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Complex assemblages of microbes in the surface ocean are responsible for approximately half of global carbon fixation. The persistence of high taxonomic diversity despite competition for a small suite of relatively homogeneously distributed nutrients, that is, 'the paradox of the plankton', represents a long-standing challenge for ecological theory. Here we find evidence consistent with temporal niche partitioning of nitrogen assimilation processes over a diel cycle in the North Pacific Subtropical Gyre. We jointly analysed transcript abundances, lipids and metabolites and discovered that a small number of diel archetypes can explain pervasive periodic dynamics. Metabolic pathway analysis of identified diel signals revealed asynchronous timing in the transcription of nitrogen uptake and assimilation genes among different microbial groups-cyanobacteria, heterotrophic bacteria and eukaryotes. This temporal niche partitioning of nitrogen uptake emerged despite synchronous transcription of photosynthesis and central carbon metabolism genes and associated macromolecular abundances. Temporal niche partitioning may be a mechanism by which microorganisms in the open ocean mitigate competition for scarce resources, supporting community coexistence.

The production of dihydrogen (H2 ) is an enigmatic yet obligate component of biological dinitrogen (N2 ) fixation. This study investigates the effect on H2 production by N2 fixing cyanobacteria when they are exposed to either air or a gas mixture consisting of argon, oxygen, and carbon dioxide (Ar:O2 :CO2 ). In the absence of N2 , nitrogenase diverts the flow of electrons to the production of H2 , which becomes a measure of Total Nitrogenase Activity (TNA). This method of argon-induced hydrogen production (AIHP) is much less commonly used to infer rates of N2 fixation than the acetylene reduction (AR) assay. We provide here a full evaluation of the AIHP method and demonstrate its ability to achieve high-resolution measurements of TNA in a gas exchange flow-through system. Complete diel profiles of H2 production were obtained for N2 fixing cyanobacteria despite the absence of N2 that broadly reproduced the temporal patterns observed by the AR assay. Comparison of H2 production under air versus Ar:O2 :CO2 revealed the efficiency of electron usage during N2 fixation and place these findings in the broader context of cell metabolism. Ultimately, AIHP is demonstrated to be a viable alternative to the AR assay with several additional merits that provide an insight into cell physiology and promise for successful field application.

Phytoplankton communities residing in the open ocean, the largest habitat on Earth, play a key role in global primary production. Through their influence on nutrient supply to the euphotic zone, open-ocean eddies impact the magnitude of primary production and its spatial and temporal distributions. It is important to gain a deeper understanding of the microbial ecology of marine ecosystems under the influence of eddy physics with the aid of advanced technologies. In March and April 2018, we deployed autonomous underwater and surface vehicles in a cyclonic eddy in the North Pacific Subtropical Gyre to investigate the variability of the microbial community in the deep chlorophyll maximum (DCM) layer. One long-range autonomous underwater vehicle (LRAUV) carrying a third-generation Environmental Sample Processor (3G-ESP) autonomously tracked and sampled the DCM layer for four days without surfacing. The sampling LRAUV's vertical position in the DCM layer was maintained by locking onto the isotherm corresponding to the chlorophyll peak. The vehicle ran on tight circles while drifting with the eddy current. This mode of operation enabled a quasi-Lagrangian time series focused on sampling the temporal variation of the DCM population. A companion LRAUV surveyed a cylindrical volume around the sampling LRAUV to monitor spatial and temporal variation in contextual water column properties. The simultaneous sampling and mapping enabled observation of DCM microbial community in its natural frame of reference.

The 2018 eruption of Kīlauea was associated with massive input of molten lava into the coastal ocean, which altered seawater chemistry and increased phytoplankton production. In seawater plumes advected away from the site of lava entry, we observed elevated concentrations of over a dozen metals relative to background seawater and unique isotopic compositions of Fe, Cu, Ni, Cd and Zn. The δ56Fe of iron released from lava was lower than basaltic, riverine and coastal iron from Hawaiʻi, but similar to observations of other high-temperature hydrothermal vent fluids. However, rapid precipitation led to only modest enrichments in dissolved iron (

