Microbes mediating the sulfur cycle in the Atlantic Ocean and their link to chemolithoautotrophy.

Only about 10%-30% of the organic matter produced in the epipelagic layers reaches the dark ocean. Under these limiting conditions, reduced inorganic substrates might be used as an energy source to fuel prokaryotic chemoautotrophic and/or mixotrophic activity. The aprA gene encodes the alpha subunit of the adenosine-5'-phosphosulfate (APS) reductase, present in sulfate-reducing (SRP) and sulfur-oxidizing prokaryotes (SOP). The sulfur-oxidizing pathway can be coupled to inorganic carbon fixation via the Calvin-Benson-Bassham cycle. The abundances of aprA and cbbM, encoding RuBisCO form II (the key CO2 fixing enzyme), were determined over the entire water column along a latitudinal transect in the Atlantic from 64°N to 50°S covering six oceanic provinces. The abundance of aprA and cbbM genes significantly increased with depth reaching the highest abundances in meso- and upper bathypelagic layers. The contribution of cells containing these genes also increased from mesotrophic towards oligotrophic provinces, suggesting that under nutrient limiting conditions alternative energy sources are advantageous. However, the aprA/cbbM ratios indicated that only a fraction of the SOP is associated with inorganic carbon fixation. The aprA harbouring prokaryotic community was dominated by Pelagibacterales in surface and mesopelagic waters, while Candidatus Thioglobus, Chromatiales and the Deltaproteobacterium_SCGC dominated the bathypelagic realm. Noticeably, the contribution of the SRP to the prokaryotic community harbouring aprA gene was low, suggesting a major utilization of inorganic sulfur compounds either as an energy source (occasionally coupled with inorganic carbon fixation) or in biosynthesis pathways.

Mesozooplankton taurine production and prokaryotic uptake in the northern Adriatic Sea.

Dissolved free taurine, an important osmolyte in phytoplankton and metazoans, has been shown to be a significant carbon and energy source for prokaryotes in the North Atlantic throughout the water column. However, the extent of the coupling between taurine production and consumption over a seasonal cycle has not been examined yet. We determined taurine production by abundant crustacean zooplankton and its role as a carbon and energy source for several prokaryotic taxa in the northern Adriatic Sea over a seasonal cycle. Taurine concentrations were generally in the low nanomolar range, reaching a maximum of 22 nmol L-1 in fall during a Pseudonitzschia bloom and coinciding with the highest zooplankton taurine release rates. Taurine accounted for up to 5% of the carbon, 11% of the nitrogen, and up to 71% of the sulfur requirements of heterotrophic prokaryotes. Members of the Roseobacter clade, Alteromonas, Thaumarchaeota, and Euryarchaeota exhibited higher cell-specific taurine assimilation rates than SAR11 cells. However, cell-specific taurine and leucine assimilation were highly variable in all taxa, suggesting species and/or ecotype specific utilization patterns of taurine and dissolved free amino acids. Copepods were able to cover the bulk taurine requirements of the prokaryotic communities in fall and winter and partly in the spring-summer period. Overall, our study emphasizes the significance of taurine as a carbon and energy source for the prokaryotic community in the northern Adriatic Sea and the importance of crustacean zooplankton as a significant source of taurine and other organic compounds for the heterotrophic prokaryotic community.

Highly variable mRNA half-life time within marine bacterial taxa and functional genes.

Messenger RNA can provide valuable insights into the variability of metabolic processes of microorganisms. However, due to uncertainties that include the stability of RNA, its application for activity profiling of environmental samples is questionable. We explored different factors affecting the decay rate of transcripts of three marine bacterial isolates using qPCR and determined mRNA half-life time of specific bacterial taxa and of functional genes by metatranscriptomics of a coastal environmental prokaryotic community. The half-life time of transcripts from 11 genes from bacterial isolates ranged from 1 to 46 min. About 80% of the analysed transcripts exhibited half-live times shorter than 10 min. Significant differences were found in the half-life time between mRNA and rRNA. The half-life time of mRNA obtained from a coastal metatranscriptome ranged from 9 to 400 min. The shortest half-life times of the metatranscriptome corresponded to transcripts from the same clusters of orthologous groups (COGs) in all bacterial classes. The prevalence of short mRNA half-life time in genes related to defence mechanisms and motility indicate a tight connection of RNA decay rate to environmental stressors. The short half-life time of RNA and its high variability needs to be considered when assessing metatranscriptomes especially in environmental samples.

