Sterecbinus neumayeri and the seastar Odontasfer valiclus (both at -1S"C). For validation, a comparison of different methods was performed with embryos and larvae of S. neumayeri. The nBOD method gave results for respiration rates during development that were equivalent to those obtained with either coulometric capacitance respirometry or standard Winkler's titrations of large (300 ml) BOD bottles. Currently, the most common method for measuring respiration rates of inverte- brate embryos and larvae is to place them in small respiration chambers and continuously monitor oxygen tension with a polarographic oxygen sensor (POS). However, respiration rates for embryos and larvae of S. neumayeri were underestimated when standard POS measurements were compared to the measurements made with either pBOD, Winkler's titrations or coulometric capacitance respirometry. A comparison of the pBOD and POS methods during early development in S. neumayeri resulted in different estimates of 920 and 343 pJ, respectively, for the total energetic cost of embryogenesis to gastrulation, illustrating that the POS error can be as great as 63 %. The yBOD method is accurate for micro-respiration measurements of invertebrate embryos and larvae as well as being simple to operate and appropriate for field work.
- Published
- 1999
30. METABOLIC IMPORTANCE OF Na+/K+-ATPase ACTIVITY DURING SEA URCHIN DEVELOPMENT
- Author
-
Donal T. Manahan and P. K. K. Leong
- Subjects
biology ,urogenital system ,Physiology ,Monensin ,Stimulation ,Metabolism ,Aquatic Science ,biology.organism_classification ,Strongylocentrotus purpuratus ,Enzyme assay ,chemistry.chemical_compound ,chemistry ,Biochemistry ,In vivo ,Insect Science ,biology.animal ,embryonic structures ,biology.protein ,Animal Science and Zoology ,Molecular Biology ,Sea urchin ,Ecology, Evolution, Behavior and Systematics ,Intracellular - Abstract
Early stages of animal development have high mass-specific rates of metabolism. The biochemical processes that establish metabolic rate and how these processes change during development are not understood. In this study, changes in Na+/K+-ATPase activity (the sodium pump) and rate of oxygen consumption were measured during embryonic and early larval development for two species of sea urchin, Strongylocentrotus purpuratus and Lytechinus pictus. Total (in vitro) Na+/K+-ATPase activity increased during development and could potentially account for up to 77 % of larval oxygen consumption in Strongylocentrotus purpuratus (pluteus stage) and 80 % in Lytechinus pictus (prism stage). The critical issue was addressed of what percentage of total enzyme activity is physiologically active in living embryos and larvae and thus what percentage of metabolism is established by the activity of the sodium pump during development. Early developmental stages of sea urchins are ideal for understanding the in vivo metabolic importance of Na+/K+-ATPase because of their small size and high permeability to radioactive tracers (86Rb+) added to sea water. A comparison of total and in vivo Na+/K+-ATPase activities revealed that approximately half of the total activity was utilized in vivo. The remainder represented a functionally active reserve that was subject to regulation, as verified by stimulation of in vivo Na+/K+-ATPase activity in the presence of the ionophore monensin. In the presence of monensin, in vivo Na+/K+-ATPase activities in embryos of S. purpuratus increased to 94 % of the maximum enzyme activity measured in vitro. Stimulation of in vivo Na+/K+-ATPase activity was also observed in the presence of dissolved alanine, presumably due to the requirement to remove the additional intracellular Na+ that was cotransported with alanine from sea water. The metabolic cost of maintaining the ionic balance was found to be high, with this process alone accounting for 40 % of the metabolic rate of sea urchin larvae (based on the measured fraction of total Na+/K+-ATPase that is physiologically active in larvae of S. purpuratus). Ontogenetic changes in pump activity and environmentally induced regulation of reserve Na+/K+-ATPase activity are important factors that determine a major proportion of the metabolic costs of sea urchin development.
- Published
- 1997
31. Quantitative and molecular genetic analyses of heterosis in bivalve molluscs
- Author
-
Daniel J. McGoldrick, Donal T. Manahan, Nicholas Appelmans, Dennis Hedgecock, B. L. Bayne, and Jay Vavra
- Subjects
Genetics ,Inbred strain ,Heterosis ,Evolutionary biology ,Backcrossing ,Epistasis ,Juvenile ,Aquatic Science ,Quantitative trait locus ,Biology ,Ecology, Evolution, Behavior and Systematics ,Nuclear DNA ,Hybrid - Abstract
Associations of allozyme-heterozygosity with growth and its physiological underpinnings have been well documented for bivalve molluscs. The associations are correlational, however, derived almost entirely from studies of wild-caught juveniles or adults. Such studies cannot resolve alternative genetic explanations of heterosis. Four experimental approaches have recently been made to this problem; (1) a correlational study contrasting allozyme and presumably selectively neutral nuclear DNA polymorphisms; (2) detailed studies of allozyme inheritance in families; (3) a study contrasting the performance of meiosis-I and meiosis-II triploids with diploids and (4) a classical quantitative genetic study of the performance of hybrids produced by crosses among inbred lines. The last approach has uncovered remarkable heterosis in growth and its physiological components, both for the larval and juvenile or adult stages, and has implicated epistasis as a significant cause of this heterosis. More importantly, this approach now permits dissection of heterosis into quantitative trait loci (QTL) mapped by the co-segregation of allozyme and nuclear DNA markers with growth phenotypes in the F2 hybrid and backcross generations.