The availability of fixed nitrogen (N) is an important factor limiting biological productivity in the oceans. In coastal waters, high dissolved inorganic N concentrations were historically thought to inhibit dinitrogen (N2) fixation, however, recent N2 fixation measurements and the presence of the N2-fixing UCYN-A/haptophyte symbiosis in nearshore waters challenge this paradigm. We characterized the contribution of UCYN-A symbioses to nearshore N2 fixation in the Southern California Current System (SCCS) by measuring bulk community and single-cell N2 fixation rates, as well as diazotroph community composition and abundance. UCYN-A1 and UCYN-A2 symbioses dominated diazotroph communities throughout the region during upwelling and oceanic seasons. Bulk N2 fixation was detected in most surface samples, with rates up to 23.0 ± 3.8 nmol N l−1 d−1, and was often detected at the deep chlorophyll maximum in the presence of nitrate (>1 µM). UCYN-A2 symbiosis N2 fixation rates were higher (151.1 ± 112.7 fmol N cell−1 d−1) than the UCYN-A1 symbiosis (6.6 ± 8.8 fmol N cell−1 d−1). N2 fixation by the UCYN-A1 symbiosis accounted for a majority of the measured bulk rates at two offshore stations, while the UCYN-A2 symbiosis was an important contributor in three nearshore stations. This report of active UCYN-A symbioses and broad mesoscale distribution patterns establishes UCYN-A symbioses as the dominant diazotrophs in the SCCS, where heterocyst-forming and unicellular cyanobacteria are less prevalent, and provides evidence that the two dominant UCYN-A sublineages are separate ecotypes.

Marine ecosystem models often consider temporal dynamics on the order of months to years, and spatial dynamics over regional and global scales as a means to understand the ecology, evolution, and biogeochemical impacts of marine life. Large-scale dynamics are themselves driven over diel scales as a result of light-driven forcing, feedback, and interactions. Motivated by high-frequency measurements taken by Lagrangian sampling in the North Pacific Subtropical Gyre, we develop a hierarchical set of multitrophic community ecology models to investigate and understand daily ecological dynamics in the near-surface ocean including impacts of light-driven growth, infection, grazing, and phytoplankton size structure. Using these models, we investigate the relative impacts of viral-induced and grazing mortality for Prochlorococcus; and more broadly compare in silico dynamics with in situ observations. Via model-data fitting, we show that a multi-trophic model with size structure can jointly explain diel changes in cyanobacterial abundances, cyanobacterial size structure, viral abundance, viral infection rates, and grazer abundances. In doing so, we find that a significant component (between 5% to 55%) of estimated Prochlorococcus mortality is not attributed to either viral lysis (by T4- or T7-like cyanophage) or grazing by heterotrophic nanoflagellates. Instead, model-data integration suggests a heightened ecological relevance of other mortality mechanisms -- including grazing by other predators, particle aggregation, and stress-induced loss mechanisms. Altogether, linking mechanistic multitrophic models with high-resolution measurements provides a route for understanding of diel origins of large-scale marine microbial community and ecosystem dynamics.

The symbiotic cyanobacterium UCYN-A is one of the most globally abundant marine dinitrogen (N2)-fixers, but cultures have not been available and its biology and ecology are poorly understood. We used cultivation-independent approaches to investigate how UCYN-A single-cell N2 fixation rates (NFRs) and nifH gene expression vary as a function of depth and photoperiod. Twelve-hour day/night incubations showed that UCYN-A only fixed N2 during the day. Experiments conducted using in situ arrays showed a light-dependence of NFRs by the UCYN-A symbiosis, with the highest rates in surface waters (5–45 m) and lower rates at depth (≥ 75 m). Analysis of NFRs versus in situ light intensity yielded a light saturation parameter (Ik) for UCYN-A of 44 μmol quanta m−2 s−1. This is low compared with other marine diazotrophs, suggesting an ecological advantage for the UCYN-A symbiosis under low-light conditions. In contrast to cell-specific NFRs, nifH gene-specific expression levels did not vary with depth, indicating that light regulates N2 fixation by UCYN-A through processes other than transcription, likely including host–symbiont interactions. These results offer new insights into the physiology of the UCYN-A symbiosis in the subtropical North Pacific Ocean and provide clues to the environmental drivers of its global distributions. En prensa

1.AbstractMesoscale eddies have been shown to support elevated dinitrogen (N2) fixation rates (NFRs) and abundances of N2-fixing microorganisms (diazotrophs), but the mechanisms underlying these observations are not well understood. We explored relationships among NFRs and cyanobacterial diazotroph abundances in eddy pairs of opposite polarity sampled in the North Pacific Subtropical Gyre and compared our observations to seasonal trends from the Hawaii Ocean Time-series (HOT) program. Consistent with previous reports, we found that NFRs were anomalously high for this region (up to 3.7-fold above previous monthly HOT observations) in the centers of the sampled anticyclones, coinciding with elevated abundances of Crocosphaera in the summertime. We then coupled our field-based observations, together with transcriptomic analyses of nutrient stress marker genes and ecological models, to evaluate potential mechanisms controlling diazotroph abundance and activity at the mesoscale. Specifically, we evaluated the role of biological (via estimates of growth and grazing rates) and physical controls on populations of Crocosphaera, Trichodesmium, and diatom symbionts. Our results suggest that increased Crocosphaera abundances associated with summertime anticyclones resulted from the alleviation of phosphate limitation, allowing cells to grow at rates exceeding grazing losses. In contrast, distributions of larger, buoyant taxa (Trichodesmium and diatom symbionts) appeared less affected by eddy-driven biological controls. Instead, they appeared driven by physical dynamics along frontal boundaries that separate cyclonic and anticyclonic eddies. Together, the interplay of eddy-specific changes in bottom-up control, top-down control, and the physical accumulation of cells likely explains the elevated diazotroph abundances and NFRs associated with anticyclones and eddy fronts.

