Search

Abstract Ammonia‐oxidizing archaea (AOA) play crucial roles in marine carbon and nitrogen cycles by fixing inorganic carbon and performing the initial step of nitrification. Evaluation of carbon and nitrogen metabolism popularly relies on functional genes such as amoA and accA. Increasing studies suggest that quorum sensing (QS) mainly studied in biofilms for bacteria may serve as a universal communication and regulatory mechanism among prokaryotes; however, this has yet to be demonstrated in marine planktonic archaea. To bridge this knowledge gap, we employed a combination of metabolic activity markers (amoA, accA, and grs) to elucidate the regulation of AOA‐mediated nitrogen, carbon processes, and their interactions with the surrounding heterotrophic population. Through co‐transcription investigations linking metabolic markers to potential key QS genes, we discovered that QS molecules could regulate AOA's carbon, nitrogen, and lipid metabolisms under different conditions. Interestingly, specific AOA ecotypes showed a preference for employing distinct QS systems and a distinct QS circuit involving a typical population. Overall, our data demonstrate that QS orchestrates nitrogen and carbon metabolism, including the exchange of organic metabolites between AOA and surrounding heterotrophic bacteria, which has been previously overlooked in marine AOA research.

Abstract Background Prokaryotic microbes have impacted marine biogeochemical cycles for billions of years. Viruses also impact these cycles, through lysis, horizontal gene transfer, and encoding and expressing genes that contribute to metabolic reprogramming of prokaryotic cells. While this impact is difficult to quantify in nature, we hypothesized that it can be examined by surveying virus-encoded auxiliary metabolic genes (AMGs) and assessing their ecological context. Results We systematically developed a global ocean AMG catalog by integrating previously described and newly identified AMGs and then placed this catalog into ecological and metabolic contexts relevant to ocean biogeochemistry. From 7.6 terabases of Tara Oceans paired prokaryote- and virus-enriched metagenomic sequence data, we increased known ocean virus populations to 579,904 (up 16%). From these virus populations, we then conservatively identified 86,913 AMGs that grouped into 22,779 sequence-based gene clusters, 7248 (~ 32%) of which were not previously reported. Using our catalog and modeled data from mock communities, we estimate that ~ 19% of ocean virus populations carry at least one AMG. To understand AMGs in their metabolic context, we identified 340 metabolic pathways encoded by ocean microbes and showed that AMGs map to 128 of them. Furthermore, we identified metabolic “hot spots” targeted by virus AMGs, including nine pathways where most steps (≥ 0.75) were AMG-targeted (involved in carbohydrate, amino acid, fatty acid, and nucleotide metabolism), as well as other pathways where virus-encoded AMGs outnumbered cellular homologs (involved in lipid A phosphates, phosphatidylethanolamine, creatine biosynthesis, phosphoribosylamine-glycine ligase, and carbamoyl-phosphate synthase pathways). Conclusions Together, this systematically curated, global ocean AMG catalog and analyses provide a valuable resource and foundational observations to understand the role of viruses in modulating global ocean metabolisms and their biogeochemical implications. Video Abstract

Our oceans are populated with a wide diversity of planktonic organisms that form complex dynamic communities at the base of marine trophic networks. Within such communities are phytoplankton, unicellular photosynthetic taxa that provide an estimated half of global primary production and support biogeochemical cycles, along with other essential ecosystem services. One of the major challenges for microbial ecologists has been to try to make sense of this complexity. While phytoplankton distributions can be well explained by abiotic factors such as temperature and nutrient availability, there is increasing evidence that their ecological roles are tightly linked to their metabolic interactions with other plankton members through complex mechanisms (e.g. competition and symbiosis). Therefore, unravelling phytoplankton metabolic interactions is the key for inferring their dependency on, or antagonism with, other taxa and better integrating them into the context of carbon and nutrient fluxes in marine trophic networks. In this review, we attempt to summarize the current knowledge brought by ecophysiology, organismal imaging, in silico predictions and co-occurrence networks using 'omics data, highlighting successful combinations of approaches that may be helpful for future investigations of phytoplankton metabolic interactions within their complex communities. This article is part of the theme issue 'Connected interactions: enriching food web research by spatial and social interactions'. [ABSTRACT FROM AUTHOR]

