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The transmission of microbes from mother to offspring is an ancient, advantageous, and widespread feature of metazoan life history. Despite this, little is known about the quantitative strategies taken to maintain symbioses across generations. The quantity of maternal microbes that is provided to each offspring through vertical transmission could theoretically be stochastic (no trend), consistent (an optimal range is allocated), or provisioned (a trade-off with fecundity). Examples currently come from animals that release free-living eggs (oviparous) and suggest that offspring are provided a consistent quantity of symbionts. The quantity of maternal microbes that is vertically transmitted in other major reproductive strategies has yet to be assessed. We used the brooding (viviparous) sponge Halichondria panicea to test whether offspring receive quantitatively similar numbers of maternal microbes. We observed that H .  panicea has a maternal pool of the obligate symbiont Candidatus Halichondribacter symbioticus and that this maternal pool is provisioned proportionally to reproductive output and allometrically by offspring size. This pattern was not observed for the total bacterial community. Experimental perturbation by antibiotics could not reduce the abundance of Ca. H. symbioticus in larvae, while the total bacterial community could be reduced without affecting the ability of larvae to undergo metamorphosis. A trade-off between offspring size and number is, by definition, maternal provisioning and parallel differences in Ca. H. symbioticus abundance would suggest that this obligate symbiont is also provisioned., Competing Interests: We declare that we have no competing interests., (© 2023 The Authors. Ecology and Evolution published by John Wiley & Sons Ltd.)

Organisms living on the seafloor are subject to encrustations by a wide variety of animals, plants and microbes. Sea urchins, however, thwart this covering. Despite having a sophisticated immune system, there is no clear molecular mechanism that allows sea urchins to remain free of epibiotic microorganisms. Here, we test the hypothesis that pigmentation biosynthesis in sea urchin spines influences their interactions with microbes in vivo using CRISPR/Cas9. We report three primary findings. First, the microbiome of sea urchin spines is species-specific and much of this community is lost in captivity. Second, different colour morphs associate with bacterial communities that are similar in taxonomic composition, diversity and evenness. Lastly, loss of the pigmentation biosynthesis genes polyketide synthase and flavin-dependent monooxygenase induces a shift in which bacterial taxa colonize sea urchin spines. Therefore, our results are consistent with the hypothesis that host pigmentation biosynthesis can, but may not always, influence the microbiome in sea urchin spines.

AbstractBacterial symbionts are functionally integral to animal reproduction and development, some of which have evolved additional mechanisms to override these host programs. One habitat that is increasingly recognized to contain phylogenetically related lineages of reproductive manipulators is the ocean. The reproduction of marine invertebrates often occurs by free spawning instead of by the physical contact of copulation in terrestrial systems. We developed an integrated model to understand whether and when microbes that manipulate host reproduction by cytoplasmic incompatibility, feminization, and male killing spread within populations of free-spawning marine invertebrates. Our model supports three primary findings. First, sex ratio distortion leads to suboptimal fertilization and zygote production in planktotrophs (feeding larvae) but enhance these processes in lecithotrophs (nonfeeding larvae). Second, feminization and a combination of male killing plus enhanced growth are effective at spreading reproductive manipulators while also inducing a female-biased sex ratio. Third, the majority of free-spawning marine invertebrates could be infected across a range of life history combinations, with infections harming species with smaller eggs and longer pelagic durations while benefiting species with larger eggs and shorter pelagic durations. Together, this supports the general premise that microbes may manipulate the reproduction of free-spawning marine invertebrates (e.g., by inducing changes in developmental life history) and that these types of manipulations overlap considerably with terrestrial systems.

Animal development is an inherently complex process that is regulated by highly conserved genomic networks, and the resulting phenotype may remain plastic in response to environmental signals. Despite development having been studied in a more natural setting for the past few decades, this framework often precludes the role of microbial prokaryotes in these processes. Here, we address how microbial symbioses impact animal development from the onset of gametogenesis through adulthood. We then provide a first assessment of which developmental processes may or may not be influenced by microbial symbioses and, in doing so, provide a holistic view of the budding discipline of developmental symbiosis., Competing Interests: Competing interests The authors declare no competing or financial interests., (© 2022. Published by The Company of Biologists Ltd.)

Marine sponges (phylum Porifera) form symbioses with diverse microbial communities that can be transmitted between generations through their developmental stages. Here, we integrate embryology and microbiology to review how symbiotic microorganisms are transmitted in this early-diverging lineage. We describe that vertical transmission is widespread but not universal, that microbes are vertically transmitted during a select developmental window, and that properties of the developmental microbiome depends on whether a species is a high or low microbial abundance sponge. Reproduction, development, and symbiosis are thus deeply rooted, but why these partnerships form remains the central and elusive tenet of these developmental symbioses., (© 2022. The Author(s).)