Differential Response of Cafeteria roenbergensis to Different Bacterial and Archaeal Prey Characteristics.

In the marine environment, the abundance of Bacteria and Archaea is either controlled bottom-up via nutrient availability or top-down via grazing. Heterotrophic nanoflagellates (HNF) are mainly responsible for prokaryotic grazing losses besides viral lysis. However, the grazing specificity of HNF on specific bacterial and archaeal taxa is under debate. Bacteria and Archaea might have different nutritive values and surface properties affecting the growth rates of HNF. In this study, we offered different bacterial and archaeal strains with different morphologic and physiologic characteristics to Cafeteria roenbergensis, one of the most abundant and ubiquitous species of HNF in the ocean. Two Nitrosopumilus maritimus-related strains isolated from the northern Adriatic Sea (Nitrosopumilus adriaticus, Nitrosopumilus piranensis), two Nitrosococcus strains, and two fast growing marine Bacteria (Pseudoalteromonas sp. and Marinobacter sp.) were fed to Cafeteria cultures. Cafeteria roenbergensis exhibited high growth rates when feeding on Pseudoalteromonas sp., Marinobacter sp., and Nitrosopumilus adriaticus, while the addition of the other strains resulted in minimal growth. Taken together, our data suggest that the differences in growth of Cafeteria roenbergensis associated to grazing on different thaumarchaeal and bacterial strains are likely due to the subtle metabolic, cell size, and physiological differences between different bacterial and thaumarchaeal taxa. Moreover, Nitrosopumilus adriaticus experienced a similar grazing pressure by Cafeteria roenbergensis as compared to the other strains, suggesting that other HNF may also prey on Archaea which might have important consequences on the global biogeochemical cycles.

Taurine Is a Major Carbon and Energy Source for Marine Prokaryotes in the North Atlantic Ocean off the Iberian Peninsula.

Taurine, an amino acid-like compound, acts as an osmostress protectant in many marine metazoans and algae and is released via various processes into the oceanic dissolved organic matter pool. Taurine transporters are widespread among members of the marine prokaryotic community, tentatively indicating that taurine might be an important substrate for prokaryotes in the ocean. In this study, we determined prokaryotic taurine assimilation and respiration throughout the water column along two transects in the North Atlantic off the Iberian Peninsula. Taurine assimilation efficiency decreased from the epipelagic waters from 55 ± 14% to 27 ± 20% in the bathypelagic layers (means of both transects). Members of the ubiquitous alphaproteobacterial SAR11 clade accounted for a large fraction of cells taking up taurine, especially in surface waters. Archaea (Thaumarchaeota + Euryarchaeota) were also able to take up taurine in the upper water column, but to a lower extent than Bacteria. The contribution of taurine assimilation to the heterotrophic prokaryotic carbon biomass production ranged from 21% in the epipelagic layer to 16% in the bathypelagic layer. Hence, we conclude that dissolved free taurine is a significant carbon and energy source for prokaryotes throughout the oceanic water column being utilized with similar efficiencies as dissolved free amino acids.

Metagenomic insights into zooplankton-associated bacterial communities.

Zooplankton and microbes play a key role in the ocean's biological cycles by releasing and consuming copious amounts of particulate and dissolved organic matter. Additionally, zooplankton provide a complex microhabitat rich in organic and inorganic nutrients in which bacteria thrive. In this study, we assessed the phylogenetic composition and metabolic potential of microbial communities associated with crustacean zooplankton species collected in the North Atlantic. Using Illumina sequencing of the 16S rRNA gene, we found significant differences between the microbial communities associated with zooplankton and those inhabiting the surrounding seawater. Metagenomic analysis of the zooplankton-associated microbial community revealed a highly specialized bacterial community able to exploit zooplankton as microhabitat and thus, mediating biogeochemical processes generally underrepresented in the open ocean. The zooplankton-associated bacterial community is able to colonize the zooplankton's internal and external surfaces using a large set of adhesion mechanisms and to metabolize complex organic compounds released or exuded by the zooplankton such as chitin, taurine and other complex molecules. Moreover, the high number of genes involved in iron and phosphorus metabolisms in the zooplankton-associated microbiome suggests that this zooplankton-associated bacterial community mediates specific biogeochemical processes (through the proliferation of specific taxa) that are generally underrepresented in the ambient waters.

