Diversity in the utilization of different molecular classes of dissolved organic matter by heterotrophic marine bacteria.

Heterotrophic marine bacteria utilize and recycle dissolved organic matter (DOM), impacting biogeochemical cycles. It is currently unclear to what extent distinct DOM components can be used by different heterotrophic clades. Here, we ask how a natural microbial community from the Eastern Mediterranean Sea (EMS) responds to different molecular classes of DOM (peptides, amino acids, amino sugars, disaccharides, monosaccharides, and organic acids) comprising much of the biomass of living organisms. Bulk bacterial activity increased after 24 h for all treatments relative to the control, while glucose and ATP uptake decreased or remained unchanged. Moreover, while the per-cell uptake rate of glucose and ATP decreased, that of Leucin significantly increased for amino acids, reflecting their importance as common metabolic currencies in the marine environment. Pseudoalteromonadaceae dominated the peptides treatment, while different Vibrionaceae strains became dominant in response to amino acids and amino sugars. Marinomonadaceae grew well on organic acids, and Alteromonadaseae on disaccharides. A comparison with a recent laboratory-based study reveals similar peptide preferences for Pseudoalteromonadaceae, while Alteromonadaceae, for example, grew well in the lab on many substrates but dominated in seawater samples only when disaccharides were added. We further demonstrate a potential correlation between the genetic capacity for degrading amino sugars and the dominance of specific clades in these treatments. These results highlight the diversity in DOM utilization among heterotrophic bacteria and complexities in the response of natural communities. IMPORTANCE: A major goal of microbial ecology is to predict the dynamics of natural communities based on the identity of the organisms, their physiological traits, and their genomes. Our results show that several clades of heterotrophic bacteria each grow in response to one or more specific classes of organic matter. For some clades, but not others, growth in a complex community is similar to that of isolated strains in laboratory monoculture. Additionally, by measuring how the entire community responds to various classes of organic matter, we show that these results are ecologically relevant, and propose that some of these resources are utilized through common uptake pathways. Tracing the path between different resources to the specific microbes that utilize them, and identifying commonalities and differences between different natural communities and between them and lab cultures, is an important step toward understanding microbial community dynamics and predicting how communities will respond to perturbations.

A model of time-dependent macromolecular and elemental composition of phytoplankton.

Phytoplankton Chl:C:N:P ratios are important from both an ecological and a biogeochemical perspective. We show that these elemental ratios can be represented by a phytoplankton physiological model of low complexity that includes major cellular macromolecular pools. In particular, our model resolves time-dependent intracellular pools of chlorophyll, proteins, nucleic acids, carbohydrates/lipids, and N and P storage. Batch culture data for two diatom and two prasinophyte species are used to constrain parameters that represent specific allocation traits and strategies. A key novelty is the simultaneous estimation of physiological parameters for two phytoplankton groups of such different sizes. The number of free parameters is reduced by assuming (i) allometric scaling for maximum uptake rates, (ii) shared half-saturation constants for synthesis of functional macromolecules, (iii) shared exudation rates of functional macromolecules across the species. The rationale behind this assumption is that across the different species, the same or similar processes, enzymes, and metabolites play a role in key physiological processes. For the turnover numbers of macromolecular synthesis and storage exudation rates, differences between diatoms and prasinophytes need to be taken into account to obtain a good fit. Our model fits suggest that the parameters related to storage dynamics dominate the differences in the C:N:P ratios between the different phytoplankton groups. Since descriptions of storage dynamics are still incomplete and imprecise, predictions of C:N:P ratios by phytoplankton models likely have a large uncertainty.

Testing the growth rate and translation compensation hypotheses in marine bacterioplankton.