AbstractMicrobial symbionts are a common life-history character of marine invertebrates and their developmental stages. Communities of bacteria that associate with the eggs, embryos, and larvae of coastal marine invertebrates tend to be species specific and correlate with aspects of host biology and ecology. The richness of bacteria associated with the developmental stages of coastal marine invertebrates spans four orders of magnitude, from single mutualists to thousands of unique taxa. This understanding stems predominately from the developmental stages of coastal species. If they are broadly representative of marine invertebrates, then we may expect deep-sea species to associate with bacterial communities that are similar in diversity. To test this, we used amplicon sequencing to profile the bacterial communities of invertebrate larvae from multiple taxonomic groups (annelids, molluscs, crustaceans) collected from 2500 to 3670 m in depth in near-bottom waters near hydrothermal vents in 3 different regions of the Pacific Ocean (the East Pacific Rise, the Mariana Back-Arc, and the Pescadero Basin). We find that larvae of deep-sea invertebrates associate with low-diversity bacterial communities (~30 bacterial taxa) that lack specificity between taxonomic groups. The diversity of these communities is estimated to be ~7.9 times lower than that of coastal invertebrate larvae, but this result depends on the taxonomic group. Associating with a low-diversity community may imply that deep-sea invertebrate larvae do not have a strong reliance on a microbiome and that the hypothesized lack of symbiotic contributions would differ from expectations for larvae of coastal marine invertebrates.

Animal gastrointestinal tracts harbor a microbiome that is integral to host function, yet species from diverse phyla have evolved a reduced digestive system or lost it completely. Whether such changes are associated with alterations in the diversity and/or abundance of the microbiome remains an untested hypothesis in evolutionary symbiosis. Here, using the life history transition from planktotrophy (feeding) to lecithotrophy (nonfeeding) in the sea urchin Heliocidaris , we demonstrate that the lack of a functional gut corresponds with a reduction in microbial community diversity and abundance as well as the association with a diet-specific microbiome. We also determine that the lecithotroph vertically transmits a Rickettsiales that may complement host nutrition through amino acid biosynthesis and influence host reproduction. Our results indicate that the evolutionary loss of a functional gut correlates with a reduction in the microbiome and the association with an endosymbiont. Symbiotic transitions can therefore accompany life history transitions in the evolution of developmental strategies., Competing Interests: The authors declare no competing interest.

Exposure to and colonization by bacteria during development have wide-ranging beneficial effects on animal biology but can also inhibit growth or cause disease. The immune system is the prime mediator of these microbial interactions and is itself shaped by them. Studies using diverse animal taxa have begun to elucidate the mechanisms underlying the acquisition and transmission of bacterial symbionts and their interactions with developing immune systems. Moreover, the contexts of these associations are often confounded by stark differences between "wild type" microbiota and the bacterial communities associated with animals raised in conventional or germ-free laboratories. In this study, we investigate the spatio-temporal kinetics of bacterial colonization and associated effects on growth and immune function in larvae of the purple sea urchin ( Strongylocentrotus purpuratus ) as a model for host-microbe interactions and immune system development. We also compare the host-associated microbiota of developing embryos and larvae raised in natural seawater or exposed to adult-associated bacteria in the laboratory. Bacteria associated with zygotes, embryos, and early larvae are detectable with 16S amplicon sequencing, but 16S-FISH indicates that the vast majority of larval bacterial load is acquired after feeding begins and is localized to the gut lumen. The bacterial communities of laboratory-cultured embryos are significantly less diverse than the natural microbiota but recapitulate its major components (Alphaproteobacteria, Gammaproteobacteria, and Bacteroidetes), suggesting that biologically relevant host-microbe interactions can be studied in the laboratory. We also demonstrate that bacterial exposure in early development induces changes in morphology and in the immune system. In the absence of bacteria, larvae grow larger at the 4-arm stage. Additionally, bacteria-exposed larvae are significantly more resistant to lethal infection with the larva-associated pathogen Vibrio lentus suggesting that early exposure to high levels of microbes, as would be expected in natural conditions, affects the immune state in later larvae. These results expand our knowledge of microbial influences on early sea urchin development and establish a model in which to study the interactions between the developing larval immune system and the acquisition of larval microbiota., (Copyright © 2020 Schuh, Carrier, Schrankel, Reitzel, Heyland and Rast.)