Macroecological patterns of archaeal ammonia oxidizers in the Atlantic Ocean.

Macroecological patterns are found in animals and plants, but also in micro-organisms. Macroecological and biogeographic distribution patterns in marine Archaea, however, have not been studied yet. Ammonia-oxidizing Archaea (AOA) show a bipolar distribution (i.e. similar communities in the northernmost and the southernmost locations, separated by distinct communities in the tropical and gyral regions) throughout the Atlantic, detectable from epipelagic to upper bathypelagic layers (<2000 m depth). This tentatively suggests an influence of the epipelagic conditions of organic matter production on bathypelagic AOA communities. The AOA communities below 2000 m depth showed a less pronounced biogeographic distribution pattern than the upper 2000 m water column. Overall, AOA in the surface and deep Atlantic waters exhibit distance-decay relationships and follow the Rapoport rule in a similar way as bacterial communities and macroorganisms. This indicates a major role of environmental conditions in shaping the community composition and assembly (species sorting) and no, or only weak limits for dispersal in the oceanic thaumarchaeal communities. However, there is indication of a different strength of these relationships between AOA and Bacteria, linked to the intrinsic differences between these two domains.

Archaeal amoA gene diversity points to distinct biogeography of ammonia-oxidizing Crenarchaeota in the ocean.

Mesophilic ammonia-oxidizing Archaea (AOA) are abundant in a diverse range of marine environments, including the deep ocean, as revealed by the quantification of the archaeal amoA gene encoding the alpha-subunit of the ammonia monooxygenase. Using two different amoA primer sets, two distinct ecotypes of marine Crenarchaeota Group I (MCGI) were detected in the waters of the tropical Atlantic and the coastal Arctic. The HAC-AOA ecotype (high ammonia concentration AOA) was ≈ 8000 times and 15 times more abundant in the coastal Arctic and the top 300 m layer of the open equatorial Atlantic, respectively, than the LAC-AOA (low ammonia concentration AOA) ecotype. In contrast, the LAC-AOA ecotype dominated the lower meso- and bathypelagic waters of the tropical Atlantic (≈ 50 times more abundant than the HAC-AOA) where ammonia concentrations are well below the detection limit using conventional spectrophotometric or fluorometric methods. Cluster analysis of the sequences from the clone libraries obtained by the two amoA primer sets revealed two phylogenetically distinct clusters. Taken together, our results suggest the presence of two ecotypes of archaeal ammonia oxidizers corresponding to the medium (1.24 µM on average in the coastal Arctic) and low ammonia concentration (< 0.01 µM) in the shallow and the deep waters respectively.

Viruses under the Antarctic Ice Shelf are active and potentially involved in global nutrient cycles.

Viruses play an important role in the marine ecosystem. However, our comprehension of viruses inhabiting the dark ocean, and in particular, under the Antarctic Ice Shelves, remains limited. Here, we mine single-cell genomic, transcriptomic, and metagenomic data to uncover the viral diversity, biogeography, activity, and their role as metabolic facilitators of microbes beneath the Ross Ice Shelf. This is the largest Antarctic ice shelf with a major impact on global carbon cycle. The viral community found in the cavity under the ice shelf mainly comprises endemic viruses adapted to polar and mesopelagic environments. The low abundance of genes related to lysogenic lifestyle (<3%) does not support a predominance of the Piggyback-the-Winner hypothesis, consistent with a low-productivity habitat. Our results indicate a viral community actively infecting key ammonium and sulfur-oxidizing chemolithoautotrophs (e.g. Nitrosopumilus spp, Thioglobus spp.), supporting a "kill-the-winner" dynamic. Based on genome analysis, these viruses carry specific auxiliary metabolic genes potentially involved in nitrogen, sulfur, and phosphorus acquisition. Altogether, the viruses under Antarctic ice shelves are putatively involved in programming the metabolism of ecologically relevant microbes that maintain primary production in these chemosynthetically-driven ecosystems, which have a major role in global nutrient cycles.