Background: Prokaryotic microbes have impacted marine biogeochemical cycles for billions of years. Viruses also impact these cycles, through lysis, horizontal gene transfer, and encoding and expressing genes that contribute to metabolic reprogramming of prokaryotic cells. While this impact is difficult to quantify in nature, we hypothesized that it can be examined by surveying virus-encoded auxiliary metabolic genes (AMGs) and assessing their ecological context. Results: We systematically developed a global ocean AMG catalog by integrating previously described and newly identified AMGs and then placed this catalog into ecological and metabolic contexts relevant to ocean biogeochemistry. From 7.6 terabases of Tara Oceans paired prokaryote- and virus-enriched metagenomic sequence data, we increased known ocean virus populations to 579,904 (up 16%). From these virus populations, we then conservatively identified 86,913 AMGs that grouped into 22,779 sequence-based gene clusters, 7248 (~ 32%) of which were not previously reported. Using our catalog and modeled data from mock communities, we estimate that ~ 19% of ocean virus populations carry at least one AMG. To understand AMGs in their metabolic context, we identified 340 metabolic pathways encoded by ocean microbes and showed that AMGs map to 128 of them. Furthermore, we identified metabolic "hot spots" targeted by virus AMGs, including nine pathways where most steps (≥ 0.75) were AMG-targeted (involved in carbohydrate, amino acid, fatty acid, and nucleotide metabolism), as well as other pathways where virus-encoded AMGs outnumbered cellular homologs (involved in lipid A phosphates, phosphatidylethanolamine, creatine biosynthesis, phosphoribosylamine-glycine ligase, and carbamoyl-phosphate synthase pathways). Conclusions: Together, this systematically curated, global ocean AMG catalog and analyses provide a valuable resource and foundational observations to understand the role of viruses in modulating global ocean metabolisms and their biogeochemical implications. 7DrB1a6JQbvrw3a2P4Hm3d Video Abstract [ABSTRACT FROM AUTHOR]

Abstract Background Plastic pollution is a severe threat to marine ecosystems. While some microbial enzymes can degrade certain plastics, the ability of the global ocean microbiome to break down diverse environmental plastics remains limited. We employed metatranscriptomic data from an international ocean survey to explore global and regional patterns in microbial plastic degradation potential. Results On a global oceanic scale, we found no significant correlation between levels of plastic pollution and the expression of genes encoding enzymes putatively identified as capable of plastic degradation. Even when looking at different regional scales, ocean depth layers, or plastic types, we found no strong or even moderate correlation between plastic pollution and relative abundances of transcripts for enzymes with presumed plastic biodegradation potential. Our data, however, indicate that microorganisms in the Southern Ocean show a higher potential for plastic degradation, making them more appealing candidates for bioprospecting novel plastic-degrading enzymes. Conclusion Our research contributes to understanding the complex global relationship between plastic pollution and microbial plastic degradation potential. We reveal that the transcription of putative plastic-degrading genes in the global ocean microbiome does not correlate to marine plastic pollution, highlighting the ongoing danger that plastic poses to marine environments threatened by plastic pollution.

Cyanobacteria can form complex interactions with heterotrophic microorganisms, but this relationship is susceptible to nutrient concentrations. Disentangling the cyanobacteria–bacteria interactions in relation to nutrient supply is essential to understanding their roles in geochemical cycles under global change. We hypothesize that enhanced nutrient supply in oligotrophic oceans can promote interactions among cyanobacteria and bacteria. Therefore, we investigated the planktonic bacteria and their interactions with cyanobacteria in relation to elevated nutrients caused by enhanced upwelling around a shallow and a deep seamount in the tropical western Pacific Ocean. We found obviously higher complexity of network occurred with significantly more cyanobacteria in the deep chlorophyll maximum layer of the shallow seamount when compared with that of the deep seamount. Cyanobacteria can shape bacterial interaction and community evenness in response to relatively high nutrient concentrations. The effects of the nutrients on cyanobacteria-related networks were further estimated based on the Tara Oceans data. Statistical analyses further showed a facilitative effect of nitrate concentrations on cyanobacteria–bacteria mutualistic interactions in the global oligotrophic ocean. By analysing the Tara Ocean macrogenomic data, we detected functional genes related to cyanobacteria–bacteria interactions in all samples, indicating the existence of a mutualistic relationship. Our results reveal cyanobacteria–bacteria interaction in response to nutrient elevation in oligotrophic ocean and highlight the potentially negative effects of global change on the bacterial community from the view of the bio-interaction. [ABSTRACT FROM AUTHOR]

Background: Plastic pollution is a severe threat to marine ecosystems. While some microbial enzymes can degrade certain plastics, the ability of the global ocean microbiome to break down diverse environmental plastics remains limited. We employed metatranscriptomic data from an international ocean survey to explore global and regional patterns in microbial plastic degradation potential. Results: On a global oceanic scale, we found no significant correlation between levels of plastic pollution and the expression of genes encoding enzymes putatively identified as capable of plastic degradation. Even when looking at different regional scales, ocean depth layers, or plastic types, we found no strong or even moderate correlation between plastic pollution and relative abundances of transcripts for enzymes with presumed plastic biodegradation potential. Our data, however, indicate that microorganisms in the Southern Ocean show a higher potential for plastic degradation, making them more appealing candidates for bioprospecting novel plastic-degrading enzymes. Conclusion: Our research contributes to understanding the complex global relationship between plastic pollution and microbial plastic degradation potential. We reveal that the transcription of putative plastic-degrading genes in the global ocean microbiome does not correlate to marine plastic pollution, highlighting the ongoing danger that plastic poses to marine environments threatened by plastic pollution. [ABSTRACT FROM AUTHOR]