Persistent nitrogen depletion in sunlit open ocean waters provides a favorable ecological niche for nitrogen-fixing (diazotrophic) cyanobacteria, some of which associate symbiotically with eukaryotic algae. All known marine examples of these symbioses have involved either centric diatom or haptophyte hosts. We report here the discovery and characterization of two distinct marine pennate diatom-diazotroph symbioses, which until now had only been observed in freshwater environments. Rhopalodiaceae diatoms Epithemia pelagica sp. nov. and Epithemia catenata sp. nov. were isolated repeatedly from the subtropical North Pacific Ocean, and analysis of sequence libraries reveals a global distribution. These symbioses likely escaped attention because the endosymbionts lack fluorescent photopigments, have nifH gene sequences similar to those of free-living unicellular cyanobacteria, and are lost in nitrogen-replete medium. Marine Rhopalodiaceae-diazotroph symbioses are a previously overlooked but widespread source of bioavailable nitrogen in marine habitats and provide new, easily cultured model organisms for the study of organelle evolution.

The microbial fixation of N2is the largest source of biologically available nitrogen (N) to the oceans. However, it is the most energetically expensive N-acquisition process and is believed inhibited when less energetically expensive forms, like dissolved inorganic N (DIN), are available. Curiously, the cosmopolitan N2-fixing UCYN-A/haptophyte symbiosis grows in DIN-replete waters, but the sensitivity of their N2fixation to DIN is unknown. We used stable isotope incubations, catalyzed reporter deposition fluorescence in-situ hybridization (CARD-FISH), and nanoscale secondary ion mass spectrometry (nanoSIMS), to investigate the N source used by the haptophyte host and sensitivity of UCYN-A N2fixation in DIN-replete waters. We demonstrate that under our experimental conditions, the haptophyte hosts of two UCYN-A sublineages do not assimilate nitrate (NO3−) and meet little of their N demands via ammonium (NH4+) uptake. Instead the UCYN-A/haptophyte symbiosis relies on UCYN-A N2fixation to supply large portions of the haptophyte’s N requirements, even under DIN-replete conditions. Furthermore, UCYN-A N2fixation rates, and haptophyte host carbon fixation rates, were at times stimulated by NO3−additions in N-limited waters suggesting a link between the activities of the bulk phytoplankton assemblage and the UCYN-A/haptophyte symbiosis. The results suggest N2fixation may be an evolutionarily viable strategy for diazotroph–eukaryote symbioses, even in N-rich coastal or high latitude waters.

Assessment of the global budget of the greenhouse gas nitrous oxide ( N 2 O) is limited by poor knowledge of the oceanic N 2 O flux to the atmosphere, of which the magnitude, spatial distribution, and temporal variability remain highly uncertain. Here, we reconstruct climatological N 2 O emissions from the ocean by training a supervised learning algorithm with over 158,000 N 2 O measurements from the surface ocean—the largest synthesis to date. The reconstruction captures observed latitudinal gradients and coastal hot spots of N 2 O flux and reveals a vigorous global seasonal cycle. We estimate an annual mean N 2 O flux of 4.2 ± 1.0 Tg N ⋅ y − 1 , 64% of which occurs in the tropics, and 20% in coastal upwelling systems that occupy less than 3% of the ocean area. This N 2 O flux ranges from a low of 3.3 ± 1.3 Tg N ⋅ y − 1 in the boreal spring to a high of 5.5 ± 2.0 Tg N ⋅ y − 1 in the boreal summer. Much of the seasonal variations in global N 2 O emissions can be traced to seasonal upwelling in the tropical ocean and winter mixing in the Southern Ocean. The dominant contribution to seasonality by productive, low-oxygen tropical upwelling systems (>75%) suggests a sensitivity of the global N 2 O flux to El Niño–Southern Oscillation and anthropogenic stratification of the low latitude ocean. This ocean flux estimate is consistent with the range adopted by the Intergovernmental Panel on Climate Change, but reduces its uncertainty by more than fivefold, enabling more precise determination of other terms in the atmospheric N 2 O budget.