- Published
- 1996
32. Energy Metabolism and Amino Acid Transport During Early Development of Antarctic and Temperate Echinoderms
- Author
-
Fraser Shilling and Donal T. Manahan
- Subjects
Biomass (ecology) ,Alanine transport ,Larva ,animal structures ,biology ,Marine larval ecology ,fungi ,Odontaster validus ,biology.organism_classification ,Nutrient ,Botany ,Sterechinus neumayeri ,General Agricultural and Biological Sciences ,Energy source - Abstract
The rates of oxygen consumption by embryos of antarctic echinoderms (Acodontaster hodgsoni, Odontaster validus, Psilaster charcoti, and Sterechinus neumayeri) were compared to the biomas (ash-free dry organic weight) of the egg of each species. These species could survive for months to years (range: 10 months to 5 years) by relying solely on the reserves present in the egg. However, certain species did not use any of the egg's reserves during early development. Embryonic stages of O. validus (a species with planktotrophic larvae) did not decrease in lipid, protein, or total biomass during the first 35 days of development. During the first 42 days of development, embryos of A. hodgsoni (a species with lecithotrophic development) used protein as an energy source. For both species lipid composed 40 to 50% of egg biomass, but was not used as an energy reserve. Larvae of O. validus have a high-affinity transport system for amino acids dissolved in seawater (K1 = 1.3 {mu}M for alanine). The rate of alanine transport from a low concentration (50 nM) could supply 32% of the larva's metabolic needs. This is a 10-fold higher input to metabolism than was determined (3% at 50 nM) for larvae of a temperate asteroid, Asterina miniata. Larvae of antarctic echinoderms live in an environment where the food supply is low for most of the year. Relative to their metabolic rates, antarctic larvae have larger energy stores and planktotrophic larvae have higher nutrient transport capacities when compared to larvae from temperate regions. These physiological differences allow antarctic larvae to survive for long periods without particulate food.
- Published
- 1994
33. High Macromolecular Synthesis with Low Metabolic Cost in Antarctic Sea Urchin Embryos
- Author
-
Robert E. Maxson, Adam G. Marsh, and Donal T. Manahan
- Subjects
Embryo, Nonmammalian ,Antarctic Regions ,Oxygen Consumption ,biology.animal ,Animals ,Extreme environment ,Sterechinus neumayeri ,RNA, Messenger ,Sea urchin ,Multidisciplinary ,biology ,Ecology ,Temperature ,Protein turnover ,Proteins ,RNA ,Metabolism ,Sea urchin embryo ,biology.organism_classification ,Cold Temperature ,Kinetics ,Blastocyst ,Biochemistry ,Protein Biosynthesis ,Sea Urchins ,Energy Metabolism ,Half-Life ,Macromolecule - Abstract
Assessing the energy costs of development in extreme environments is important for understanding how organisms can exist at the margins of the biosphere. Macromolecular turnover rates of RNA and protein were measured at –1.5°C during early development of an Antarctic sea urchin. Contrary to expectations of low synthesis with low metabolism at low temperatures, protein and RNA synthesis rates exhibited temperature compensation and were equivalent to rates in temperate sea urchin embryos. High protein metabolism with a low metabolic rate is energetically possible in this Antarctic sea urchin because the energy cost of protein turnover, 0.45 joules per milligram of protein, is 1/25th the values reported for other animals.
- Published
- 2001
34. Unequal and genotype-dependent expression of mitochondrial genes in larvae of the pacific oyster Crassostrea gigas
- Author
-
Eli Meyer, Jason P. Curole, Donal T. Manahan, and Dennis Hedgecock
- Subjects
Cloning ,Expressed sequence tag ,Mitochondrial DNA ,RNA, Untranslated ,Genotype ,Molecular Sequence Data ,Gene Expression ,Sequence Analysis, DNA ,Biology ,Pacific oyster ,biology.organism_classification ,Molecular biology ,DNA, Mitochondrial ,DNA sequencing ,Mitochondrial Proteins ,Genes, Mitochondrial ,Larva ,Gene expression ,Crassostrea ,Animals ,General Agricultural and Biological Sciences ,Gene ,Crosses, Genetic - Abstract
Mitochondria are essential for regulation of energy metabolism, but little is known about patterns of mitochondrial genome expression in invertebrates. To explore the association of mitochondrial expression with differential growth of Crassostrea gigas, the Pacific oyster, we crossed two inbred lines to produce inbred and hybrid larvae, which grew at different rates under the same environmental conditions. Using high-throughput cloning and sequencing methods, we identified 1.1 million expressed sequence tags from the mitochondrial genome, 96.7% of which were perfect matches to genes targeted by the method. Expression varied significantly among genes, ranging over nearly four orders of magnitude, from mt:lRNA, which constituted 21% of all transcripts, to mt:CoII, which constituted less than 0.02% of all transcripts. Variable expression of genes coding for subunits of macromolecular complexes (e.g., mt:CoI and mt:CoII) implies that stoichiometry in these complexes must be regulated post-transcriptionally. Surprisingly, the mitochondrial transcriptome contained non-coding transcripts, which may play a role in the regulation of mitochondrial function. Finally, mitochondrial expression depended strongly on maternal factors and nuclear-cytoplasmic interactions, which may explain previously observed growth differences between reciprocal hybrids. Differences in mitochondrial gene expression could provide a biochemical index for the metabolic basis of genetically determined differences in larval growth.