Unicellular eukaryotes that are capable of phago-mixotrophy in the ocean compete for inorganic nutrients and light with autotrophs, and for bacterial prey with heterotrophs. In this study, we ask what the overall prevalence of eukaryotic mixotrophs in the vast open ocean is, and how the availability of inorganic nutrients, light, and prey affects their relative success. We utilized the Tara Oceans eukaryotic 18S rRNA gene and environmental context variables dataset to conduct a large-scale field analysis. We also performed isolate-based culture experiments to verify growth and nutritional resource relationships for representative mixotrophic taxa. The field analysis suggested that the overall prevalence of mixotrophs were negatively correlated with nutrient concentrations and positively associated with light availability. Concentrations of heterotrophic bacteria as a single variable also presented a positive correlation with mixotrophic prevalence, but to a lesser extent. On the other hand, the culture experiments demonstrated a taxa-specific relationship between mixotrophic growth and nutrition resources, i.e., the growth of one group was significantly dependent on light availability, while the other group was less affected by light when they received sufficient prey. Both groups were capable of growing efficiently with low inorganic nutrients when receiving sufficient prey and light. Therefore, our field analysis and culture experiments both suggest that phago-mixotrophy for ocean eukaryotes is seemingly an efficient strategy to compensate for nutrient deficiency but unnecessary to compensate for light scarcity. This study collectively revealed a close relationship between abiotic and biotic nutritional resources and the prevalence of trophic strategies, shedding light on the importance of light and nutrients for determining the competitive success of mixotrophs versus autotrophic and heterotrophic eukaryotes in the ocean. [ABSTRACT FROM AUTHOR]

Extant species of the dinoflagellate genus Gonyaulax are capable of producing resting cysts morphologically similar to different cyst-based genera, and their cyst-theca relationships are far from resolved. Here we have carried out germination experiments on several living cysts that resemble Spiniferites delicatus from the subtropical regions of China and Mexico. Both cyst and theca morphology were examined by light and scanning electron microscopy. A new species, Gonyaulax pospelovana, is described, characterized by a cingulum displacement and an overhang of twice its width, and two short antapical spines. The cysts of G. pospelovana had a granular surface and gonal processes with petaloid tips. Maximum likelihood and Bayesian inference analyses based on LSU and SSU rRNA gene sequences revealed that strains identified as G. pospelovana were monophyletic, forming a sister clade to Gonyaulax ellegaardiae and several presumable strains of Gonyaulax spinifera. One Chinese strain and two Mexican strains of G. pospelovana were examined for yessotoxin production using LC-MS/MS, but were not found to produce a detectable amount of toxins. Metabarcoding targeting the 18S V4 rRNA gene was performed on monthly collected samples in Xiamen Bay, China. A ZOTU (zero-radius operational taxonomic units) was detected that was consistent with G. pospelovana. Its maximum abundance was recorded in summer. Additionally, an OTU was identified as G. pospelovana from the Tara Oceans metabarcoding data, which occurred in the Indian and Pacific oceans at temperatures ranging from 28°C to 31°C, suggesting that it is a warm water species. [ABSTRACT FROM AUTHOR]

Ocean microbial communities strongly influence the biogeochemistry, food webs, and climate of our planet. Despite recent advances in understanding their taxonomic and genomic compositions, little is known about how their transcriptomes vary globally. Here, we present a dataset of 187 metatranscriptomes and 370 metagenomes from 126 globally distributed sampling stations and establish a resource of 47 million genes to study community-level transcriptomes across depth layers from pole-to-pole. We examine gene expression changes and community turnover as the underlying mechanisms shaping community transcriptomes along these axes of environmental variation and show how their individual contributions differ for multiple biogeochemically relevant processes. Furthermore, we find the relative contribution of gene expression changes to be significantly lower in polar than in non-polar waters and hypothesize that in polar regions, alterations in community activity in response to ocean warming will be driven more strongly by changes in organismal composition than by gene regulatory mechanisms. VIDEO ABSTRACT.

ABSTRACT The rapid growth of diatoms makes them one of the most pervasive and productive types of plankton in the world’s ocean, but the physiological basis for their high growth rates remains poorly understood. Here, we evaluate the factors that elevate diatom growth rates, relative to other plankton, using a steady-state metabolic flux model that computes the photosynthetic C source from intracellular light attenuation and the carbon cost of growth from empirical cell C quotas, across a wide range of cell sizes. For both diatoms and other phytoplankton, growth rates decline with increased cell volume, consistent with observations, because the C cost of division increases with size faster than photosynthesis. However, the model predicts overall higher growth rates for diatoms due to reduced C requirements and the low energetic cost of Si deposition. The C savings from the silica frustule are supported by metatranscriptomic data from Tara Oceans, which show that the abundance of transcripts for cytoskeleton components in diatoms is lower than in other phytoplankton. Our results highlight the importance of understanding the origins of phylogenetic differences in cellular C quotas, and suggest that the evolution of silica frustules may play a critical role in the global dominance of marine diatoms. IMPORTANCE This study addresses a longstanding issue regarding diatoms, namely, their fast growth. Diatoms, which broadly are phytoplankton with silica frustules, are the world’s most productive microorganisms and dominate in polar and upwelling regions. Their dominance is largely supported by their high growth rate, but the physiological reasoning behind that characteristic has been obscure. In this study, we combine a quantitative model and metatranscriptomic approaches and show that diatoms' low carbon requirements and low energy costs for silica frustule production are the key factors supporting their fast growth. Our study suggests that the effective use of energy-efficient silica as a cellular structure, instead of carbon, enables diatoms to be the most productive organisms in the global ocean.