Sunlight drives daily rhythms of photosynthesis, growth, and division of photoautotrophs throughout the surface oceans. However, the cascading impacts of oscillatory light input on diverse microbial communities and community-scale metabolism remains unclear. Here we use an unsupervised machine learning approach to show that a small number of diel archetypes can explain pervasive periodic dynamics amongst more than 65,000 distinct time series, including transcriptional activity, macromolecules, lipids, and metabolites from the North Pacific Subtropical Gyre. Overall, we find evidence for synchronous timing of carbon-cycle gene expression that underlie daily oscillations in the concentrations of particulate organic carbon. In contrast, we find evidence of asynchronous timing in gene transcription related to nitrogen metabolism and related metabolic processes consistent with temporal niche partitioning amongst microorganisms in the bacterial and eukaryotic domains.

Dinitrogen (N-2) fixation is an important source of biologically reactive nitrogen (N) to the global ocean. The magnitude of this flux, however, remains uncertain, in part because N-2 fixation rates have been estimated following divergent protocols and because associated levels of uncertainty are seldom reported-confounding comparison and extrapolation of rate measurements. A growing number of reports of relatively low but potentially significant rates of N-2 fixation in regions such as oxygen minimum zones, the mesopelagic water column of the tropical and subtropical oceans, and polar waters further highlights the need for standardized methodological protocols for measurements of N-2 fixation rates and for calculations of detection limits and propagated error terms. To this end, we examine current protocols of the N-15(2) tracer method used for estimating diazotrophic rates, present results of experiments testing the validity of specific practices, and describe established metrics for reporting detection limits. We put forth a set of recommendations for best practices to estimate N-2 fixation rates using N-15(2) tracer, with the goal of fostering transparency in reporting sources of uncertainty in estimates, and to render N-2 fixation rate estimates intercomparable among studies.

Crocosphaera is one of the major N2-fixing microorganisms in the open ocean. On a global scale, the process of N2 fixation is important in balancing the N budget, but the factors governing the rate of N2 fixation remain poorly resolved. Here, we combine a mechanistic model and both previous and present laboratory studies of Crocosphaera to quantify how chemical factors such as C, N, Fe, and O2 and physical factors such as temperature and light affect N2 fixation. Our study shows that Crocosphaera combines multiple mechanisms to reduce intracellular O2 to protect the O2-sensitive N2-fixing enzyme. Our model, however, indicates that these protections are insufficient at low temperature due to reduced respiration and the rate of N2 fixation becomes severely limited. This provides a physiological explanation for why the geographic distribution of Crocosphaera is confined to the warm low-latitude ocean., Crocosphaera is a major dinitrogen (N2)-fixing microorganism, providing bioavailable nitrogen (N) to marine ecosystems. The N2-fixing enzyme nitrogenase is deactivated by oxygen (O2), which is abundant in marine environments. Using a cellular scale model of Crocosphaera sp. and laboratory data, we quantify the role of three O2 management strategies by Crocosphaera sp.: size adjustment, reduced O2 diffusivity, and respiratory protection. Our model predicts that Crocosphaera cells increase their size under high O2. Using transmission electron microscopy, we show that starch granules and thylakoid membranes are located near the cytoplasmic membranes, forming a barrier for O2. The model indicates a critical role for respiration in protecting the rate of N2 fixation. Moreover, the rise in respiration rates and the decline in ambient O2 with temperature strengthen this mechanism in warmer water, providing a physiological rationale for the observed niche of Crocosphaera at temperatures exceeding 20°C. Our new measurements of the sensitivity to light intensity show that the rate of N2 fixation reaches saturation at a lower light intensity (∼100 μmol m−2 s−1) than photosynthesis and that both are similarly inhibited by light intensities of >500 μmol m−2 s−1. This suggests an explanation for the maximum population of Crocosphaera occurring slightly below the ocean surface. IMPORTANCE Crocosphaera is one of the major N2-fixing microorganisms in the open ocean. On a global scale, the process of N2 fixation is important in balancing the N budget, but the factors governing the rate of N2 fixation remain poorly resolved. Here, we combine a mechanistic model and both previous and present laboratory studies of Crocosphaera to quantify how chemical factors such as C, N, Fe, and O2 and physical factors such as temperature and light affect N2 fixation. Our study shows that Crocosphaera combines multiple mechanisms to reduce intracellular O2 to protect the O2-sensitive N2-fixing enzyme. Our model, however, indicates that these protections are insufficient at low temperature due to reduced respiration and the rate of N2 fixation becomes severely limited. This provides a physiological explanation for why the geographic distribution of Crocosphaera is confined to the warm low-latitude ocean.

