Oxygen availability drives changes in microbial diversity and biogeochemical cycling between the aerobic surface layer and the anaerobic core in nitrite-rich anoxic marine zones (AMZs), which constitute huge oxygen-depleted regions in the tropical oceans. The current paradigm is that primary production and nitrification within the oxic surface layer fuel anaerobic processes in the anoxic core of AMZs, where 30-50% of global marine nitrogen loss takes place. Here we demonstrate that oxygenic photosynthesis in the secondary chlorophyll maximum (SCM) releases significant amounts of O 2 to the otherwise anoxic environment. The SCM, commonly found within AMZs, was dominated by the picocyanobacteria Prochlorococcus spp. Free O 2 levels in this layer were, however, undetectable by conventional techniques, reflecting a tight coupling between O 2 production and consumption by aerobic processes under apparent anoxic conditions. Transcriptomic analysis of the microbial community in the seemingly anoxic SCM revealed the enhanced expression of genes for aerobic processes, such as nitrite oxidation. The rates of gross O 2 production and carbon fixation in the SCM were found to be similar to those reported for nitrite oxidation, as well as for anaerobic dissimilatory nitrate reduction and sulfate reduction, suggesting a significant effect of local oxygenic photosynthesis on Pacific AMZ biogeochemical cycling.Prochlorococcus | oxygen minimum zone | secondary chlorophyll maximum | metatranscriptomics | aerobic metabolism
Anaerobic ammonium oxidation (anammox) contributes substantially to ocean nitrogen loss, particularly in anoxic marine zones (AMZs). Ammonium is scarce in AMZs, raising the hypothesis that organic nitrogen compounds may be ammonium sources for anammox. Biochemical measurements suggest that the organic compounds urea and cyanate can support anammox in AMZs. However, it is unclear if anammox bacteria degrade these compounds to ammonium themselves, or rely on other organisms for this process. Genes for urea degradation have not been found in anammox bacteria, and genomic evidence for cyanate use for anammox is limited to a cyanase gene recovered from the sediment bacterium Candidatus Scalindua profunda. Here, analysis of Ca. Scalindua single amplified genomes from the Eastern Tropical North Pacific AMZ revealed genes for urea degradation and transport, as well as for cyanate degradation. Urease and cyanase genes were transcribed, along with anammox genes, in the AMZ core where anammox rates peaked. Homologs of these genes were also detected in meta-omic datasets from major AMZs in the Eastern Tropical South Pacific and Arabian Sea. These results suggest that anammox bacteria from different ocean regions can directly access organic nitrogen substrates. Future studies should assess if and under what environmental conditions these substrates contribute to the ammonium budget for anammox.
Prochlorococcus and Synechococcus are the most abundant free‐living photosynthetic microorganisms in the ocean. Uncultivated lineages of these picocyanobacteria also thrive in the dimly illuminated upper part of oxygen‐deficient zones (ODZs), where an important portion of ocean nitrogen (N) loss takes place via denitrification and anaerobic ammonium oxidation. Recent metagenomic studies revealed that ODZ Prochlorococcus have the genetic potential for using different N forms, including nitrate and nitrite, uncommon N sources for Prochlorococcus, but common for Synechococcus. To determine which N sources ODZ picocyanobacteria are actually using in nature, the cellular 15N natural abundance (δ15N) and assimilation rates of different N compounds were determined using cell sorting by flow cytometry and mass spectrometry. The natural δ15N of the ODZ Prochlorococcus varied from −4.0‰ to 13.0‰ (n = 9), with 50% of the values in the range of −2.1–2.6‰. While the highest values suggest nitrate use, most observations indicate the use of nitrite, ammonium, or a mixture of N sources. Meanwhile, incubation experiments revealed potential assimilation rates of ammonium and urea in the same order of magnitude as that expected for total N in several environments including ODZs, whereas rates of nitrite and nitrate assimilation were very low. Our results thus indicate that reduced forms of N and nitrite are the dominant sources for ODZ picocyanobacteria, although nitrate might be important on some occasions. ODZ picocyanobacteria might thus represent potential competitors with anammox bacteria for ammonium and nitrite, with ammonia‐oxidizing archaea for ammonium, and with nitrite‐oxidizing bacteria for nitrite.