Phytoplankton account for >45% of global primary production, and have an enormous impact on aquatic food webs and on the entire Earth System. Their members are found among prokaryotes (cyanobacteria) and multiple eukaryotic lineages containing chloroplasts. Genetic surveys of phytoplankton communities generally consist of PCR amplification of bacterial (16S), nuclear (18S) and/or chloroplastic (16S) rRNA marker genes from DNA extracted from environmental samples. However, our appreciation of phytoplankton abundance or biomass is limited by PCR‐amplification biases, rRNA gene copy number variations across taxa, and the fact that rRNA genes do not provide insights into metabolic traits such as photosynthesis. Here, we targeted the photosynthetic gene psbO from metagenomes to circumvent these limitations: the method is PCR‐free, and the gene is universally and exclusively present in photosynthetic prokaryotes and eukaryotes, mainly in one copy per genome. We applied and validated this new strategy with the size‐fractionated marine samples collected by Tara Oceans, and showed improved correlations with flow cytometry and microscopy than when based on rRNA genes. Furthermore, we revealed unexpected features of the ecology of these ecosystems, such as the high abundance of picocyanobacterial aggregates and symbionts in the ocean, and the decrease in relative abundance of phototrophs towards the larger size classes of marine dinoflagellates. To facilitate the incorporation of psbO in molecular‐based surveys, we compiled a curated database of >18,000 unique sequences. Overall, psbO appears to be a promising new gene marker for molecular‐based evaluations of entire phytoplankton communities. see also the Perspective by Georgina L. Brennan [ABSTRACT FROM AUTHOR]

Marine planktonic diatom species can exhibit contrasting distribution patterns, from endemic to cosmopolitan. Endemicity is counter-intuitive for planktonic species given their potentially large population sizes and ample migration opportunities by means of ocean currents. Here, we analyse the biogeography of six species of the diatom genus Bacteriastrum with apparently contrasting distribution patterns. Occurrence data obtained from metabarcode reads in samples from Ocean Sampling Day (OSD) sites and from Tara Oceans stations as well as from their observational records included in biodiversity data repositories of GBIF and OBIS were plotted in occurrence maps. According to metabarcoding data, the six species examined here occur all over the temperate and tropical parts of the oceans. Observational records corroborate this finding for B. elegans, B. furcatum, B. hyalinum and B. mediterraneum. Instead, atypical colony former B. jadranum is encountered at just a few distant sites, and solitary B. parallelum only in the Gulf of Naples. The metabarcoding data reveal that the latter two species are far more widely distributed than their actual sightings according to GBIF and OBIS, and that B. hyalinum also occurs in the Arctic. The most likely reasons for the discrepancies among the different data sources are the relatively recent description of B. jadranum and B. parallelum, their diminutive and inconspicuous habitus, and their possible misidentification in routine plankton counting. HIGHLIGHTS • Metabarcoding data of Tara Oceans and OSD discern Bacteriastrum species.• Pan-oceanic distribution of Bacteriastrum species according to global metabarcoding data.• Distribution patterns of phytoplankton species can be inferred from global metabarcode datasets. [ABSTRACT FROM AUTHOR]

Filamentous and colony-forming cells within the cyanobacterial genus Trichodesmium might account for nearly half of nitrogen fixation in the sunlit ocean, a critical mechanism that sustains plankton's primary productivity. Trichodesmium has long been portrayed as a diazotrophic genus. By means of genome-resolved metagenomics, here we reveal that nondiazotrophic Trichodesmium species not only exist but also are abundant and widespread in the open ocean, benefiting from a previously overlooked functional lifestyle to expand the biogeography of this prominent marine genus. Near-complete environmental genomes for those closely related candidate species reproducibly shared functional features including a lack of genes related to nitrogen fixation, hydrogen recycling, and hopanoid lipid production concomitant with the enrichment of nitrogen assimilation genes. Our results elucidate fieldwork observations of Trichodesmium cells fixing carbon but not nitrogen. The Black Queen hypothesis and burden of low-oxygen concentration requirements provide a rationale to explain gene loss linked to nitrogen fixation among Trichodesmium species. Disconnecting taxonomic signal for this genus from a microbial community's ability to fix nitrogen will help refine our understanding of the marine nitrogen balance. Finally, we are reminded that established links between taxonomic lineages and functional traits do not always hold true. [ABSTRACT FROM AUTHOR]