Trichodesmium is an important dinitrogen (N2)-fixing cyanobacterium in marine ecosystems. Recent nucleic acid analyses indicate that Trichodesmium colonies with their diverse epibionts support various nitrogen (N) transformations beyond N2 fixation. However, rates of these transformations and concentration gradients of N compounds in Trichodesmium colonies remain largely unresolved. We combined isotope-tracer incubations, micro-profiling and numeric modelling to explore carbon fixation, N cycling processes as well as oxygen, ammonium and nitrate concentration gradients in individual field-sampled Trichodesmium colonies. Colonies were net-autotrophic, with carbon and N2 fixation occurring mostly during the day. Ten percent of the fixed N was released as ammonium after 12-h incubations. Nitrification was not detectable but nitrate consumption was high when nitrate was added. The consumed nitrate was partly reduced to ammonium, while denitrification was insignificant. Thus, the potential N transformation network was characterised by fixed N gain and recycling processes rather than denitrification. Oxygen concentrations within colonies were ~60–200% air-saturation. Moreover, our modelling predicted steep concentration gradients, with up to 6-fold higher ammonium concentrations, and nitrate depletion in the colony centre compared to the ambient seawater. These gradients created a chemically heterogeneous microenvironment, presumably facilitating diverse microbial metabolisms in millimetre-sized Trichodesmium colonies.

Crocosphaera is a major dinitrogen (N2)-fixing microorganism, providing bioavailable nitrogen (N) to marine ecosystems. The N2-fixing enzyme nitrogenase is deactivated by oxygen (O2), which is abundant in marine environments. Using a cellular scale model of Crocosphaera sp. and laboratory data, we quantify the role of three O2 management strategies by Crocosphaera sp.: size adjustment, reduced O2 diffusivity, and respiratory protection. Our model predicts that Crocosphaera cells increase their size under high O2. Using transmission electron microscopy, we show that starch granules and thylakoid membranes are located near the cytoplasmic membranes, forming a barrier for O2. The model indicates a critical role for respiration in protecting the rate of N2 fixation. Moreover, the rise in respiration rates and the decline in ambient O2 with temperature strengthen this mechanism in warmer water, providing a physiological rationale for the observed niche of Crocosphaera at temperatures exceeding 20°C. Our new measurements of the sensitivity to light intensity show that the rate of N2 fixation reaches saturation at a lower light intensity (∼100 μmol m−2 s−1) than photosynthesis and that both are similarly inhibited by light intensities of >500 μmol m−2 s−1. This suggests an explanation for the maximum population of Crocosphaera occurring slightly below the ocean surface. IMPORTANCECrocosphaera is one of the major N2-fixing microorganisms in the open ocean. On a global scale, the process of N2 fixation is important in balancing the N budget, but the factors governing the rate of N2 fixation remain poorly resolved. Here, we combine a mechanistic model and both previous and present laboratory studies of Crocosphaera to quantify how chemical factors such as C, N, Fe, and O2 and physical factors such as temperature and light affect N2 fixation. Our study shows that Crocosphaera combines multiple mechanisms to reduce intracellular O2 to protect the O2-sensitive N2-fixing enzyme. Our model, however, indicates that these protections are insufficient at low temperature due to reduced respiration and the rate of N2 fixation becomes severely limited. This provides a physiological explanation for why the geographic distribution of Crocosphaera is confined to the warm low-latitude ocean.

Net community production (NCP) constrains the amount of carbon that is available for storage within or export from, the photic zone of marine ecosystems. With the aim of studying the control exerted by microbial community respiration (MCR) and gross primary production (GPP) over NCP, short-term variability in rates of MCR, GPP and NCP were measured over a 13-day sampling period (August 23–September 4, 2012) at Station ALOHA. During this period, picoplankton abundances and concentrations of photosynthetic pigments demonstrated weak to moderate decreases coincident with the passage of a low salinity water mass through the sampling area. During the same period, rates of MCR, measured using the in vivo INT method, varied by 2.7-fold. Rates of primary production (PP) were estimated based on four different methodologies: Fast Repetition Rate Fluorometry (FRRF), 14C-bicarbonate assimilation, diel changes in mixed layer O2 concentrations based on Seaglider measurements, and isotopic composition (17ΔO2) of dissolved O2. Remarkably, these different methods for measuring microbial metabolism were consistent, suggesting that collectively these different approaches provide an accurate constraint on ecosystem metabolism, despite the different time and space scales over which these measurements integrate. FRRF-derived estimates of PP, which were similar in magnitude to 14C-based-PP, were significantly correlated with variability in mixed layer MCR. None of the other independent measurements of PP demonstrated significant relationships to MCR. Day-to-day variability in MCR and bacterial growth efficiency (BGE), derived based on measurements of bacterial production (as estimated by 3H-leucine incorporation) and MCR, were related to changes in NCP estimated from O2/Ar ratios (O2/Ar-NCP), suggesting short-term variability in the efficiency with which microorganisms consume dissolved organic matter exerts direct control on rates of NCP in this ecosystem. Our results highlight internal consistency among the derived rates of ecosystem metabolism using a suite of different methodologies to estimate productivity and respiration. Moreover, we find that rates of MCR can be as variable as PP and that variability in MCR may regulate NCP in this ecosystem.