Microbes can play an important role in the physiology of animals by providing essential nutrients, inducing immune pathways, and influencing the specific species that compose the microbiome through competitive or facilitatory interactions. The community of microbes associated with animals can be dynamic depending on the local environment, and factors that influence the composition of the microbiome are essential to our understanding of how microbes may influence the biology of their animal hosts. Regularly repeated changes in the environment, such as diel lighting, can result in two different organismal responses: a direct response to the presence and absence of exogenous light and endogenous rhythms resulting from a molecular circadian clock, both of which can influence the associated microbiota. Here, we report how diel lighting and a potential circadian clock impacts the diversity and relative abundance of bacteria in the model cnidarian Nematostella vectensis using an amplicon-based sequencing approach. Comparisons of bacterial communities associated with anemones cultured in constant darkness and in light:dark conditions revealed that individuals entrained in the dark had a more diverse microbiota. Overall community composition showed little variation over a 24-hr period in either treatment; however, abundances of individual bacterial OTUs showed significant cycling in each treatment. A comparative analysis of genes involved in the innate immune system of cnidarians showed differential expression between lighting conditions in N. vectensis, with significant up-regulation during long-term darkness for a subset of genes. Together, our studies support a hypothesis that the bacterial community associated with this species is relatively stable under diel light conditions when compared with static conditions and that particular bacterial members may have time-dependent abundance that coincides with the diel photoperiod in an otherwise stable community.

Determining the factors underlying the assembly, structure, and diversity of symbiont communities remains a focal point of animal-microbiome research. Much of these efforts focus on taxonomic variation of microbiota within or between animal populations, but rarely test the proportional impacts of ecological components that may affect animal-associated microbiota. Using larvae from the sea urchin Strongylocentrotus droebachiensis from the Atlantic and Pacific Oceans, we test the hypothesis that, under natural conditions, inter-population differences in the composition of larval-associated bacterial communities are larger than intra-population variation due to a heterogeneous feeding environment. Despite significant differences in bacterial community structure within each S. droebachiensis larval population based on food availability, development, phenotype, and time, variation in OTU membership and community composition correlated more strongly with geographic location. Moreover, 20-30% of OTUs associated with larvae were specific to a single location while less than 10% were shared. Taken together, these results suggest that inter-populational variation in symbiont communities may be more pronounced than intra-populational variation, and that this difference may suggest that broad-scale ecological variables (e.g., across ocean basins) may mask smaller scale ecological variables (e.g., food availability)., (© FEMS 2019.)

Objective: The aim of this study was to assess the impact of a urinary tract infection (UTI) management bundle to reduce the treatment of asymptomatic bacteriuria (AB) and to improve the management of symptomatic UTIs., Design: Before-and-after intervention study.SettingsTertiary-care hospital.PatientsConsecutive sample of inpatients with positive single or mixed-predominant urine cultures collected and reported while admitted to the hospital., Methods: The UTI management bundle consisted of nursing and prescriber education, modification of the reporting of positive urine cultures, and pharmacists' prospective audit and feedback. A retrospective chart review of consecutive inpatients with positive urinary cultures was performed before and after implementation of the management bundle., Results: Prior to the implementation of the management bundle, 276 patients were eligible criteria for chart review. Of these 276 patients, 165 (59·8%) were found to have AB; of these 165 patients with AB, 111 (67·3%) were treated with antimicrobials. Moreover, 268 patients met eligibility criteria for postintervention review. Of these 268, 133 patients (49·6%) were found to have AB; of these 133 with AB, 22 (16·5%) were treated with antimicrobials. Thus, a 75·5% reduction of AB treatment was achieved. Educational components of the bundle resulted in a substantial decrease in nonphysician-directed urine sample submission. Adherence to a UTI management algorithm improved substantially in the intervention period, with a notable decrease in fluoroquinolone prescription for empiric UTI treatment., Conclusions: A UTI management bundle resulted in a dramatic improvement in the management of urinary tract infection, particularly a reduction in the treatment of AB and improved management of symptomatic UTI.

Morphological plasticity is a genotype-by-environment interaction that enables organisms to increase fitness across varying environments. Symbioses with diverse microbiota may aid in acclimating to this variation, but whether the associated bacteria community is phenotype specific remains understudied. Here we induce morphological plasticity in three species of sea urchin larvae and measure changes in the associated bacterial community. While each host species has unique bacterial communities, the expression of plasticity results in the convergence on a phenotype-specific microbiome that is, in part, driven by differential association with α- and γ-proteobacteria. Furthermore, these results suggest that phenotype-specific signatures are the product of the environment and are correlated with ingestive and digestive structures. By manipulating diet quantity over time, we also show that differentially associating with microbiota along a phenotypic continuum is bidirectional. Taken together, our data support the idea of a phenotype-specific microbial community and that phenotypic plasticity extends beyond a genotype-by-environment interaction.