Interplay between autotrophic and heterotrophic prokaryotic metabolism in the bathypelagic realm revealed by metatranscriptomic analyses.

BACKGROUND: Heterotrophic microbes inhabiting the dark ocean largely depend on the settling of organic matter from the sunlit ocean. However, this sinking of organic materials is insufficient to cover their demand for energy and alternative sources such as chemoautotrophy have been proposed. Reduced sulfur compounds, such as thiosulfate, are a potential energy source for both auto- and heterotrophic marine prokaryotes. METHODS: Seawater samples were collected from Labrador Sea Water (LSW, ~ 2000 m depth) in the North Atlantic and incubated in the dark at in situ temperature unamended, amended with 1 µM thiosulfate, or with 1 µM thiosulfate plus 10 µM glucose and 10 µM acetate (thiosulfate plus dissolved organic matter, DOM). Inorganic carbon fixation was measured in the different treatments and samples for metatranscriptomic analyses were collected after 1 h and 72 h of incubation. RESULTS: Amendment of LSW with thiosulfate and thiosulfate plus DOM enhanced prokaryotic inorganic carbon fixation. The energy generated via chemoautotrophy and heterotrophy in the amended prokaryotic communities was used for the biosynthesis of glycogen and phospholipids as storage molecules. The addition of thiosulfate stimulated unclassified bacteria, sulfur-oxidizing Deltaproteobacteria (SAR324 cluster bacteria), Epsilonproteobacteria (Sulfurimonas sp.), and Gammaproteobacteria (SUP05 cluster bacteria), whereas, the amendment with thiosulfate plus DOM stimulated typically copiotrophic Gammaproteobacteria (closely related to Vibrio sp. and Pseudoalteromonas sp.). CONCLUSIONS: The gene expression pattern of thiosulfate utilizing microbes specifically of genes involved in energy production via sulfur oxidation and coupled to CO2 fixation pathways coincided with the change in the transcriptional profile of the heterotrophic prokaryotic community (genes involved in promoting energy storage), suggesting a fine-tuned metabolic interplay between chemoautotrophic and heterotrophic microbes in the dark ocean. Video Abstract.

Phylogenetically and functionally diverse microorganisms reside under the Ross Ice Shelf.

Throughout coastal Antarctica, ice shelves separate oceanic waters from sunlight by hundreds of meters of ice. Historical studies have detected activity of nitrifying microorganisms in oceanic cavities below permanent ice shelves. However, little is known about the microbial composition and pathways that mediate these activities. In this study, we profiled the microbial communities beneath the Ross Ice Shelf using a multi-omics approach. Overall, beneath-shelf microorganisms are of comparable abundance and diversity, though distinct composition, relative to those in the open meso- and bathypelagic ocean. Production of new organic carbon is likely driven by aerobic lithoautotrophic archaea and bacteria that can use ammonium, nitrite, and sulfur compounds as electron donors. Also enriched were aerobic organoheterotrophic bacteria capable of degrading complex organic carbon substrates, likely derived from in situ fixed carbon and potentially refractory organic matter laterally advected by the below-shelf waters. Altogether, these findings uncover a taxonomically distinct microbial community potentially adapted to a highly oligotrophic marine environment and suggest that ocean cavity waters are primarily chemosynthetically-driven systems.

Changes in viral and bacterial communities during the ice-melting season in the coastal Arctic (Kongsfjorden, Ny-Ålesund).