Two different hypotheses have been raised as to how temperature affects resource allocation in microorganisms. The translation-compensation hypothesis (TCH) predicts that the increase in enzymatic efficiency with temperature results in fewer required ribosomes per cell and lower RNA:protein ratio. In contrast, the growth rate hypothesis (GRH) predicts that increasing the growth rate with temperature requires more ribosomes and hence a higher cellular RNA:protein. We tested these two hypotheses in laboratory cultures of Prochlorococcus and Alteromonas as well as over an annual cycle in the Eastern Mediterranean Sea. The RNA:protein of Alteromonas mostly decreased with temperature in accordance with the TCH, while that of Prochlorococcus increased with temperature, as predicted by the GRH. No support was found for either hypothesis in surface waters from the Eastern Mediterranean, whereas the fraction of phosphorus in RNA was positively correlated with per-cell bacterial production in the deep chlorophyll maximum, supporting the GRH in this niche. A considerable part of the cellular phosphorus was not allocated to RNA, DNA, phospholipids or polyphosphate, raising the question which cellular molecules contain these P reserves. While macromolecular quotas differed significantly between laboratory cultures and field samples, these were connected through a power law, suggesting common rules of resource allocation.

Phytoplankton Producer Species and Transformation of Released Compounds over Time Define Bacterial Communities following Phytoplankton Dissolved Organic Matter Pulses.

Phytoplankton-bacterium interactions are mediated, in part, by phytoplankton-released dissolved organic matter (DOMp). Two factors that shape the bacterial community accompanying phytoplankton are (i) the phytoplankton producer species, defining the initial composition of released DOMp, and (ii) the DOMp transformation over time. We added phytoplankton DOMp from the diatom Skeletonema marinoi and the cyanobacterium Prochlorococcus marinus MIT9312 to natural bacterial communities from the eastern Mediterranean and determined the bacterial responses over a time course of 72 h in terms of cell numbers, bacterial production, alkaline phosphatase activity, and changes in active bacterial community composition based on rRNA amplicon sequencing. Both DOMp types were demonstrated to serve the bacterial community as carbon and, potentially, phosphorus sources. Bacterial communities in diatom-derived DOM treatments maintained higher Shannon diversities throughout the experiment and yielded higher bacterial production and lower alkaline phosphatase activity compared to cyanobacterium-derived DOM after 24 h of incubation (but not after 48 and 72 h), indicating greater bacterial usability of diatom-derived DOM. Bacterial communities significantly differed between DOMp types as well as between different incubation times, pointing to a certain bacterial specificity for the DOMp producer as well as a successive utilization of phytoplankton DOM by different bacterial taxa over time. The highest differences in bacterial community composition with DOMp types occurred shortly after DOMp additions, suggesting a high specificity toward highly bioavailable DOMp compounds. We conclude that phytoplankton-associated bacterial communities are strongly shaped by the phytoplankton producer as well as the transformation of its released DOMp over time. IMPORTANCE Phytoplankton-bacterium interactions influence biogeochemical cycles of global importance. Phytoplankton photosynthetically fix carbon dioxide and subsequently release the synthesized compounds as dissolved organic matter (DOMp), which becomes processed and recycled by heterotrophic bacteria. Yet the importance of phytoplankton producers in combination with the time-dependent transformation of DOMp compounds on the accompanying bacterial community has not been explored in detail. The diatom Skeletonema marinoi and the cyanobacterium Prochlorococcus marinus MIT9312 belong to globally important phytoplankton genera, and our study revealed that DOMp of both species was selectively incorporated by the bacterial community. The producer species had the highest impact shortly after DOMp appropriation, and its effect diminished over time. Our results improve the understanding of the dynamics of organic matter produced by phytoplankton in the oceans as it is utilized and modified by cooccurring bacteria.

Phytoplankton exudates provide full nutrition to a subset of accompanying heterotrophic bacteria via carbon, nitrogen and phosphorus allocation.

Marine bacteria rely on phytoplankton exudates as carbon sources (DOCp). Yet, it is unclear to what extent phytoplankton exudates also provide nutrients such as phytoplankton-derived N and P (DONp, DOPp). We address these questions by mesocosm exudate addition experiments with spent media from the ubiquitous pico-cyanobacterium Prochlorococcus to bacterial communities in contrasting ecosystems in the Eastern Mediterranean - a coastal and an open-ocean, oligotrophic station with and without on-top additions of inorganic nutrients. Inorganic nutrient addition did not lower the incorporation of exudate DONp, nor did it reduce alkaline phosphatase activity, suggesting that bacterial communities are able to exclusively cover their nitrogen and phosphorus demands with organic forms provided by phytoplankton exudates. Approximately half of the cells in each ecosystem took up detectable amounts of Prochlorococcus-derived C and N, yet based on 16S rRNA sequencing different bacterial genera were responsible for the observed exudate utilization patterns. In the coastal community, several phylotypes of Aureimarina, Psychrosphaera and Glaciecola responded positively to the addition of phytoplankton exudates, whereas phylotypes of Pseudoalteromonas increased and dominated the open-ocean communities. Together, our results strongly indicate that phytoplankton exudates provide coastal and open-ocean bacterial communities with organic carbon, nitrogen and phosphorus, and that phytoplankton exudate serve a full-fledged meal for the accompanying bacterial community in the nutrient-poor eastern Mediterranean.