- Published
- 2010
35. Gene expression profiling of genetically determined growth variation in bivalve larvae (Crassostrea gigas)
- Author
-
Eli Meyer and Donal T. Manahan
- Subjects
Male ,Ribosomal Proteins ,Genotype ,Physiology ,Molecular Sequence Data ,Aquatic Science ,Biology ,Transcriptome ,Complementary DNA ,Animals ,Crassostrea ,Molecular Biology ,Gene ,Ecology, Evolution, Behavior and Systematics ,Crosses, Genetic ,Genetics ,Gene Expression Profiling ,RNA ,Gene Expression Regulation, Developmental ,biology.organism_classification ,Molecular biology ,Phenotype ,Gene expression profiling ,Insect Science ,GenBank ,Larva ,Animal Science and Zoology ,Female - Abstract
SUMMARY Growth rates in animals are governed by a wide range of biological factors, many of which remain poorly understood. To identify the genes that establish growth differences in bivalve larvae, we compared expression patterns in contrasting phenotypes (slow- and fast-growth) that were experimentally produced by genetic crosses of the Pacific oyster Crassostrea gigas. Based on transcriptomic profiling of 4.5 million cDNA sequence tags, we sequenced and annotated 181 cDNA clones identified by statistical analysis as candidates for differential growth. Significant matches were found in GenBank for 43% of clones (N=78), including 34 known genes. These sequences included genes involved in protein metabolism, energy metabolism and regulation of feeding activity. Ribosomal protein genes were predominant, comprising half of the 34 genes identified. Expression of ribosomal protein genes showed non-additive inheritance — i.e. expression in fast-growing hybrid larvae was different from average levels in inbred larvae from these parental families. The expression profiles of four ribosomal protein genes (RPL18, RPL31, RPL352 and RPS3) were validated by RNA blots using additional, independent crosses from the same families. Expression of RPL35 was monitored throughout early larval development, revealing that these expression patterns were established early in development (in 2-day-old larvae). Our findings (i) provide new insights into the mechanistic bases of growth and highlight genes not previously considered in growth regulation, (ii) support the general conclusion that genes involved in protein metabolism and feeding regulation are key regulators of growth, and (iii) provide a set of candidate biomarkers for predicting differential growth rates during animal development.
- Published
- 2010
36. Experimental manipulations of the organic compositions of seawater: implications for studies of energy budgets in marine invertebrate larvae
- Author
-
William B. Jaeckle and Donal T. Manahan
- Subjects
chemistry.chemical_classification ,animal structures ,biology ,Ecology ,Marine larval ecology ,fungi ,Energetics ,Veliger ,Aquatic Science ,Bivalvia ,biology.organism_classification ,Animal science ,chemistry ,Trochophore ,Organic matter ,Seawater ,Mollusca ,Ecology, Evolution, Behavior and Systematics - Abstract
Correct measurement of changes in biomass and metabolic rates over time are two essential elements for the accurate construction of energy budgets for invertebrate larvae. Both components of larval energetics are altered by changes in the organic chemistry of the seawater. Axenic (bacteria-free) veliger larvae (88 μm shell length) of the bivalve Crassostrea gigas (Thunberg, 1795) had a 53% enhancement of their metabolic rate relative to control values (5.8 ± 0.6 pmol larva −1 h −1 , x ± 1 se ) when exposed to seawater to which 1 μM glucose had been added. Gastrulae, prism-stage, and pluteus-stage, larvae of the sea urchin Lytechinus pictus (Verrill, 1867) had significantly higher metabolic rates when 1 μM amino acids (16 amino acids at 62.5 nM each) was added to seawater. Gastrulae increased their rate of respiration by 35%, from 10 ± 0.9 to 13.5 ± 1.4 pmol O2 embryo−1 h−; prism-stage larvae by 33% from 40.9 ± 2.0 to 54.4 ± 2.8; and pluteus-stage larvae by 50%, from 33.4 ± 1.5 to 50.3 ± 3.1. Lecithotrophic larvaei of the gastropod Haliotis rufescens Swainson, 1822, either had no change (Day 1, trochophore larvae) or a significant increase (Day 2, veliger larvae) in dry organic weight when reared in natural seawater that had been passed through a filter of 0.2-μm pore size (to remove particles). In contrast, sibling larvae always decreased in dry organic weight when reared in seawater which had first been passed through a sand-filter (a treatment that alters the organic chemistry of seawater), and then a 0.2-μm (pore size) filter. These data show that alterations of the organic chemistry of seawater can affect the growth and metabolism of invertebrate larvae. If such modifications are not controlled, energy budgets constructed from laboratory experiments on larvae in altered seawater may bear little resemblance to the energetics of larvae in the field.