Microbial communities in Arctic coastal waters experience dramatic changes in environmental conditions during the spring to summer transition period, potentially leading to major variations in the relationship between viral and prokaryotic communities. To document these variations, a number of physico-chemical and biological parameters were determined during the ice-melting season in the coastal Arctic (Kongsfjorden, Ny-Ålesund, Spitsbergen). The bacterial and viral abundance increased during the spring to summer transition period, probably associated to the increase in temperature and the development of a phytoplankton bloom. The increase in viral abundance was less pronounced than the increase in prokaryotic abundance; consequently, the viral to prokaryotic abundance ratio decreased. The bacterial and viral communities were stratified as determined by Automated Ribosomal Intergenic Spacer Analysis and Randomly Amplified Polymorphic DNA-PCR respectively. Both the bacterial and viral communities were characterized by a relatively low number of operational taxonomic units (OTUs). Despite the apparent low complexity of the bacterial and viral communities, the link between these two communities was weak over the melting season, as suggested by the different trends of prokaryotic and viral abundance during the sampling period. This weak relationship between the two communities might be explained by UV radiation and suspended particles differently affecting the viruses and prokaryotes in the coastal Arctic during this period. Based on our results, we conclude that the viral and bacterial communities in the Arctic were strongly affected by the variability of the environmental conditions during the transition period between spring and summer.

An Advanced Protocol for the Quantification of Marine Sediment Viruses via Flow Cytometry.

Viruses are highly abundant, diverse, and active components of marine environments. Flow cytometry has helped to increase the understanding of their impact on shaping microbial communities and biogeochemical cycles in the pelagic zone. However, to date, flow cytometric quantification of sediment viruses is still hindered by interference from the sediment matrix. Here, we developed a protocol for the enumeration of marine sediment viruses by flow cytometry based on separation of viruses from sediment particles using a Nycodenz density gradient. Results indicated that there was sufficient removal of background interference to allow for flow cytometric quantification. Applying this new protocol to deep-sea and tidal-flat samples, viral abundances enumerated by flow cytometry correlated well (R2 = 0.899) with counts assessed by epifluorescence microscopy over several orders of magnitude from marine sediments of various compositions. Further optimization may be needed for sediments with low biomass or high organic content. Overall, the new protocol enables fast and accurate quantification of marine sediment viruses, and opens up the options for virus sorting, targeted viromics, and single-virus sequencing.

Combined Methylome, Transcriptome and Proteome Analyses Document Rapid Acclimatization of a Bacterium to Environmental Changes.

Polynucleobacter asymbioticus strain QLW-P1DMWA-1T represents a group of highly successful heterotrophic ultramicrobacteria that is frequently very abundant (up to 70% of total bacterioplankton) in freshwater habitats across all seven continents. This strain was originally isolated from a shallow Alpine pond characterized by rapid changes in water temperature and elevated UV radiation due to its location at an altitude of 1300 m. To elucidate the strain's adjustment to fluctuating environmental conditions, we recorded changes occurring in its transcriptomic and proteomic profiles under contrasting experimental conditions by simulating thermal conditions in winter and summer as well as high UV irradiation. To analyze the potential connection between gene expression and regulation via methyl group modification of the genome, we also analyzed its methylome. The methylation pattern differed between the three treatments, pointing to its potential role in differential gene expression. An adaptive process due to evolutionary pressure in the genus was deduced by calculating the ratios of non-synonymous to synonymous substitution rates for 20 Polynucleobacter spp. genomes obtained from geographically diverse isolates. The results indicate purifying selection.

Bacterial Stress and Mortality may be a Source of Cell-free Enzymatic Activity in the Marine Environment.

Marine microbes play a central role in driving biogeochemical cycles. Microbial extracellular enzymatic activities (EEA) are the 'gatekeeper' of the marine carbon cycle, and these enzymes may be found attached to cells or dissolved (cell-free). Recent studies indicated that the proportion of dissolved enzymatic activity is generally similar to (if not higher than) cell-attached activity. Thus, it is critical to understand the sources and sinks of cell-free EEA in the ocean. We herein empirically tested whether bacterial stress and mortality (induced by mitomycin C) are a source of the cell-free EEA of alkaline phosphatase (APase), beta-glucosidase (BGase), and leucine aminopeptidase (LAPase). We found that bacterial stress and mortality caused relative increases in the proportion of dissolved relative to total EEA of up to 10.5% for APase, 13.5% for BGase, and 7.3% for LAPase. These relative increases in dissolved EEA corresponded to absolute increases in the cell-free pool of 4.8, 7.2, and 3.8% for APase, BGase and LAPase, respectively. Collectively, our results contribute relevant information on the origin of free dissolved extracellular enzymes in marine waters, indicating that bacterial stress and mortality are a source of cell-free enzymatic activity and suggesting a potential link between microbial interactions and the degradation of organic matter via the release of cell-free enzymes.