Oxygen minimum zones (OMZs) are critical to marine nitrogen cycling and global climate change. While OMZ microbial communities are relatively well-studied, little is known about their viruses. Here, we assess the viral community ecology of 22 deeply sequenced viral metagenomes along a gradient of oxygenated to anoxic waters (<0.02 μmol/l O 2 ) in the Eastern Tropical South Pacific (ETSP) OMZ. We identified 46 127 viral populations (≥5 kb), which augments the known viruses from ETSP by 10-fold. Viral communities clustered into six groups that correspond to oceanographic features. Oxygen concentration was the predominant environmental feature driving viral community structure. Alpha and beta diversity of viral communities in the anoxic zone were lower than in surface waters, which parallels the low microbial diversity seen in other studies. ETSP viruses were largely endemic, with the majority of shared viruses (87%) also present in other OMZ samples. We detected 543 putative viral-encoded auxiliary metabolic genes (AMGs), of which some have a distribution that reflects physico-chemical characteristics across depth. Together these findings provide an ecological baseline for viral community structure, drivers and population variability in OMZs that will help future studies assess the role of viruses in these climatecritical environments.
It is commonly known that phytoplankton have a pivotal role in marine biogeochemistry and ecosystems as carbon fixers and oxygen producers, but their response to deoxygenation has scarcely been studied. Nonetheless, in the major oceanic oxygen minimum zones (OMZs), all surface phytoplankton groups, regardless of size, disappear and are replaced by unique cyanobacteria lineages below the oxycline. To develop reasonable hypotheses to explain this pattern, we conduct a review of available information on OMZ phytoplankton, and we re-analyze previously published data (flow cytometric and hydrographic) on vertical structure of phytoplankton communities in relation to light and O 2 levels. We also review the physical constraints on O 2 acquisition as well as O 2 -dependent metabolisms in phototrophs. These considerations, along with estimates of the photosynthetic capacity of phytoplankton along OMZ depth profiles using published data, suggest that top-down grazing, respiratory demand, and irradiance are insufficient to fully explain the vertical structure observed in the upper, more sunlit portions of OMZs. Photorespiration and water-water cycles are O 2 -dependent pathways with low O 2 affinities. Although their metabolic roles are still poorly understood, a hypothetical dependence on such pathways by the phytoplankton adapted to the oxic ocean might explain vertical patterns in OMZs and results of laboratory experiments. This can be represented in a simple model in which the requirement for photorespiration in surface phytoplankton and O 2 -inhibition of OMZ lineages reproduces the observed vertical fluorescence profiles and the replacement of phytoplankton adapted to O 2 by lineages restricted to the most O 2 -deficient waters. A high O 2 requirement by modern phytoplankton would suggest a positive feedback that intensifies trends in OMZ extent and ocean oxygenation or deoxygenation, both in Earth's past and in response to current climate change.Deoxygenation in oceans is a growing phenomenon associated with anthropogenic climate change with several interacting causes that include changes in circulation and mixing, decreased solubility of oxygen (O 2 ) as temperature increases, and possibly biogeochemical changes (Ito et al., 2017;Schmidtko et al. 2017;Oschlies et al. 2018). The first evidence of a decline in dissolved O 2 was recorded in the 1980s (Horak et al. 2016;Ito et al. 2017). Oxygen minimum zones (OMZs) are naturally occurring zones where O 2 in sub-surface waters drops below a threshold that varies among authors but is
SummaryOxygen minimum zones (OMZs) are critical to marine nitrogen cycling and global climate change. While OMZ microbial communities are relatively well-studied, little is known about their viruses. Here we assess the viral community ecology of 22 deeply sequenced viral metagenomes along a gradient of surface oxygenated to anoxic waters (< 0.02 μmol/L O2) in the Eastern Tropical South Pacific (ETSP) OMZ. We identified 46,127 viral populations (>5 kb), which augments the known viruses at this site by 10-fold. ETSP viral communities clustered into 6 groups that correspond to oceanographic features, with 3 clusters representing samples from suboxic to anoxic waters. Oxygen concentration was the predominant environmental feature driving viral community structure. Alpha and beta diversity of viral communities in the anoxic zone were lower than in surface waters, which parallels the low microbial diversity seen in other studies. Viruses were largely endemic as few (6% of viruses from this study) were found in at least another marine metagenome, and of those, most (77%) were restricted to other OMZs. Together these findings provide an ecological baseline for viral community structure, drivers and population variability in OMZs that will help future studies assess the role of viruses in these climate-critical environments.Originality-Significance StatementMarine oxygen minimum zones (OMZs) are unique and important ocean ecosystems where microbes drive climate-altering nutrient transformations. This study provides a baseline, deeply sequenced viral metagenomic dataset and reference viral genomes to assess ecological change and drivers across the oxygenated surface to de-oxygenated deep waters of the Eastern Tropical South Pacific (ETSP) OMZ. Community ecological assessment of the ETSP viromes reveals a relatively low diversity viral community with a high degree of endemic populations in the OMZ waters.
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