- Published
- 1992
37. Nutrient uptake by marine invertebrates: cloning and functional analysis of amino acid transporter genes in developing sea urchins (Strongylocentrotus purpuratus)
- Author
-
Donal T. Manahan and Eli Meyer
- Subjects
animal structures ,Amino Acid Transport Systems ,Molecular Sequence Data ,Gene Expression ,biology.animal ,Animals ,Amino acid transporter ,Cloning, Molecular ,Sea urchin ,Gene ,Strongylocentrotus purpuratus ,Phylogeny ,Alanine ,chemistry.chemical_classification ,Alanine transport ,biology ,Sequence Homology, Amino Acid ,Gene Expression Profiling ,Gene Expression Regulation, Developmental ,Marine invertebrates ,Sequence Analysis, DNA ,biology.organism_classification ,Amino acid ,Biochemistry ,chemistry ,embryonic structures ,Oocytes ,General Agricultural and Biological Sciences - Abstract
Transport of amino acids from low concentrations in seawater by marine invertebrates has been extensively studied, but few of the genes involved in this physiological process have been identified. We have characterized three amino acid transporter genes cloned from embryos of the sea urchin Strongylocentrotus purpuratus. These genes show phylogenetic proximity to classical amino acid transport systems, including Gly and B0+, and the inebriated gene (INE). Heterologous expression of these genes in frog oocytes induced a 40-fold increase in alanine transport above endogenous levels, demonstrating that these genes mediate alanine transport. Antibodies specific to one of these genes (Sp-AT1) inhibited alanine transport, confirming the physiological activity of this gene in larvae. Whole-mount antibody staining of larvae revealed expression of Sp-AT1 in the ectodermal tissues associated with amino acid transport, as independently demonstrated by autoradiographic localization of radioactive alanine. Maximum rates of alanine transport increased 6-fold during early development, from embryonic to larval stages. Analysis of gene expression during this developmental period revealed that Sp-AT1 transcript abundance remained nearly constant, while that of another transporter gene (Sp-AT2) increased 11-fold. The functional characterization of these genes establishes a molecular biological basis for amino acid transport by developmental stages of marine invertebrates.
- Published
- 2009
38. Energetics of early development for the sea urchinsStrongylocentrotus purpuratus andLytechinus pictus and the crustaceanArtemia sp
- Author
-
Fraser Shilling and Donal T. Manahan
- Subjects
Ecology ,biology ,urogenital system ,Energetics ,Zoology ,Branchiopoda ,Artificial seawater ,Aquatic Science ,biology.organism_classification ,Strongylocentrotus purpuratus ,Crustacean ,biology.animal ,embryonic structures ,Dissolved organic carbon ,Seawater ,Sea urchin ,Ecology, Evolution, Behavior and Systematics - Abstract
Embryos and larvae of two species of sea urchin,Strongylocentrotus purpuratus andLytechinus pictus, and larvae of the brine shrimpArtemia sp. (San Francisco brand) were cultured to investigate the contribution of dissolved organic material in seawater to the energetics of early development. When embroys ofS. purpuratus were reared in artificial seawater, a net loss in dry organic mass was observed. In contrast, when sibling embryos were reared to Day 2 under identical conditions in natural seawater, there was either a net increase in dry organic mass or no change. A net decrease in mass was observed in only one of five cultures reared in filtered natural seawater. Energy budgets for each species were determined by giving energy equivalents to the changes in carbohydrate, lipid and protein, and to the rate of oxygen consumption for each day of development. In the case ofS. purpuratus, the use of endogenous reserves accounted for either 0 or 38% of the metabolic demand for two independent cultures reared from Days 0 to 2. For larvae ofL. pictus, reared to 8 d, only 66% of the metabolic demand could be accounted for by the use of endogenous reserves. Sea urchins are capable of transporting dissolved organic material from seawater. Calculations revealed that the energy deficit during the early development of sea urchins (S. purpuratus) could be accounted for by the uptake of dissolved organic matter from seawater. However, for a species that cannot use this resource (Artemia sp.), the metabolic needs during development are supplied through the use of endogenous reserves.