Marine diatoms, the most successful photoautotrophs in the ocean, efficiently sequester a significant part of atmospheric CO2 to the ocean interior through their participation in the biological carbon pump. However, it is poorly understood how marine diatoms fix such a considerable amount of CO2, which is vital information toward modeling their response to future CO2 levels. The Tara Oceans expeditions generated molecular data coupled with in situ biogeochemical measurements across the main ocean regions, and thus provides a framework to compare diatom genetic and transcriptional flexibility under natural CO2 variability. The current study investigates the interlink between the environmental variability of CO2 and other physicochemical parameters with the gene and transcript copy numbers of five key enzymes of diatom CO2 concentration mechanisms (CCMs): Rubisco activase and carbonic anhydrase (CA) as part of the physical pathway, together with phosphoenolpyruvate carboxylase, phosphoenolpyruvate carboxykinase, and malic enzyme as part of the potential C4 biochemical pathway. Toward this aim, we mined >200 metagenomes and >220 metatranscriptomes generated from samples of the surface layer of 66 globally distributed sampling sites and corresponding to the four main size fractions in which diatoms can be found: 0.8–5 μm, 5–20 μm, 20–180 μm, and 180–2,000 μm. Our analyses revealed that the transcripts for the enzymes of the putative C4 biochemical CCM did not in general display co-occurring profiles. The transcripts for CAs were the most abundant, with an order of magnitude higher values than the other enzymes, thus implying the importance of physical CCMs in diatom natural communities. Among the different classes of this enzyme, the most prevalent was the recently characterized iota class. Consequently, very little information is available from natural diatom assemblages about the distribution of this class. Biogeographic distributions for all the enzymes show different abundance hotspots according to the size fraction, pointing to the influence of cell size and aggregation in CCMs. Environmental correlations showed a complex pattern of responses to CO2 levels, total phytoplankton biomass, temperature, and nutrient concentrations. In conclusion, we propose that biophysical CCMs are prevalent in natural diatom communities.

Marine diatoms, the most successful photoautotrophs in the ocean, efficiently sequester a significant part of atmospheric CO2 to the ocean interior through their participation in the biological carbon pump. However, it is poorly understood how marine diatoms fix such a considerable amount of CO2, which is vital information toward modeling their response to future CO2 levels. The Tara Oceans expeditions generated molecular data coupled with in situ biogeochemical measurements across the main ocean regions, and thus provides a framework to compare diatom genetic and transcriptional flexibility under natural CO2 variability. The current study investigates the interlink between the environmental variability of CO2 and other physicochemical parameters with the gene and transcript copy numbers of five key enzymes of diatom CO2 concentration mechanisms (CCMs): Rubisco activase and carbonic anhydrase (CA) as part of the physical pathway, together with phosphoenolpyruvate carboxylase, phosphoenolpyruvate carboxykinase, and malic enzyme as part of the potential C4 biochemical pathway. Toward this aim, we mined >200 metagenomes and >220 metatranscriptomes generated from samples of the surface layer of 66 globally distributed sampling sites and corresponding to the four main size fractions in which diatoms can be found: 0.8–5 μm, 5–20 μm, 20–180 μm, and 180–2,000 μm. Our analyses revealed that the transcripts for the enzymes of the putative C4 biochemical CCM did not in general display co-occurring profiles. The transcripts for CAs were the most abundant, with an order of magnitude higher values than the other enzymes, thus implying the importance of physical CCMs in diatom natural communities. Among the different classes of this enzyme, the most prevalent was the recently characterized iota class. Consequently, very little information is available from natural diatom assemblages about the distribution of this class. Biogeographic distributions for all the enzymes show different abundance hotspots according to the size fraction, pointing to the influence of cell size and aggregation in CCMs. Environmental correlations showed a complex pattern of responses to CO2 levels, total phytoplankton biomass, temperature, and nutrient concentrations. In conclusion, we propose that biophysical CCMs are prevalent in natural diatom communities. [ABSTRACT FROM AUTHOR]

Aim: Plankton diversity is a pivotal element of marine ecosystem stability and functioning. A major obstacle in the assessment of diversity is the lack of consistency between patterns assessed by molecular and morphological data. This work aims to reconcile the two in a single richness measure, to investigate the environmental drivers affecting this measure, and finally to predict its spatio‐temporal patterns. Location and time period: This is a global scale study, based on data collected within the 2009–2013 interval during the Tara Oceans expedition. Major taxa studied: The focus of this study is diatoms. They play an important role in several biogeochemical cycles and within marine food webs, and display high taxonomic and functional richness. Methods: We integrate measures of diatom richness across the global ocean using molecular and morphological approaches, giving particular attention to 'the rare biosphere'. We then perform a machine‐learning‐based analysis of these reconciled patterns to extrapolate diatom richness at the global scale and to identify the main environmental processes governing it. Finally, we model the response of diatom richness to climate change. Results: By filtering out 0.3% of the rarest operational taxonomic units, molecular‐based richness patterns show the best possible match with the morphological approach. Temperature, phosphate, chlorophyll a and the Lyapunov exponent are the major explainers of these reconciled patterns. Global scale predictions provide a first approximation of the global geography of diatom richness and of the possible impacts of climate change. Main conclusions: Our models suggest that diatom richness is controlled by different processes characteristic of distinct environmental scenarios: lateral mixing in highly dynamic regions, and both nutrient availability and temperature elsewhere. We present herein the effects of these processes on richness and how these same effects differ from other diversity indices because of the main component of richness: the rare biosphere. [ABSTRACT FROM AUTHOR]