Microbe Profile: Alteromonas macleodii - a widespread, fast-responding, 'interactive' marine bacterium.

Alteromonas macleodii is a marine heterotrophic bacterium with widespread distribution - from temperate to tropical oceans, and from surface to deep waters. Strains of A. macleodii exhibit considerable genomic and metabolic variability, and can grow rapidly on diverse organic compounds. A. macleodii is a model organism for the study of population genomics, physiological adaptations and microbial interactions, with individual genomes encoding diverse phenotypic traits influenced by recombination and horizontal gene transfer.

Particle-associated and free-living bacterial communities in an oligotrophic sea are affected by different environmental factors.

In the oceans and seas, environmental conditions change over multiple temporal and spatial scales. Here, we ask what factors affect the bacterial community structure across time, depth and size fraction during six seasonal cruises (2 years) in the ultra-oligotrophic Eastern Mediterranean Sea. The bacterial community varied most between size fractions (free-living (FL) vs. particle-associated), followed by depth and finally season. The FL community was taxonomically richer and more stable than the particle-associated (PA) one, which was characterized by recurrent 'blooms' of heterotrophic bacteria such as Alteromonas and Ralstonia. The heterotrophic FL and PA communities were also correlated with different environmental parameters: the FL population correlated with depth and phytoplankton, whereas PA bacteria were correlated primarily with the time of sampling. A significant part of the variability in community structure could, however, not be explained by the measured parameters. The metabolic potential of the PA community, predicted from 16S rRNA amplicon data using PICRUSt, was enriched in pathways associated with the degradation and utilization of biological macromolecules, as well as plastics, other petroleum products and herbicides. The FL community was enriched in predicted pathways for the metabolism of inositol phosphate, a potential phosphorus source, and of polycyclic aromatic hydrocarbons.

Conservation and turnover of miRNAs and their highly complementary targets in early branching animals.

MicroRNAs (miRNAs) are crucial post-transcriptional regulators that have been extensively studied in Bilateria, a group comprising the majority of extant animals, where more than 30 conserved miRNA families have been identified. By contrast, bilaterian miRNA targets are largely not conserved. Cnidaria is the sister group to Bilateria and thus provides a unique opportunity for comparative studies. Strikingly, like their plant counterparts, cnidarian miRNAs have been shown to predominantly have highly complementary targets leading to transcript cleavage by Argonaute proteins. Here, we assess the conservation of miRNAs and their targets by small RNA sequencing followed by miRNA target prediction in eight species of Anthozoa (sea anemones and corals), the earliest-branching cnidarian class. We uncover dozens of novel miRNAs but only a few conserved ones. Further, given their high complementarity, we were able to computationally identify miRNA targets in each species. Besides evidence for conservation of specific miRNA target sites, which are maintained between sea anemones and stony corals across 500 Myr of evolution, we also find indications for convergent evolution of target regulation by different miRNAs. Our data indicate that cnidarians have only few conserved miRNAs and corresponding targets, despite their high complementarity, suggesting a high evolutionary turnover.

A tentacle for every occasion: comparing the hunting tentacles and sweeper tentacles, used for territorial competition, in the coral Galaxea fascicularis.