- Published
- 1990
39. Adaptations by Invertebrate Larvae for Nutrient Acquisition from Seawater
- Author
-
Donal T. Manahan
- Subjects
Alanine transport ,biology ,fungi ,Biomass ,Marine invertebrates ,biology.organism_classification ,Nutrient ,Botany ,General Earth and Planetary Sciences ,Seawater ,Axenic ,Energy source ,General Environmental Science ,Invertebrate - Abstract
Unlike life on land, animals that live in seawater are surrounded by a medium that contains organic nutrients in dilute solution. Larval forms of soft-bodied marine invertebrates are adapted to take advantage of the fact that most of the organic carbon in their environment is in solution as dissolved organic material (DOM). New evidence for the importance of DOM to metazoans is presented by showing that larval forms can increase in biomass, even in the absence of paniculate foods. Such increases occurred only in those species capable of transporting DOM. The physiological basis for using DOM as an energy source is dependent upon an increased transport capacity for DOM as growth proceeds. Using bivalve larvae, mass coefficients and exponents were determined for (i) alanine transport rates and (ii) metabolic rates. These coefficients were not statistically different when determined over the life span of a larva. Thus, as growth proceeds, these larvae increase their ability to obtain a potential supply of metabolic fuel (DOM) in direct proportion to the increase in their metabolic demand. The percent of this increased transport capacity that larvae could actually utilize in nature will depend upon the substrate concentrations in their environment. Current views on what these concentrations are in seawater may be altered as more attention is given to the fine scale distributions of organic chemicals in the ocean. After DOM has been transported by the animal, its metabolic fate can now be rigorously studied using bacteria-free larvae. Measurements of amino acid synthesis in larvae cultured under axenic conditions suggest that a much greater plasticity may exist in the biochemical requirements of larvae for dietary amino acids.
- Published
- 1990
40. Cost of protein synthesis and energy allocation during development of antarctic sea urchin embryos and larvae
- Author
-
Donal T. Manahan and Douglas A. Pace
- Subjects
animal structures ,Embryo, Nonmammalian ,Zoology ,Antarctic Regions ,Biology ,Oxygen Consumption ,biology.animal ,Respiration ,Temperate climate ,Protein biosynthesis ,Sterechinus neumayeri ,Animals ,Amino Acids ,Radioactive Tracers ,Sea urchin ,Larva ,Ecology ,Protein turnover ,biology.organism_classification ,Cold Temperature ,Protein Biosynthesis ,Sea Urchins ,embryonic structures ,Seawater ,General Agricultural and Biological Sciences ,Energy Metabolism - Abstract
Cold environments represent a substantial volume of the biosphere. To study developmental physiology in subzero seawater temperatures typically found in the Southern Ocean, rates and costs of protein synthesis were measured in embryos and larvae of Sterechinus neumayeri, the Antarctic sea urchin. Our analysis of the "cost of living" in extreme cold for this species shows (1) that cost of protein synthesis is strikingly low during development, at 0.41 +/- 0.05 J (mg protein synthesized)(-1) (n = 16); (2) that synthesis cost is fixed and independent of synthesis rate; and (3) that a low synthesis cost permits high rates of protein turnover at -1 degrees C, at rates comparable to those of temperate species of sea urchin embryos developing at 15 degrees C. With a low synthesis cost, even at the highest synthesis rates measured (gastrulae), the proportion of total metabolism accounted for by protein synthesis in the Antarctic sea urchin was 54%-a value similar to that of temperate sea urchin embryos. In the Antarctic sea urchin, up to 87% of metabolic rate can be accounted for by the combined energy costs of protein synthesis and the sodium pump. We conclude that, in Antarctic sea urchin embryos, high rates of protein synthesis can be supported in extreme-cold environments while still maintaining low rates of respiration.
- Published
- 2007
41. Fixed metabolic costs for highly variable rates of protein synthesis in sea urchin embryos and larvae
- Author
-
Donal T. Manahan and Douglas A. Pace
- Subjects
animal structures ,Embryo, Nonmammalian ,Time Factors ,Physiology ,Aquatic Science ,Biology ,Animal science ,biology.animal ,Protein biosynthesis ,Animals ,Body Size ,Carbon Radioisotopes ,Amino Acids ,Molecular Biology ,Sea urchin ,Ecology, Evolution, Behavior and Systematics ,Lytechinus pictus ,Larva ,Analysis of Variance ,Alanine ,Ecology ,fungi ,Proteins ,Embryo ,Biological Transport ,Metabolism ,Blastula ,Insect Science ,Protein Biosynthesis ,Sea Urchins ,Metabolic rate ,Animal Science and Zoology ,Energy Metabolism - Abstract
SUMMARY Defining the physiological mechanisms that set metabolic rates and the`cost of living' is important for understanding the energy costs of development. Embryos and larvae of the sea urchin Lytechinus pictus(Verrill) were used to test hypotheses regarding differential costs of protein synthesis in animals differing in size, rates of protein synthesis, and physiological feeding states. For embryos, the rate of protein synthesis was 0.22±0.014 ng protein embryo-1 h-1 (mean ±s.e.m.) and decreased in unfed larvae to an average rate of 0.05±0.001 ng protein larva-1 h-1. Fed larvae had rates of synthesis that were up to 194 times faster than unfed larvae (9.7±0.81 ng protein larva-1 h-1). There was no significant difference, however, in the cost of protein synthesis between these larvae with very different physiological states. Furthermore, the cost of synthesis in the larval stages was also similar to costs measured for blastula and gastrula embryos of 8.4±0.99 J mg-1 protein synthesized. The cost of protein synthesis was obtained using both direct (`inhibitor') and indirect (`correlative') measurements; both methods gave essentially identical results. Protein synthesis accounted for up to 54±8% of metabolic rate in embryos. Percent of metabolism accounted for by protein synthesis in larvae was dependent on their physiological feeding state, with protein synthesis accounting for 16±4% in unfed larvae and 75±11% in fed larvae. This regulation of metabolic rate was due to differential rates of synthesis for a fixed energy cost per unit mass of protein synthesized. The cost of synthesizing a unit of protein did not change with increasing rates of protein synthesis. We conclude that the cost of protein synthesis is independent of the rate of synthesis, developmental stage, size and physiological feeding state during sea urchin development.