Acclimation allowed by variation in gene or allele expression in natural populations is increasingly understood as a decisive mechanism, as much as adaptation, for species evolution. However, for small eukaryotic organisms, as species from zooplankton, classical methods face numerous challenges. Here, we propose the concept of allelic differential expression at the population-scale (psADE) to investigate the variation in allele expression in natural populations. We developed a novel approach to detect psADE based on metagenomic and metatranscriptomic data from environmental samples. This approach was applied on the widespread marine copepod, Oithona similis, by combining samples collected during the Tara Oceans expedition (2009-2013) and de novo transcriptome assemblies. Among a total of 25,768 single nucleotide variants (SNVs) of O. similis, 572 (2.2%) were affected by psADE in at least one population (FDR < 0.05). The distribution of SNVs under psADE in different populations is significantly shaped by population genomic differentiation (Pearson r = 0.87, p = 5.6 x 10-30), supporting a partial genetic control of psADE. Moreover, a significant amount of SNVs (0.6%) were under both selection and psADE (p < .05), supporting the hypothesis that natural selection and psADE tends to impact common loci. Population-scale allelic differential expression offers new insights into the gene regulation control in populations and its link with natural selection. [ABSTRACT FROM AUTHOR]

Selenium (Se) is an essential trace element for many organisms, which is required in the biosynthesis of proteins with selenocysteine, tRNAs with selenouridine, and certain enzymes with Se as a cofactor. Recent large-scale metagenomics projects provide a unique opportunity for studying the global trends of Se utilization in marine environments. Here, we analyzed samples from different marine microbial communities, revealed by the Tara Oceans project, to characterize the Se utilization traits. We found that the selenophosphate synthetase gene, which defines the overall Se utilization, and Se utilization traits are present in all samples. Regions with samples rich and poor in Se utilization traits were categorized. From the analysis of environmental factors, the mesopelagic zone and high temperature (> 15°C) of water are favorable, while geographical location has little influence on Se utilization. All Se utilization traits showed a relatively independent occurrence. The taxonomic classification of Se traits shows that most of the sequences corresponding to Se utilization traits belong to the phylum Proteobacteria. Overall, our study provides useful insights into the general features of Se utilization in ocean samples and may help to understand the evolutionary dynamics of Se utilization in different marine environments. [ABSTRACT FROM AUTHOR]

In this study, we used miTAG approach to analyze the distributional pattern and fine‐scale genetic diversity of the ammonia oxidizing archaea (AOA) lineages in the global oceans with the metagenomics data sets of the Tara Oceans global expedition (2009–2013). Using the ammonium monooxygenase alpha subunit gene as a biomarker, the AOA communities in the global oceans were recovered with highly diverse operational taxonomic units that affiliated to previously defined clades, including water column A (WCA), water column B (WCB), and SCM1‐like clades. In general, the AOA communities were obviously segregated with depth (except the upwelling regions), and the communities in the euphotic zones were more heterogeneous than in the mesopelagic zones (MPZs). The WCA distributed more evenly and widely in the euphotic zone and MPZs, while WCB and SCM1‐like clade mainly distributed in MPZ and high‐latitude waters, respectively. At fine‐scale genetic diversity, SCM1‐like and 2 WCA subclades showed distinctive niche separations of distributional pattern. We further divided the AOA subclades into ecological significant taxonomic units (ESTUs), which were delineated from the distribution pattern of their corresponding subclades. For example, ESTUs of WCA have different correlations with depth, nitrate to silicate ratio, and salinity; SCM1‐like A was negatively correlated with irradiation, whereas other SCM1‐like ESTUs preferred low‐temperature and high‐nutrient conditions. Our result showed that the previously defined AOA clades and ecotypes consist of highly diverse sublineages, whose diversity might be overlooked in the past. The distribution patterns of different ESTUs imply their ecophysiological characteristics and potential roles in biogeochemical cycling. Plain Language Summary: In the ocean, ammonia oxidizing archaea (AOA) are widely distributed microbes that play important roles in the marine nitrogen cycling and the emission of the highly potent greenhouse gas (N2O). However, the majority of the marine AOA are currently uncultivated; the physiology of marine AOA and the factors that mediate their distribution still remain unclear. In this study, we have analyzed the fine‐scale phylogenetic diversity and community structures of the AOA in the global ocean. Based on the results, the genetic diversity of marine AOA might be overlooked in the past since highly diverse groups that showed differential distribution patterns in the previously defined AOA ecotypes are found. Besides, by analyzing the correlations of their distributions with the varied environmental conditions in the global oceans, the diverse AOA groups were delineated with particular physiochemical factors. At a finer resolution than the previously defined ecotypes, our findings provide new insights into the determinants and the ecophysiology of the widely distributed but uncultivated AOA groups. Key Points: Vertical segregation of AOA community was highly predictable throughout the global ocean, while physical forcing disrupted the patternThe ecotypes WCA and WCB consist of diverse subgroups that showed differential distribution patterns and correlations with environmental factorsThe specific correlations between genetic diversity and environmental factors provided new insights into the determinants of AOA in the ocean [ABSTRACT FROM AUTHOR]