Teasing apart the different size pools of extracellular enzymatic activity in the ocean.

Extracellular enzymatic activity (EEA) is performed by cell-associated and cell-free (i.e., "dissolved") enzymes. This cell-free fraction is operationally defined as passing through a 0.22 µm filter. The contribution of cell-free to total EEA is comparable to the cell-associated counterpart, so it is critical to understand what controls the relative importance of cell-free versus cell-associated EEA. However, attempts to tease apart the contribution of EEAs in the so-called dissolved fraction (<0.22 µm) in general, and of the nanoparticle size fraction (0.020-0.20 µm) in particular, to the total EEA pool are lacking. Here we performed experiments with Northern and Southern Hemisphere coastal waters to characterize the potential contribution of that nanoparticle fraction to the total EEA fraction of alkaline phosphatase, beta-glucosidase and leucine aminopeptidase. We found a significant contribution (in both hemispheres) of the nanoparticle fraction to the total EEA pool (up to 53%) that differed depending on the enzyme type and location. Collectively, our results indicate that a significant fraction of the so-called "dissolved EEA" is not really dissolved but associated to nanoparticles, colloidal nanogels and/or viruses. Thus, the total marine EEA pool can actually be divided into a cell-associated, undissolved-cell-free (associated to nano-particle of different origins such as viruses and nanogels) and a dissolved-cell-free pools. Our results also imply that the dissolved EEA pool is more complex than thus far anticipated. Future research will be now needed to further characterize the factors controlling the relative importance of these different pools of EEA, which are key in the recycling of organic matter in the ocean.

Viral Communities in the Global Deep Ocean Conveyor Belt Assessed by Targeted Viromics.

Viruses are an abundant, diverse and dynamic component of marine and terrestrial ecosystems. In the ocean, viruses play a key role in the biogeochemical cycles and controlling microbial abundance, diversity and evolution. Recent metagenomics studies assessed the structure of the viral community in the upper ocean. However, little is known about the compositional changes in viral communities along the deep ocean conveyor belt. To assess potential changes in the viral community in the global deep-water circulation system, water samples were collected in the core of the North Atlantic Deep Water (NADW) (∼2,500 m) and Pacific Antarctic Bottom Water (∼4,000 m). Microbial and viral abundance were evaluated by flow cytometry. Subsequently, flow cytometry was used to sort virus-like particles and next generation sequencing was applied to build DNA libraries from the sorted virus populations. The viral communities were highly diverse across different oceanic regions with high dissimilarity between samples. Only 18% of the viral protein clusters were shared between the NADW and the Pacific Antarctic Bottom Water. Few viral groups, mainly associated with uncultured environmental and uncultured Mediterranean viruses were ubiquitously distributed along the global deep-water circulation system. Thus, our results point to a few groups of widely distributed abundant viruses in addition to the presence of rare and diverse types of viruses at a local scale.

Seasonal dynamics of marine snow-associated and free-living demethylating bacterial communities in the coastal northern Adriatic Sea.

The extent of DMSP demethylation has been hypothesized to depend on DMSP availability and bacterial sulfur demand, which might lead to niche differentiation of the demethylating bacterial community. In this study, we determined DMSP concentrations in marine snow and the ambient water over a seasonal cycle and linked DMSP concentrations to the abundance of bacteria harbouring the demethylation dmdA gene in the Adriatic Sea. In marine snow, DMSP concentrations were up to four times higher than in the ambient water and three times higher in marine snow in summer than in winter. The average dmdA:recA gene ratio over the sampling period was 0.40 ± 0.24 in marine snow and 0.48 ± 0.21 in the ambient water. However, at the subclade level, differences in the demethylating bacterial community of marine snow and the ambient water were apparent. Seasonal patterns of potentially demethylating bacteria were best visible at the oligotype level. In the ambient water, the SAR116 and the OM60/NOR5 clade were composed of oligotypes that correlated to high DMSP concentrations, while oligotypes of the Rhodospirillales correlated to low DMSP concentrations. Our results revealed a pronounced seasonal variability and spatial heterogeneity in DMSP concentrations and the associated demethylating bacterial community.