- Published
- 2005
42. Energy metabolism during larval development of green and white abalone, Haliotis fulgens and H. sorenseni
- Author
-
Donal T. Manahan and Amy L. Moran
- Subjects
Larva ,biology ,Abalone ,Ecology ,Marine larval ecology ,fungi ,Energetics ,Zoology ,Proteins ,Metabolism ,biology.organism_classification ,Congener ,Oxygen Consumption ,Mollusca ,parasitic diseases ,Haliotis fulgens ,Biological dispersal ,Animals ,Seawater ,General Agricultural and Biological Sciences ,Energy Metabolism ,Phospholipids ,Triglycerides - Abstract
An understanding of the biochemical and physiological energetics of lecithotrophic development is useful for interpreting patterns of larval development, dispersal potential, and life-history evolution. This study investigated the metabolic rates and use of biochemical reserves in two species of abalone, Haliotis fulgens (the green abalone) and H. sorenseni (the white abalone). Larvae of H. fulgens utilized triacylglycerol as a primary source of endogenous energy reserves for development ( approximately 50% depletion from egg to metamorphic competence). Amounts of phospholipid remained constant, and protein dropped by about 30%. After embryogenesis, larvae of H. fulgens had oxygen consumption rates of 81.7 +/- 5.9 (SE) pmol larva(-1) h(-1) at 15 degrees C through subsequent development. The loss of biochemical reserves fully met the needs of metabolism, as measured by oxygen consumption. Larvae of H. sorenseni were examined during later larval development and were metabolically and biochemically similar to H. fulgens larvae at a comparable stage. Metabolic rates of both species were very similar to previous data for a congener, H. rufescens, suggesting that larval metabolism and energy utilization may be conserved among closely related species that also share similar developmental morphology and feeding modes.
- Published
- 2003
43. Coulometric measurement of oxygen consumption during development of marine invertebrate embryos and larvae
- Author
-
Donal T. Manahan and Ove Hoegh-Guldberg
- Subjects
biology ,Physiology ,Ecology ,fungi ,Oxygen evolution ,chemistry.chemical_element ,Marine invertebrates ,Aquatic Science ,biology.organism_classification ,Oxygen ,Respirometry ,chemistry ,Dendraster excentricus ,Insect Science ,Environmental chemistry ,Respiration ,Respirometer ,Animal Science and Zoology ,Limiting oxygen concentration ,Molecular Biology ,Ecology, Evolution, Behavior and Systematics - Abstract
Determining the metabolic rate of larval invertebrates from aquatic habitats is complicated by the problems of small size and the scarcity of suitable measurement techniques. In this study, coulometric respirometry (a new technique for the study of marine embryos and larvae) was used to explore several issues associated with the rate of energy use during embryonic and larval development of marine invertebrates from three phyla. Coulometric respirometry measures rates of oxygen consumption under normoxic conditions by electrochemically replacing the oxygen consumed by organisms during an experiment. This technique is based on the assumption that all electrons consumed by the anodic reactions result in the production of oxygen. We verify this assumption using direct measurements of oxygen production and show that the technique is sensitive enough (1 nmol O2 h-1) to quantify the oxygen consumption of a single individual swimming freely in a relatively large volume (2 ml). Continuous measurements can span days, and embryos in the coulometric respiration chambers develop to the larval stage at normal rates of differentiation. Measurements of metabolic rates were made with the coulometric respirometer during the complete life-span of larvae of three species (asteroid, Asterina miniata; bivalve, Crassostrea gigas; echinoid, Dendraster excentricus). For these species, metabolic power equations had mass exponents near unity (0.9–1.1), showing that metabolic rate scales isometrically with mass during larval growth. Metabolic rates were independent of the concentration of larvae used in the respirometer chambers for a range of larval concentrations from 4 to 400 larvae ml-1 (coulometric respirometer) and from 241 to 809 larvae ml-1 (polarographic oxygen sensor). Metabolic rates were measured using coulometric respirometry and two other commonly used techniques, polarographic oxygen sensors and Winkler’s titration. Polarographic oxygen sensors in small, sealed chambers (100 μl) consistently gave the lowest values (by as much as 80 %) for the asteroid, echinoid and molluscan larvae. By comparison, rates of oxygen consumption measured using coulometric respirometry and Winkler’s titration (to measure the change in oxygen concentration over time) were similar and consistently higher. Although the polarographic oxygen sensor is the most widely used method for measuring the metabolism of small animals in sealed 100–1000 μl chambers, it appears that the metabolism of some larvae is adversely affected by the conditions within these respirometers.