The microbial fixation of N

Gradients of oxygen (O-2) and pH, as well as small-scale fluxes of carbon (C), nitrogen (N) and O-2 were investigated under different partial pressures of carbon dioxide (pCO(2)) in field-collected colonies of the marine dinitrogen (N-2)-fixing cyanobacterium Trichodesmium. Microsensor measurements indicated that cells within colonies experienced large fluctuations in O-2, pH and CO2 concentrations over a day-night cycle. O-2 concentrations varied with light intensity and time of day, yet colonies exposed to light were supersaturated with O-2 (up to similar to 200%) throughout the light period and anoxia was not detected. Alternating between light and dark conditions caused a variation in pH levels by on average 0.5 units (equivalent to 15 nmol l(-1) proton concentration). Single-cell analyses of C and N assimilation using secondary ion mass spectrometry (SIMS; large geometry SIMS and nanoscale SIMS) revealed high variability in metabolic activity of single cells and trichomes of Trichodesmium, and indicated transfer of C and N to colony-associated non-photosynthetic bacteria. Neither O-2 fluxes nor C fixation by Trichodesmium were significantly influenced by short-term incubations under different pCO(2) levels, whereas N-2 fixation increased with increasing pCO(2). The large range of metabolic rates observed at the single-cell level may reflect a response by colony-forming microbial populations to highly variable microenvironments.

Populations of nitrogen-fixing cyanobacteria in the genus Trichodesmium are critical to ocean ecosystems, yet predicting patterns of Trichodesmium distribution and their role in ocean biogeochemistry is an ongoing challenge. This may, in part, be due to differences in the physiological ecology of Trichodesmium species, which are not typically considered independently in field studies. In this study, the abundance of the two dominant Trichodesmium clades (Clade I and Clade III) was investigated during a survey at Station ALOHA in the North Pacific Subtropical Gyre (NPSG) using a clade-specific qPCR approach. While Clade I dominated the Trichodesmium community, Clade III abundance was >50% in some NPSG samples, in contrast to the western North Atlantic where Clade III abundance was always 80 m, while Clade III populations were only observed in the mixed layer and found to be significantly correlated with depth and temperature. These data suggest active niche partitioning of Trichodesmium species from different clades, as has been observed in other cyanobacteria. Tracking the distribution and physiology of Trichodesmium spp. would contribute to better predictions of the physiological ecology of this biogeochemically important genus in the present and future ocean.

Trichodesmium is a major nitrogen-fixing cyanobacterium and exerts a significant influence on the oceanic nitrogen cycle. It is also a widely used model organism in laboratory studies. Since the nitrogen-fixing enzyme nitrogenase is extremely sensitive to oxygen, how these surface-dwelling plankton manage the two conflicting processes of nitrogen fixation and photosynthesis has been a long-standing question. In this study, we developed a simple model of metabolic fluxes of Trichodesmium capturing observed daily cycles of photosynthesis, nitrogen fixation, and boundary layer oxygen concentrations. The model suggests that forming a chain of cells for spatially segregating nitrogen fixation and photosynthesis is essential but not sufficient. It also requires a barrier against oxygen diffusion and high rates of oxygen scavenging by respiration. Finally, the model indicates that the life span of intracellular oxygen is extremely short, thus enabling cells to instantly create a low-oxygen environment upon deactivation of photosynthesis., The cyanobacterium Trichodesmium is an important contributor of new nitrogen (N) to the surface ocean, but its strategies for protecting the nitrogenase enzyme from inhibition by oxygen (O2) remain poorly understood. We present a dynamic physiological model to evaluate hypothesized conditions that would allow Trichodesmium to carry out its two conflicting metabolic processes of N2 fixation and photosynthesis. First, the model indicates that managing cellular O2 to permit N2 fixation requires high rates of respiratory O2 consumption. The energetic cost amounts to ∼80% of daily C fixation, comparable to the observed diminution of the growth rate of Trichodesmium relative to other phytoplankton. Second, by forming a trichome of connected cells, Trichodesmium can segregate N2 fixation from photosynthesis. The transfer of stored C to N-fixing cells fuels the respiratory O2 consumption that protects nitrogenase, while the reciprocal transfer of newly fixed N to C-fixing cells supports cellular growth. Third, despite Trichodesmium lacking the structural barrier found in heterocystous species, the model predicts low diffusivity of cell membranes, a function that may be explained by the presence of Gram-negative membrane, production of extracellular polysaccharide substances (EPS), and “buffer cells” that intervene between N2-fixing and photosynthetic cells. Our results suggest that all three factors—respiratory protection, trichome formation, and diffusion barriers—represent essential strategies that, despite their energetic costs, facilitate the growth of Trichodesmium in the oligotrophic aerobic ocean and permit it to be a major source of new reactive nitrogen. IMPORTANCE Trichodesmium is a major nitrogen-fixing cyanobacterium and exerts a significant influence on the oceanic nitrogen cycle. It is also a widely used model organism in laboratory studies. Since the nitrogen-fixing enzyme nitrogenase is extremely sensitive to oxygen, how these surface-dwelling plankton manage the two conflicting processes of nitrogen fixation and photosynthesis has been a long-standing question. In this study, we developed a simple model of metabolic fluxes of Trichodesmium capturing observed daily cycles of photosynthesis, nitrogen fixation, and boundary layer oxygen concentrations. The model suggests that forming a chain of cells for spatially segregating nitrogen fixation and photosynthesis is essential but not sufficient. It also requires a barrier against oxygen diffusion and high rates of oxygen scavenging by respiration. Finally, the model indicates that the life span of intracellular oxygen is extremely short, thus enabling cells to instantly create a low-oxygen environment upon deactivation of photosynthesis.