BACKGROUND: Coral reefs are among the most diverse, complex and densely populated marine ecosystems. To survive, morphologically simple and sessile cnidarians have developed mechanisms to catch prey, deter predators and compete with adjacent corals for space, yet the mechanisms underlying these functions are largely unknown. Here, we characterize the histology, toxic activity and gene expression patterns in two different types of tentacles from the scleractinian coral Galaxea fascilcularis - catch tentacles (CTs), used to catch prey and deter predators, and sweeper tentacles (STs), specialized tentacles used for territorial aggression. RESULTS: STs exhibit more mucocytes and higher expression of mucin genes than CTs, and lack the ectodermal cilia used to deliver food to the mouth and remove debris. STs and CTs also express different sensory rhodopsin-like g-protein coupled receptors, suggesting they may employ different sensory pathways. Each tentacle type has a different complement of stinging cells (nematocytes), and the expression in the two tentacles of genes encoding structural nematocyte proteins suggests the stinging cells develop within the tentacles. CTs have higher neurotoxicity to blowfly larvae and hemolytic activity compared to the STs, consistent with a role in prey capture. In contrast, STs have higher phospholipase A2 activity, which we speculate may have a role in inducing tissue damage during territorial aggression. The expression of genes encoding cytolytic toxins (actinoporins) and phospholipases also differs between the tentacle types. CONCLUSIONS: These results show that the same organism utilizes two distinct tentacle types, each equipped with a different venom apparatus and toxin composition, for prey capture and defense and for territorial aggression.

Metagenomic analysis reveals unusually high incidence of proteorhodopsin genes in the ultraoligotrophic Eastern Mediterranean Sea.

Sunlight can be directly harvested by photoheterotrophic bacteria to create a pH gradient across the membrane, which can then be utilized to produce ATP. Despite the potential importance of this trophic strategy, when and where such organisms are found in the seas and oceans is poorly described. Here, we describe the abundance and taxonomy of bacteria with different trophic strategies (heterotrophs, phototrophs and photoheterotrophs) in contrasting water masses of the ultra-oligotrophic eastern Mediterranean Sea. These water bodies, an anticyclonic eddy and a high-chlorophyll patch resulting from transport of nutrient-rich coastal waters into offshore oligotrophic waters, each supported different microbial populations in surface waters. Based on infrared microscopy and metagenomics, aerobic anoxygenic photoheterotrophic (AAP) bacteria represented up to 10.4% of the microbial community. In contrast, the proteorhodopsin (PR) gene was found in 78.6%-118.8% of the bacterial genome equivalents, the highest abundance reported to date. These results suggest that PR-mediated photoheterotrophy may be especially important in oligotrophic, potentially phosphate-limited conditions.

The dynamically evolving nematocyst content of an anthozoan, a scyphozoan, and a hydrozoan.

Nematocytes, the stinging cells of cnidarians, are the most evolutionarily ancient venom apparatus. These nanosyringe-like weaponry systems reach pressures of approximately 150 atmospheres before discharging and punching through the outer layer of the prey or predator at accelerations of more than 5 million g, making them one of the fastest biomechanical events known. To gain better understanding of the function of the complex, phylum-specific nematocyst organelle, and its venom payload, we compared the soluble nematocyst's proteome from the sea anemone Anemonia viridis, the jellyfish Aurelia aurita, and the hydrozoan Hydra magnipapillata, each belonging to one of the three basal cnidarian lineages which diverged over 600 Ma. Although the basic morphological and functional characteristics of the nematocysts of the three organisms are similar, out of hundreds of proteins identified in each organism, only six are shared. These include structural proteins, a chaperone which may help maintain venon activity over extended periods, and dickkopf, an enigmatic Wnt ligand which may also serve as a toxin. Nevertheless, many protein domains are shared between the three organisms' nematocyst content suggesting common proteome functionalities. The venoms of Hydra and Aurelia appear to be functionally similar and composed mainly of cytotoxins and enzymes, whereas the venom of the Anemonia is markedly unique and based on peptide neurotoxins. Cnidarian venoms show evidence for functional recruitment, yet evidence for diversification through positive selection, common to other venoms, is lacking. The final injected nematocyst payload comprises a mixture of dynamically evolving proteins involved in the development, maturation, maintenance, and discharge of the nematocysts, which is unique to each organism and potentially to each nematocyst type.

AdE-1, a new inotropic Na(+) channel toxin from Aiptasia diaphana, is similar to, yet distinct from, known anemone Na(+) channel toxins.