Benthic marine suspension feeders provide an important link between benthic and pelagic ecosystems. The strength of this link is determined by suspension-feeding rates. Many studies have measured suspension-feeding rates using indirect clearance-rate methods, which are based on the depletion of suspended particles. Direct methods that measure the flow of water itself are less common, but they can be more broadly applied because, unlike indirect methods, direct methods are not affected by properties of the cleared particles. We present pumping rates for three species of suspension feeders, the clams Mya arenaria and Mercenaria mercenaria and the tunicate Ciona intestinalis , measured using a direct method based on particle image velocimetry (PIV). Past uses of PIV in suspension-feeding studies have been limited by strong laser reflections that interfere with velocity measurements proximate to the siphon. We used a new approach based on fitting PIV-based velocity profile measurements to theoretical profiles from computational fluid dynamic (CFD) models, which allowed us to calculate inhalant siphon Reynolds numbers ( Re ). We used these inhalant Re and measurements of siphon diameters to calculate exhalant Re , pumping rates, and mean inlet and outlet velocities. For the three species studied, inhalant Re ranged from 8 to 520, and exhalant Re ranged from 15 to 1073. Volumetric pumping rates ranged from 1.7 to 7.4 l h -1 for M . arenaria , 0.3 to 3.6 l h -1 for M . m ercenaria and 0.07 to 0.97 l h -1 for C . intestinalis We also used CFD models based on measured pumping rates to calculate capture regions, which reveal the spatial extent of pumped water. Combining PIV data with CFD models may be a valuable approach for future suspension-feeding studies., Competing Interests: Competing interestsThe authors declare no competing or financial interests., (© 2017. Published by The Company of Biologists Ltd.)

Our understanding of the diverse interactions between hosts and microbes has grown profoundly over the past two decades and, as a product, has revolutionized our knowledge of the life sciences. Through primarily laboratory experiments, the current framework for holobionts and their respective hologenomes aims to decipher the underpinnings and implications of symbioses between host and microbiome. However, the laboratory setting restricts the full spectrum of host-associated symbionts as compared to those found in nature; thus, limiting the potential for a holistic interpretation of the functional roles the microbiome plays in host biology. When holobionts are studied in nature, associated microbial communities vary considerably between conditions, resulting in more microbial associates as part of the "hologenome" across environments than in either environment alone. We review and synthesize empirical evidence suggesting that hosts may associate with a larger microbial network that, in part, corresponds to experiencing diverse environmental conditions. To conceptualize the interactions between host and microbiome in an ecological context, we suggest the "host-associated microbial repertoire," which is the sum of microbial species a host may associate with over the course of its life-history under all encountered environmental circumstances. Furthermore, using examples from both terrestrial and marine ecosystems, we discuss how this concept may be used as a framework to compare the ability of the holobiont to acclimate and adapt to environmental variation, and propose three "signatures" of the concept.

Background: Some metazoa have the capacity to regenerate lost body parts. This phenomenon in adults has been classically described in echinoderms, especially in sea stars (Asteroidea). Sea star bipinnaria larvae can also rapidly and effectively regenerate a complete larva after surgical bisection. Understanding the capacity to reverse cell fates in the larva is important from both a developmental and biomedical perspective; yet, the mechanisms underlying regeneration in echinoderms are poorly understood., Results: Here, we describe the process of bipinnaria regeneration after bisection in the bat star Patiria miniata. We tested transcriptional, translational, and cell proliferation activity after bisection in anterior and posterior bipinnaria halves as well as expression of SRAP, reported as a sea star regeneration associated protease (Vickery et al., 2001b). Moreover, we found several genes whose transcripts increased in abundance following bisection, including: Vasa, dysferlin, vitellogenin 1 and vitellogenin 2., Conclusion: These results show a transformation following bisection, especially in the anterior halves, of cell fate reassignment in all three germ layers, with clear and predictable changes. These results define molecular events that accompany the cell fate changes coincident to the regenerative response in echinoderm larvae., (Crown Copyright © 2016. Published by Elsevier Ireland Ltd. All rights reserved.)

Planktotrophic sea urchin larvae are developmentally plastic: in response to food scarcity, development of the juvenile rudiment is suspended and larvae instead develop elongated arms, thus increasing feeding capacity and extending larval life. Here, data are presented on the effect of different feeding regimes on gene expression in larvae of the green sea urchin Strongylocentrotus droebachiensis. These data indicate that during periods of starvation, larvae down-regulate genes involved in growth and metabolic activity while up-regulating genes involved in lipid transport, environmental sensing, and defense. Additionally, we show that starvation increases FoxO activity and that in well-fed larvae rapamycin treatment impedes rudiment growth, indicating that the latter requires TOR activity. These results suggest that the developmental plasticity of echinoplutei is regulated by genes known to control aging and longevity in other animals., (© 2015 Marine Biological Laboratory.)