Ocean greening off Hawai'i From June to August 2018, the eruption of Kīlauea volcano triggered a diatom-dominated phytoplankton bloom. Wilson et al. set sail to sample the plume, deploying subsea gliders and using satellite monitoring to measure the dynamics of this rare event in the nutrient-poor Pacific (see the Perspective by Ducklow and Plank). They found subsurface chlorophyll maxima not visible by remote sensing, performed transcriptome and N isotope marker analysis, and measured nutrients, partitioning of biomass into different organisms, and primary production. Much of the data are corroborated by physical modeling of the ocean dynamics. The authors conclude that the plume was fed by the lava heating subsurface water and triggering upwelling of deepwater nutrients to the surface rather than by direct injection of micronutrients from lava. Science , this issue p. 1040 ; see also p. 978

The cyanobacterium Prochlorococcus is the dominant phototroph in surface waters of the vast oligotrophic oceans, the foundation of marine food webs, and an important component of global biogeochemical cycles. The prominence of Prochlorococcus across the environmental gradients of the open ocean is attributed to its extensive genetic diversity and flexible chlorophyll physiology, enabling light capture over a wide range of intensities. What remains unknown is the balance between temporal dynamics of genetic diversity and chlorophyll physiology in the ability of Prochlorococcus to respond to a variety of short (approximately one day) and longer (months to year) changes in the environment. Previous field research established depth-dependent Prochlorococcus single cell chlorophyll distributions in the North Pacific Subtropical Gyre. Here, we examined whether the shifts in chlorophyll distributions correspond to changes in Prochlorococcus genetic diversity (i.e. ecotype-level community structure) or photoacclimation of stable communities over short time intervals. We report that community structure was relatively stable despite abrupt shifts in Prochlorococcus chlorophyll physiology, due to unexpected physiological plasticity of high-light adapted Prochlorococcus ecotypes. Through comparison with seasonal-scale changes, our data suggest that variability on daily scales triggers shifts in Prochlorococcus photoacclimation, while seasonal-scale dynamics trigger shifts in community structure. Together, these data highlight the importance of incorporating the process of photoacclimation and chlorophyll dynamics into interpretations of phytoplankton population dynamics from chlorophyll data as well as the importance of daily-scale variability to Prochlorococcus ecology.

The overarching logistical challenge in microbial oceanography is acquiring enough samples to provide meaningful scientific interpretation. The number of samples collected during ship expeditions is limited by weather, time on station, and budget. Here we describe a robotic, autonomous vehicle platform equipped with a unique sampling instrument that mitigates some of these constraints. In a joint cruise on the R/V Falkor, the Monterey Bay Aquarium Research Institute and the University of Hawaii deployed two of these vehicles in a mesoscale eddy north of the island of Maui. One vehicle collected contextual measurements while circling a freely drifting sampling vehicle. On the sampling vehicle we implemented several behaviors, including sampling every three hours for a 4-day underwater drift while maintaining position within the deep chlorophyll maximum layer (~100m). Results demonstrate the ability to remain with features of interest and point to an exciting future of long-term, directed, persistent sampling.

Marine microbial communities are critical for biogeochemical cycles and the productivity of ocean ecosystems. Primary productivity in the surface ocean is constrained by nutrients which are supplied, in part, by mixing with deeper water. Little is known about the time scales, frequency, or impact of mixing on microbial communities. We combined in situ sampling using the Environmental Sample Processor and a small-scale mixing experiment with lower euphotic zone water to determine how individual populations respond to mixing. Transcriptional responses were measured using the MicroTOOLs (Microbiological Targets for Ocean Observing Laboratories) microarray, which targets all three domains of life and viruses. The experiment showed that mixing substantially affects photosynthetic taxa as expected, but surprisingly also showed that populations respond differently to unfiltered deep water which contains particles (organisms and detritus) compared to filtered deep water that only contains nutrients and viruses, pointing to the impact of biological interactions associated with these events. Comparison between experimental and in situ population transcription patterns indicated that manipulated populations can serve as analogs for natural populations, and that natural populations may be frequently or continuously responding to nutrients from deeper waters. Finally, this study also shows that the microarray approach, which is complementary to metatranscriptomic sequencing, is useful for determining the physiological status of in situ microbial communities.