Niche Differentiation of Aerobic and Anaerobic Ammonia Oxidizers in a High Latitude Deep Oxygen Minimum Zone.

To elucidate the potential for nitrification and denitrification processes in a high latitude deep oxygen minimum zone (OMZ) we determined the abundance and community composition of the main microbial players in the aerobic and anaerobic (anammox) ammonium oxidation and denitrification processes in the Gulf of Alaska throughout the water column. Within the dominant bacterial groups, Flavobacterales, Rhodobacterales, Actinomarinales, and SAR86 were more abundant in epipelagic waters and decreased with depth, whereas SAR11, SAR324, Marinimicrobia, and Thiomicrospirales increased their contribution to the bacterial community with depth. Nitrosopumilaceae also increased with depth and dominated the OMZ and bathypelagic archaeal communities. Euryarchaeota Marine Group II exhibited an opposite depth pattern to Nitrosopumilaceae, whereas Marine Group III and Woesearchaeota were more abundant in the bathypelagic realm. Candidatus Brocadia contributed 70-100% of the anammox bacterial community throughout the water column. Archaeal ammonia oxidizers (AOA) dominated the microbial community involved in the nitrogen cycle. Two AOA ecotypes, the high ammonia (HAC) and low ammonia (LAC)-AOA, characterized by distinct genes for aerobic ammonia oxidation (amoA) and for denitrification (nirK), exhibited a distinct distribution pattern related to depth and ammonia concentrations. HAC-AOA dominated in epipelagic (80.5 ± 28.3% of total AOA) oxygenated and ammonia-rich waters, and LAC-AOA dominated in the OMZ (90.9 ± 5.1%) and bathypelagic waters (85.5 ± 13.5%), characterized by lower oxygen and ammonia concentrations. Bacterial denitrifiers (3.7 ± 6.9 bacterial nirK gene mL-1) and anaerobic ammonia oxidizers (78 ± 322 anammox 16S rRNA genes L-1) were low in abundance under the oxygen conditions in the Gulf of Alaska throughout the water column. The widespread distribution of bacterial denitrifiers and anaerobic ammonia oxidizers in low abundances reveals a reservoir of genetic and metabolic potential ready to colonize the environment under the predicted increase of OMZs in the ocean. Taken together, our results reinforce the niche partitioning of archaeal ammonia oxidizers based on their distinct metabolic characteristics resulting in the dominance of LAC-AOA in a high latitude deep OMZ. Considering the different ecological roles and functions of the two archaeal ecotypes, the expansion of the zones dominated by the LAC-ecotype might have implications for the nitrogen cycle in the future ocean.

Marine microbial metagenomes sampled across space and time.

Recent advances in understanding the ecology of marine systems have been greatly facilitated by the growing availability of metagenomic data, which provide information on the identity, diversity and functional potential of the microbial community in a particular place and time. Here we present a dataset comprising over 5 terabases of metagenomic data from 610 samples spanning diverse regions of the Atlantic and Pacific Oceans. One set of metagenomes, collected on GEOTRACES cruises, captures large geographic transects at multiple depths per station. The second set represents two years of time-series data, collected at roughly monthly intervals from 3 depths at two long-term ocean sampling sites, Station ALOHA and BATS. These metagenomes contain genomic information from a diverse range of bacteria, archaea, eukaryotes and viruses. The data's utility is strengthened by the availability of extensive physical, chemical, and biological measurements associated with each sample. We expect that these metagenomes will facilitate a wide range of comparative studies that seek to illuminate new aspects of marine microbial ecosystems.