Marine Synechococcus cyanobacteria are major contributors to global oceanic primary production and exhibit a unique diversity of photosynthetic pigments, allowing them to exploit a wide range of light niches. However, the relationship between pigment content and niche partitioning has remained largely undetermined due to the lack of a single-genetic marker resolving all pigment types (PTs). Here, we developed and employed a robust method based on three distinct marker genes (cpcBA, mpeBA, and mpeW) to estimate the relative abundance of all known Synechococcus PTs from metagenomes. Analysis of the Tara Oceans dataset allowed us to reveal the global distribution of Synechococcus PTs and to define their environmental niches. Green-light specialists (PT 3a) dominated in warm, green equatorial waters, whereas blue-light specialists (PT 3c) were particularly abundant in oligotrophic areas. Type IV chromatic acclimaters (CA4-A/B), which are able to dynamically modify their light absorption properties to maximally absorb green or blue light, were unexpectedly the most abundant PT in our dataset and predominated at depth and high latitudes. We also identified populations in which CA4 might be nonfunctional due to the lack of specific CA4 genes, notably inwarm high-nutrient low-chlorophyll areas. Major ecotypes within clades I-IV and CRD1 were preferentially associated with a particular PT, while others exhibited a wide range of PTs. Altogether, this study provides important insights into the ecology of Synechococcus and highlights the complex interactions between vertical phylogeny, pigmentation, and environmental parameters that shape Synechococcus community structure and evolution. [ABSTRACT FROM AUTHOR]

Oceanic phytoplankton serve as a base for the food webs within the largest planetary ecosystem. Despite this, surprisingly little is known about species composition, function and ecology of phytoplankton communities, especially for vast areas of the open ocean. In this study we focus on the marine phytoplankton microflora from the vicinity of the Marquesas Islands in the Southern Pacific Ocean collected during the Tara Oceans expedition. Multiple samples from four sites and two depths were studied in detail using light microscopy, scanning electron microscopy, and automated confocal laser scanning microscopy. In total 289 taxa were identified, with Dinophyceae and Bacillariophyceae contributing 60% and 32% of taxa, respectively, to phytoplankton community composition. Notwithstanding, a large number of cells could not be assigned to any known species. Coccolithophores and other flagellates together contributed less than 8% to the species list. Observed cell densities were generally low, but at sites of high autotrophic biomass, diatoms reached the highest cell densities (1.26 × 104 cells L−1). Overall, 18S rRNA metabarcode-based community compositions matched microscopy-based estimates, particularly for the main diatom taxa, indicating consistency and complementarity between different methods, while the wide range of microscopy-based methods permitted several unknown and poorly studied taxa to be revealed and identified. [ABSTRACT FROM AUTHOR]

The Tara Oceans Expedition has provided large, publicly-accessible microbial metagenomic datasets from a circumnavigation of the globe. Utilizing several size fractions from the samples originating in the Mediterranean Sea, we have used current assembly and binning techniques to reconstruct 290 putative draft metagenome-assembled bacterial and archaeal genomes, with an estimated completion of ≥50%, and an additional 2,786 bins, with estimated completion of 0–50%. We have submitted our results, including initial taxonomic and phylogenetic assignments, for the putative draft genomes to open-access repositories for the scientific community to use in ongoing research.

Pangenomes offer detailed characterizations of core and accessory genes found in a set of closely related microbial genomes, generally by clustering genes based on sequence homology. In comparison, metagenomes facilitate highly resolved investigations of the relative distribution of microbial genomes and individual genes across environments through read recruitment analyses. Combining these complementary approaches can yield unique insights into the functional basis of microbial niche partitioning and fitness, however, advanced software solutions are lacking. Here we present an integrated analysis and visualization strategy that provides an interactive and reproducible framework to generate pangenomes and to study them in conjunction with metagenomes. To investigate its utility, we applied this strategy to a Prochlorococcus pangenome in the context of a large-scale marine metagenomic survey. The resulting Prochlorococcus metapangenome revealed remarkable differential abundance patterns between very closely related isolates that belonged to the same phylogenetic cluster and that differed by only a small number of gene clusters in the pangenome. While the relationships between these genomes based on gene clusters correlated with their environmental distribution patterns, phylogenetic analyses using marker genes or concatenated single-copy core genes did not recapitulate these patterns. The metapangenome also revealed a small set of core genes that mostly occurred in hypervariable genomic islands of the Prochlorococcus populations, which systematically lacked read recruitment from surface ocean metagenomes. Notably, these core gene clusters were all linked to sugar metabolism, suggesting potential benefits to Prochlorococcus from a high sequence diversity of sugar metabolism genes. The rapidly growing number of microbial genomes and increasing availability of environmental metagenomes provide new opportunities to investigate the functioning and the ecology of microbial populations, and metapangenomes can provide unique insights for any taxon and biome for which genomic and sufficiently deep metagenomic data are available. [ABSTRACT FROM AUTHOR]