Despite increasing acknowledgment that microorganisms underpin the healthy functioning of basically all multicellular life, few cross-disciplinary teams address the diversity and function of microbiota across organisms and ecosystems. Our newly formed consortium of junior faculty spanning fields such as ecology and geoscience to mathematics and molecular biology from the University of Hawai‘i at Mānoa aims to fill this gap., Despite increasing acknowledgment that microorganisms underpin the healthy functioning of basically all multicellular life, few cross-disciplinary teams address the diversity and function of microbiota across organisms and ecosystems. Our newly formed consortium of junior faculty spanning fields such as ecology and geoscience to mathematics and molecular biology from the University of Hawai‘i at Mānoa aims to fill this gap. We are united in our mutual interest in advancing a new paradigm for biology that incorporates our modern understanding of the importance of microorganisms. As our first concerted research effort, we will assess the diversity and function of microbes across an entire watershed on the island of Oahu, Hawai‘i. Due to its high ecological diversity across tractable areas of land and sea, Hawai‘i provides a model system for the study of complex microbial communities and the processes they mediate. Owing to our diverse expertise, we will leverage this study system to advance the field of biology.

©2015. American Geophysical Union. All Rights Reserved. Time-series observations are critical to understand the structure, function, and dynamics of marine ecosystems. The Hawaii Ocean Time-series program has maintained near-monthly sampling at Station ALOHA (22°45′N, 158°00′W) in the oligotrophic North Pacific Subtropical Gyre (NPSG) since 1988 and has identified ecosystem variability over seasonal to interannual timescales. To further extend the temporal resolution of these near-monthly time-series observations, an extensive field campaign was conducted during July-September 2012 at Station ALOHA with near-daily sampling of upper water-column biogeochemistry, phytoplankton abundance, and activity. The resulting data set provided biogeochemical measurements at high temporal resolution and documents two important events at Station ALOHA: (1) a prolonged period of low productivity when net community production in the mixed layer shifted to a net heterotrophic state and (2) detection of a distinct sea-surface salinity minimum feature which was prominent in the upper water column (0-50 m) for a period of approximately 30 days. The shipboard observations during July-September 2012 were supplemented with in situ measurements provided by Seagliders, profiling floats, and remote satellite observations that together revealed the extent of the low productivity and the sea-surface salinity minimum feature in the NPSG.

One challenge in field-based marine microbial ecology is to achieve sufficient spatial resolution to obtain representative information about microbial distributions and biogeochemical processes. The challenges are exacerbated when conducting rate measurements of biological processes due to potential perturbations during sampling and incubation. Here we present the first application of a robotic microlaboratory, the 4 L-submersible incubation device (SID), for conducting in situ measurements of the rates of biological nitrogen (N2) fixation (BNF). The free-drifting autonomous instrument obtains samples from the water column that are incubated in situ after the addition of 15N2 tracer. After each of up to four consecutive incubation experiments, the 4-L sample is filtered and chemically preserved. Measured BNF rates from two deployments of the SID in the oligotrophic North Pacific ranged from 0.8 to 2.8 nmol N L?1 day?1, values comparable with simultaneous rate measurements obtained using traditional conductivity–temperature–depth (CTD)–rosette sampling followed by on-deck or in situ incubation. Future deployments of the SID will help to better resolve spatial variability of oceanic BNF, particularly in areas where recovery of seawater samples by CTD compromises their integrity, e.g. anoxic habitats.

Using autonomous underwater gliders, we quantified diurnal periodicity in dissolved oxygen, chlorophyll, and temperature in the subtropical North Pacific near the Hawaii Ocean Time-series (HOT) Station ALOHA during summer 2012. Oxygen optodes provided sufficient stability and precision to quantify diel cycles of average amplitude of 0.6 µmol kg−1. A theoretical diel curve was fit to daily observations to infer an average mixed layer gross primary productivity (GPP) of 1.8 mmol O2 m−3 d−1. Cumulative net community production (NCP) over 110 days was 500 mmol O2 m−2 for the mixed layer, which averaged 57 m in depth. Both GPP and NCP estimates indicated a significant period of below-average productivity at Station ALOHA in 2012, an observation confirmed by 14C productivity incubations and O2/Ar ratios. Given our success in an oligotrophic gyre where biological signals are small, our diel GPP approach holds promise for remote characterization of productivity across the spectrum of marine environments.