Heart failure is one of the most prevalent causes of death in the western world. Sea anemone contains a myriad of short peptide neurotoxins affecting many pharmacological targets, several of which possess cardiotonic activity. In the present study we describe the isolation and characterization of AdE-1 (ion channel modifier), a novel cardiotonic peptide from the sea anemone Aiptasia diaphana, which differs from other cnidarian toxins. Although AdE-1 has the same cysteine residue arrangement as sea anemone type 1 and 2 Na(+) channel toxins, its sequence contains many substitutions in conserved and essential sites and its overall homology to other toxins identified to date is low (<36%). Physiologically, AdE-1 increases the amplitude of cardiomyocyte contraction and slows the late phase of the twitch relaxation velocity with no induction of spontaneous twitching. It increases action potential duration of cardiomyocytes with no effect on its threshold and on the cell's resting potential. Similar to other sea anemone Na(+) channel toxins such as Av2 (Anemonia viridis toxin II), AdE-1 markedly inhibits Na(+) current inactivation with no significant effect on current activation, suggesting a similar mechanism of action. However, its effects on twitch relaxation velocity, action potential amplitude and on the time to peak suggest that this novel toxin affects cardiomyocyte function via a more complex mechanism. Additionally, Av2's characteristic delayed and early after-depolarizations were not observed. Despite its structural differences, AdE-1 physiologic effectiveness is comparable with Av2 with a similar ED(50) value to blowfly larvae. This finding raises questions regarding the extent of the universality of structure-function in sea anemone Na(+) channel toxins.

Catalytic promiscuity in the biosynthesis of cyclic peptide secondary metabolites in planktonic marine cyanobacteria.

Our understanding of secondary metabolite production in bacteria has been shaped primarily by studies of attached varieties such as symbionts, pathogens, and soil bacteria. Here we show that a strain of the single-celled, planktonic marine cyanobacterium Prochlorococcus-which conducts a sizable fraction of photosynthesis in the oceans-produces many cyclic, lanthionine-containing peptides (lantipeptides). Remarkably, in Prochlorococcus MIT9313 a single promiscuous enzyme transforms up to 29 different linear ribosomally synthesized peptides into a library of polycyclic, conformationally constrained products with highly diverse ring topologies. Genes encoding this system are found in variable abundances across the oceans-with a hot spot in a Galapagos hypersaline lagoon-suggesting they play a habitat- and/or community-specific role. The extraordinarily efficient pathway for generating structural diversity enables these cyanobacteria to produce as many secondary metabolites as model antibiotic-producing bacteria, but with much smaller genomes.

Phototroph-heterotroph interactions during growth and long-term starvation across Prochlorococcus and Alteromonas diversity.

Due to their potential impact on ecosystems and biogeochemistry, microbial interactions, such as those between phytoplankton and bacteria, have been studied intensively using specific model organisms. Yet, to what extent interactions differ between closely related organisms, or how these interactions change over time, or culture conditions, remains unclear. Here, we characterize the interactions between five strains each of two globally abundant marine microorganisms, Prochlorococcus (phototroph) and Alteromonas (heterotroph), from the first encounter between individual strains and over more than a year of repeated cycles of exponential growth and long-term nitrogen starvation. Prochlorococcus-Alteromonas interactions had little effect on traditional growth parameters such as Prochlorococcus growth rate, maximal fluorescence, or lag phase, affecting primarily the dynamics of culture decline, which we interpret as representing cell mortality and lysis. The shape of the Prochlorococcus decline curve and the carrying capacity of the co-cultures were determined by the phototroph and not the heterotroph strains involved. Comparing various mathematical models of culture mortality suggests that Prochlorococcus death rate increases over time in mono-cultures but decreases in co-cultures, with cells potentially becoming more resistant to stress. Our results demonstrate intra-species differences in ecologically relevant co-culture outcomes. These include the recycling efficiency of N and whether the interactions are mutually synergistic or competitive. They also highlight the information-rich growth and death curves as a useful readout of the interaction phenotype.

Selecting 16S rRNA Primers for Microbiome Analysis in a Host-Microbe System: The Case of the Jellyfish Rhopilema nomadica.