Summary The world’s oceans represent by far the largest biome, with great importance for the global ecosystem [ 1–4 ]. The vast majority of ocean biomass and biodiversity is composed of microscopic plankton. Recent results from the Tara Oceans metabarcoding study revealed that a significant part of the plankton in the upper sunlit layer of the ocean is represented by an understudied group of heterotrophic excavate flagellates called diplonemids [ 5, 6 ]. We have analyzed the diversity and distribution patterns of diplonemid populations on the extended set of Tara Oceans V9 18S rDNA metabarcodes amplified from 850 size- fractionated plankton communities sampled across 123 globally distributed locations, for the first time also including samples from the mesopelagic zone, which spans the depth from about 200 to 1,000 meters. Diplonemids separate into four major clades, with the vast majority falling into the deep-sea pelagic diplonemid clade. Remarkably, diversity of this clade inferred from metabarcoding data surpasses even that of dinoflagellates, metazoans, and rhizarians, qualifying diplonemids as possibly the most diverse group of marine planktonic eukaryotes. Diplonemids display strong vertical separation between the photic and mesopelagic layers, with the majority of their relative abundance and diversity occurring in deeper waters. Globally, diplonemids display no apparent biogeographic structuring, with a few hyperabundant cosmopolitan operational taxonomic units (OTUs) dominating their communities. Our results suggest that the planktonic diplonemids are among the key heterotrophic players in the largest ecosystem of our biosphere, yet their roles in this ecosystem remain unknown. [ABSTRACT FROM AUTHOR]

Prochlorococcus and Synechococcus are the two most abundant and widespread phytoplankton in the global ocean. To better understand the factors controlling their biogeography, a reference database of the high-resolution taxonomic marker petB, encoding cytochrome b6, was used to recruit reads out of 109 metagenomes from the Tara Oceans expedition. An unsuspected novel genetic diversity was unveiled within both genera, even for the most abundant and well-characterized clades, and 136 divergent petB sequences were successfully assembled from metagenomic reads, significantly enriching the reference database. We then defined Ecologically Significant Taxonomic Units (ESTUs)--that is, organisms belonging to the same clade and occupying a common oceanic niche. Three major ESTU assemblages were identified along the cruise transect for Prochlorococcus and eight for Synechococcus. Although Prochlorococcus HLIIIA and HLIVA ESTUs codominated in iron-depleted areas of the Pacific Ocean, CRD1 and the yet-to-be cultured EnvB were the prevalent Synechococcus clades in this area, with three different CRD1 and EnvB ESTUs occupying distinct ecological niches with regard to iron availability and temperature. Sharp community shifts were also observed over short geographic distances--for example, around the Marquesas Islands or between southern Indian and Atlantic Oceans--pointing to a tight correlation between ESTU assemblages and specific physico-chemical parameters. Together, this study demonstrates that there is a previously overlooked, ecologically meaningful, fine-scale diversity within some currently defined picocyanobacterial ecotypes, bringing novel insights into the ecology, diversity, and biology of the two most abundant phototrophs on Earth. [ABSTRACT FROM AUTHOR]

Diatoms (Bacillariophyta) constitute one of the most diverse and ecologically important groups of phytoplankton. They are considered to be particularly important in nutrient-rich coastal ecosystems and at high latitudes, but considerably less so in the oligotrophic open ocean. The Tara Oceans circumnavigation collected samples from a wide range of oceanic regions using a standardized sampling procedure. Here, a total of ~12 million diatom V9-18S ribosomal DNA (rDNA) ribotypes, derived from 293 size-fractionated plankton communities collected at 46 sampling sites across the global ocean euphotic zone, have been analyzed to explore diatom global diversity and community composition. We provide a new estimate of diversity of marine planktonic diatoms at 4,748 operational taxonomic units (OTUs). Based on the total assigned ribotypes, Chaetoceros was the most abundant and diverse genus, followed by Fragilariopsis, Thalassiosira, and Corethron. We found only a few cosmopolitan ribotypes displaying an even distribution across stations and high abundance, many of which could not be assigned with confidence to any known genus. Three distinct communities from South Pacific, Mediterranean, and Southern Ocean waters were identified that share a substantial percentage of ribotypes within them. Sudden drops in diversity were observed at Cape Agulhas, which separates the Indian and Atlantic Oceans, and across the Drake Passage between the Atlantic and Southern Oceans, indicating the importance of these ocean circulation choke points in constraining diatom distribution and diversity. We also observed high diatom diversity in the open ocean, suggesting that diatoms may be more relevant in these oceanic systems than generally considered. [ABSTRACT FROM AUTHOR]

Marine planktonic eukaryotes play critical roles in global biogeochemical cycles and climate. However, their poor representation in culture collections limits our understanding of the evolutionary history and genomic underpinnings of planktonic ecosystems. Here, we used 280 billion Tara Oceans metagenomic reads from polar, temperate, and tropical sunlit oceans to reconstruct and manually curate more than 700 abundant and widespread eukaryotic environmental genomes ranging from 10 Mbp to 1.3 Gbp. This genomic resource covers a wide range of poorly characterized eukaryotic lineages that complement long-standing contributions from culture collections while better representing plankton in the upper layer of the oceans. We performed the first, to our knowledge, comprehensive genome-wide functional classification of abundant unicellular eukaryotic plankton, revealing four major groups connecting distantly related lineages. Neither trophic modes of plankton nor its vertical evolutionary history could completely explain the functional repertoire convergence of major eukaryotic lineages that coexisted within oceanic currents for millions of years., Competing Interests: The authors declare no competing interests., (© 2022 The Author(s).)