- Published
- 1995
44. Concepts of Adaptation in Aquatic Animals: Deviations from the Terrestrial Paradigm—A Rationale for the Symposium
- Author
-
Margaret J. McFall-Ngai and Donal T. Manahan
- Subjects
Geography ,General Earth and Planetary Sciences ,Environmental ethics ,Aquatic animal ,Adaptation (computer science) ,General Environmental Science - Published
- 1990
45. The uptake of dissolved glycine following fertilization of oyster eggs, Crassostrea gigas (Thunberg)
- Author
-
Donal T. Manahan
- Subjects
Oyster ,animal structures ,Cell division ,Ecology ,fungi ,Embryo ,Aquatic Science ,Biology ,biology.organism_classification ,Ouabain ,Nutrient ,Human fertilization ,biology.animal ,embryonic structures ,Glycine ,Botany ,medicine ,Crassostrea ,Ecology, Evolution, Behavior and Systematics ,medicine.drug - Abstract
Embryos of the oyster, Crassostrea gigas (Thunberg), can take up [ 14 C]glycine from micromolar concentrations, but unfertilized eggs do not. Activation of uptake mechanisms coincides with the first cell division of the fertilized egg. Uptake of glycine is inhibited by ouabain, an inhibitor of the sodium pump. This study, when combined with earlier work, demonstrates that bivalves utilize dissolved organic nutrients throughout their life span, from fertilized egg to adulthood.
- Published
- 1983
46. Feeding by a ?nonfeeding? larva: uptake of dissolved amino acids from seawater by lecithotrophic larvae of the gastropod Haliotis rufescens
- Author
-
W. B. Jaeckle and Donal T. Manahan
- Subjects
Alanine ,chemistry.chemical_classification ,Taurine ,animal structures ,genetic structures ,Ecology ,biology ,Abalone ,fungi ,Veliger ,Aquatic Science ,biology.organism_classification ,Amino acid ,chemistry.chemical_compound ,Biochemistry ,chemistry ,Trochophore ,Lipid biosynthesis ,parasitic diseases ,Mollusca ,Ecology, Evolution, Behavior and Systematics - Abstract
Larvae of the red abalone (Haliotis rufescens Swainson) are functionally incapable of capturing particulate foods. The aim of this study was to determine whether these larvae could acquire energy from seawater in the form of dissolved organic material. Trochophore and veliger larvae were shown to acquire energy by transporting dissolved organic material from seawater. Both larval stages took up all classes of amino acids tested. The influx of radiolabeled alanine represented the net substrate flux, as determined by direct chemical measurement for both trochophore and veliger larvae. Although veliger larvae have a transport system to take up taurine from seawater, a net efflux was observed for this amino acid. The release of taurine occurred independently of the presence of either taurine or other amino acids in the medium. Transported alanine was used in both anabolic and catabolic pathways. The percent of 14C-alanine in the trichloroacetic acid-insoluble fraction (macromolecules) of veliger larvae ranged from 21 to 56% of the total radioactivity in the larvae. No lipid biosynthesis was detected from 14C-labeled alanine. Veliger larvae catabolized 15 to 19% of the total alanine taken up and released it as 14CO2. The metabolic rate (oxygen consumption) and the rate of amino acid uptake were both determined for the same group of veliger larvae. The percent contribution that the uptake of amino acids, from a total concentration of 1.6 μM, made to the metabolic demand of abalone larvae ranged from 39 to 70%. Thus, these lecithotrophic larvae are not energetically independent of their environment, a result which differs from the current view of energy allocation to “nonfeeding” larvae.
- Published
- 1989
47. Technical advances in the study of nutrition of marine molluscs
- Author
-
Donal T. Manahan and Grover C. Stephens
- Subjects
Fishery ,Hplc analysis ,Technical innovation ,Environmental chemistry ,fungi ,Marine habitats ,Mariculture ,Seawater ,Water quality ,Aquatic Science ,Biology ,Quantitative determination ,Qualitative composition - Abstract
Recent investigation has shown that the several marine bivalves that have been studied can remove small organic compounds from natural seawater at rates that provide a substantial supplement to particulate food. It is possible to make this statement without qualification because of two technical advances in the study of molluscan nutrition. First, bacteria-free suspensions of marine bivalve larvae are now available. Therefore, interactions between larvae and microbial elements in such suspensions can be precisely controlled or completely eliminated. The other technical innovation, which is the focus of this article, is the application of high performance liquid chromatography (HPLC) to analysis of small organic compounds in seawater. The following applications of HPLC are introduced and illustrated: 1. 1. Demonstration of net entry of dissolved organic substrates into bacteria-free bivalves 2. 2. Modification of concentrations and qualitative composition of organic substrates in seawater caused by typical mariculture procedures 3. 3. Quantitative determination of organic substrates normally present in specific marine habitats. The combination of HPLC analysis and use of bacteria-free experimental material provides an opportunity to characterize specific organic requirements for molluscan survival and growth, to describe explicitly an important component of “water quality”, and to increase understanding and control of feeding regimes in mariculture.