Amplicon sequencing of the 16S rRNA gene is extensively used to characterize bacterial communities, including those living in association with eukaryotic hosts. Deciding which region of the 16S rRNA gene to analyze and selecting the appropriate PCR primers remains a major decision when initiating any new microbiome study. Based on a detailed literature survey of studies focusing on cnidarian microbiomes, we compared three commonly used primers targeting different hypervariable regions of the 16S rRNA gene, V1V2, V3V4, and V4V5, using the jellyfish Rhopilema nomadica as a model. Although all primers exhibit a similar pattern in bacterial community composition, the performance of the V3V4 primer set was superior to V1V2 and V4V5. The V1V2 primers misclassified bacteria from the Bacilli class and exhibited low classification resolution for Rickettsiales, which represent the second most abundant 16S rRNA gene sequence in all the primers. The V4V5 primer set detected almost the same community composition as the V3V4, but the ability of these primers to also amplify the eukaryotic 18S rRNA gene may hinder bacterial community observations. However, after overcoming the challenges possessed by each one of those primers, we found that all three of them show very similar bacterial community dynamics and compositions. Nevertheless, based on our results, we propose that the V3V4 primer set is potentially the most suitable for studying jellyfish-associated bacterial communities. Our results suggest that, at least for jellyfish samples, it may be feasible to directly compare microbial community estimates from different studies, each using different primers but otherwise similar experimental protocols. More generally, we recommend specifically testing different primers for each new organism or system as a prelude to large-scale 16S rRNA gene amplicon analyses, especially of previously unstudied host-microbe associations.

Characterization of membrane vesicles in Alteromonas macleodii indicates potential roles in their copiotrophic lifestyle.

Bacterial membrane vesicles (MVs) are abundant in the oceans, but their potential functional roles remain unclear. In this study we characterized MV production and protein content of six strains of Alteromonas macleodii, a cosmopolitan marine bacterium. Alteromonas macleodii strains varied in their MV production rates, with some releasing up to 30 MVs per cell per generation. Microscopy imaging revealed heterogenous MV morphologies, including some MVs aggregated within larger membrane structures. Proteomic characterization revealed that A. macleodii MVs are rich in membrane proteins related to iron and phosphate uptake, as well as proteins with potential functions in biofilm formation. Furthermore, MVs harbored ectoenzymes, such as aminopeptidases and alkaline phosphatases, which comprised up to 20% of the total extracellular enzymatic activity. Our results suggest that A. macleodii MVs may support its growth through generation of extracellular 'hotspots' that facilitate access to essential substrates. This study provides an important basis to decipher the ecological relevance of MVs in heterotrophic marine bacteria.

Metabolic Phenotyping of Marine Heterotrophs on Refactored Media Reveals Diverse Metabolic Adaptations and Lifestyle Strategies.

Microbial communities, through their metabolism, drive carbon cycling in marine environments. These complex communities are composed of many different microorganisms including heterotrophic bacteria, each with its own nutritional needs and metabolic capabilities. Yet, models of ecosystem processes typically treat heterotrophic bacteria as a "black box," which does not resolve metabolic heterogeneity nor address ecologically important processes such as the successive modification of different types of organic matter. Here we directly address the heterogeneity of metabolism by characterizing the carbon source utilization preferences of 63 heterotrophic bacteria representative of several major marine clades. By systematically growing these bacteria on 10 media containing specific subsets of carbon sources found in marine biomass, we obtained a phenotypic fingerprint that we used to explore the relationship between metabolic preferences and phylogenetic or genomic features. At the class level, these bacteria display broadly conserved patterns of preference for different carbon sources. Despite these broad taxonomic trends, growth profiles correlate poorly with phylogenetic distance or genome-wide gene content. However, metabolic preferences are strongly predicted by a handful of key enzymes that preferentially belong to a few enriched metabolic pathways, such as those involved in glyoxylate metabolism and biofilm formation. We find that enriched pathways point to enzymes directly involved in the metabolism of the corresponding carbon source and suggest potential associations between metabolic preferences and other ecologically relevant traits. The availability of systematic phenotypes across multiple synthetic media constitutes a valuable resource for future quantitative modeling efforts and systematic studies of interspecies interactions. IMPORTANCE Half of the Earth's annual primary production is carried out by phytoplankton in the surface ocean. However, this metabolic activity is heavily impacted by heterotrophic bacteria, which dominate the transformation of organic matter released from phytoplankton. Here, we characterize the diversity of metabolic preferences across many representative heterotrophs by systematically growing them on different fractions of dissolved organic carbon. Our analysis suggests that different clades of bacteria have substantially distinct preferences for specific carbon sources, in a way that cannot be simply mapped onto phylogeny. These preferences are associated with the presence of specific genes and pathways, reflecting an association between metabolic capabilities and ecological lifestyles. In addition to helping understand the importance of heterotrophs under different conditions, the phenotypic fingerprint we obtained can help build higher resolution quantitative models of global microbial activity and biogeochemical cycles in the oceans.

A comparative whole-genome approach identifies bacterial traits for marine microbial interactions.

Microbial interactions shape the structure and function of microbial communities with profound consequences for biogeochemical cycles and ecosystem health. Yet, most interaction mechanisms are studied only in model systems and their prevalence is unknown. To systematically explore the functional and interaction potential of sequenced marine bacteria, we developed a trait-based approach, and applied it to 473 complete genomes (248 genera), representing a substantial fraction of marine microbial communities. We identified genome functional clusters (GFCs) which group bacterial taxa with common ecology and life history. Most GFCs revealed unique combinations of interaction traits, including the production of siderophores (10% of genomes), phytohormones (3-8%) and different B vitamins (57-70%). Specific GFCs, comprising Alpha- and Gammaproteobacteria, displayed more interaction traits than expected by chance, and are thus predicted to preferentially interact synergistically and/or antagonistically with bacteria and phytoplankton. Linked trait clusters (LTCs) identify traits that may have evolved to act together (e.g., secretion systems, nitrogen metabolism regulation and B vitamin transporters), providing testable hypotheses for complex mechanisms of microbial interactions. Our approach translates multidimensional genomic information into an atlas of marine bacteria and their putative functions, relevant for understanding the fundamental rules that govern community assembly and dynamics.

Spatiotemporal Variation of Microbial Communities in the Ultra-Oligotrophic Eastern Mediterranean Sea.

Marine microbial communities vary seasonally and spatially, but these two factors are rarely addressed together. In this study, the temporal and spatial patterns of the bacterial and archaeal community were studied along a coast-to-offshore transect in the Eastern Mediterranean Sea (EMS) over six cruises, in three seasons of 2 consecutive years. Amplicon sequencing of 16S rRNA genes and transcripts was performed to determine presence and activity, respectively. The ultra-oligotrophic status of the Southeastern Mediterranean Sea was reflected in the microbial community composition dominated by oligotrophic bacterial groups such as SAR11, even at the most coastal station sampled, throughout the year. Seasons significantly affected the microbial communities, explaining more than half of the observed variability. However, the same few taxa dominated the community over the 2-year sampling period, varying only in their degree of dominance. While there was no overall effect of station location on the microbial community, the most coastal site (16 km offshore) differed significantly in community structure and activity from the three further offshore stations in early winter and summer. Our data on the microbial community compositions and their seasonality support previous notions that the EMS behaves like an oceanic gyre.

Single-cell measurements and modelling reveal substantial organic carbon acquisition by Prochlorococcus.

Marine phytoplankton are responsible for about half of the photosynthesis on Earth. Many are mixotrophs, combining photosynthesis with heterotrophic assimilation of organic carbon, but the relative contribution of these two lifestyles is unclear. Here single-cell measurements reveal that Prochlorococcus at the base of the photic zone in the Eastern Mediterranean Sea obtain only ~20% of carbon required for growth by photosynthesis. This is supported by laboratory-calibrated calculations based on photo-physiology parameters and compared with in situ growth rates. Agent-based simulations show that mixotrophic cells could grow tens of metres deeper than obligate photo-autotrophs, deepening the nutricline by ~20 m. Time series from the North Atlantic and North Pacific indicate that, during thermal stratification, on average 8-10% of the Prochlorococcus cells live without enough light to sustain obligate photo-autotrophic populations. Together, these results suggest that mixotrophy underpins the ecological success of a large fraction of the global Prochlorococcus population and its collective genetic diversity.