- Published
- 1984
48. THE UPTAKE AND METABOLISM OF DISSOLVED AMINO ACIDS BY BIVALVE LARVAE
- Author
-
Donal T. Manahan
- Subjects
chemistry.chemical_classification ,Oyster ,Larva ,animal structures ,fungi ,Metabolism ,Biology ,biology.organism_classification ,Mytilus ,Amino acid ,chemistry ,Biochemistry ,Dry weight ,biology.animal ,Glycine ,Crassostrea ,Food science ,General Agricultural and Biological Sciences - Abstract
The rates of uptake and metabolism of 14C-labeled glycine and alanine from sea water into larval oysters, Crassostrea gigas (Thunberg) and mussels, Mytilus edulis L. were determined. Kinetic studies showed that both species have a Kt value of 3-4 µM, indicating that bivalve larvae have amino acid transport mechanisms that function efficiently in natural sea water. The Kt values for larvae are similar to those reported for adult bivalves. However, larvae take up dissolved amino acids at approximately ten times the rate reported for adult bivalves on a gram dry weight basis. This difference in uptake capacity presumably reflects the greater absorptive surface area to volume ratio of a larva. Rates of metabolism of absorbed amino acids by larvae were also rapid. Following a 100 min exposure, oyster larvae incorporated 47% of the glycine into protein and 38% was produced as CO2. In comparison to adults, larval bivalves have a more rapid weight-specific uptake and faster rate of utilizing absorbed amino acids....
- Published
- 1983
49. Amino Acid Uptake and Metabolism by Larvae of the Marine Worm Urechis caupo (Echiura), a New Species in Axenic Culture
- Author
-
Donal T. Manahan and William Jaeckle
- Subjects
Alanine ,Echiura ,Biochemistry ,Catabolism ,Lipid biosynthesis ,Aspartic acid ,Metabolism ,Biology ,General Agricultural and Biological Sciences ,Axenic ,biology.organism_classification ,Marine worm - Abstract
Axenic (bacteria-free) larval cultures of the marine echiuran worm, Urechis caupo, were reliably obtained by aseptically removing gametes directly from the gamete storage organs. Trochophore larvae only removed neutral amino acids from seawater as measured by high-performance liquid chromatography (HPLC). There was no detectable uptake, as measured by HPLC, of acidic or basic amino acids. Kinetic analysis showed that the transport system for alanine in 4-day-old larvae had a Kt of 4-6 µM and a Jmax of 9-10 pmol larva-1 h-1. Following a 50-min exposure, the majority of the radioactivity (95%) from 14C-alanine was found in the trichloroacetic acid-soluble fraction. Very little label appeared as acid-insoluble material, and there was no detectable lipid biosynthesis from 14C-alanine. Approximately 12% of the total alanine transported was released in the form of 14CO2. Thin-layer chromatography of intracellular free amino acid pools demonstrated that aspartic acid and glutamic acid were radiolabeled from the alanine precursor. A comparison of the energy acquired from the transport of alanine, with the metabolic rate of 4-day-old larvae, revealed that 51% of the metabolic demand could be provided by the transport and complete catabolism of this single amino acid at a concentration of 595 nM in seawater.
- Published
- 1989
50. The use of high performance liquid chromatography to measure dissolved organic compounds in bivalve aquaculture systems
- Author
-
Grover C. Stephens and Donal T. Manahan
- Subjects
business.industry ,Ecology ,fungi ,food and beverages ,Aquatic Science ,Biology ,High-performance liquid chromatography ,law.invention ,Nutrient ,Aquaculture ,law ,Environmental chemistry ,Composition (visual arts) ,Mariculture ,Seawater ,Food quality ,business ,Filtration - Abstract
Concentrations of specific free amino acids (FAA) at points in the seawater systems of two aquaculture laboratories were measured using high performance liquid chromatography (HPLC). The processes used to culture bivalves severely modified the FAA composition of sea water. Sand filtration removed FAA almost completely. FAA were then added back to the sea water in varying amounts depending on the algal species used as food. There were large differences in the FAA concentrations from the filtrates of the different algal species routinely used as food for oysters. As bivalves absorb FAA from sea water and use them as a nutritional supplement, the dissolved organic nutrients present in algal filtrates may be an important factor in the food quality of a given algal species. HPLC techniques can be used to understand the interaction of developing larvae with dissolved organic compounds inadvertently introduced into mariculture sytems.
- Published
- 1983
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