skip to main content

Title: Substantial oxygen consumption by aerobic nitrite oxidation in oceanic oxygen minimum zones
Abstract

Oceanic oxygen minimum zones (OMZs) are globally significant sites of biogeochemical cycling where microorganisms deplete dissolved oxygen (DO) to concentrations <20 µM. Amid intense competition for DO in these metabolically challenging environments, aerobic nitrite oxidation may consume significant amounts of DO and help maintain low DO concentrations, but this remains unquantified. Using parallel measurements of oxygen consumption rates and15N-nitrite oxidation rates applied to both water column profiles and oxygen manipulation experiments, we show that the contribution of nitrite oxidation to overall DO consumption systematically increases as DO declines below 2 µM. Nitrite oxidation can account for all DO consumption only under DO concentrations <393 nM found in and below the secondary chlorophyll maximum. These patterns are consistent across sampling stations and experiments, reflecting coupling between nitrate reduction and nitrite-oxidizingNitrospinawith high oxygen affinity (based on isotopic and omic data). Collectively our results demonstrate that nitrite oxidation plays a pivotal role in the maintenance and biogeochemical dynamics of OMZs.

Authors:
; ; ; ; ; ; ; ; ; ; ;
Publication Date:
NSF-PAR ID:
10360690
Journal Name:
Nature Communications
Volume:
12
Issue:
1
ISSN:
2041-1723
Publisher:
Nature Publishing Group
Sponsoring Org:
National Science Foundation
More Like this
  1. The Eastern Tropical North Pacific (ETNP) is a large, persistent, and intensifying oxygen minimum zone (OMZ) that accounts for almost half of the total area of global OMZs. Within the OMZ core (350–700 m depth), dissolved oxygen is typically near or below the analytical detection limit of modern sensors (10 nM). Steep oxygen gradients above and below the OMZ core lead to vertical structuring of microbial communities that also vary between particle-associated (PA) and free-living (FL) size fractions. Here, we use 16S amplicon sequencing (iTags) to analyze the diversity and distribution of prokaryotic populations between FL and PA size fractions and among the range of ambient redox conditions. The hydrographic conditions at our study area were distinct from those previously reported in the ETNP and other OMZs, such as the ETSP. Trace oxygen concentrations (0.35 mM) were present throughout the OMZ core at our sampling location. Consequently, nitrite accumulations typically reported for OMZ cores were absent as were sequences for anammox bacteria (Brocadiales genus Candidatus Scalindua), which are commonly found across oxic-anoxic boundaries in other systems. However, ammonia-oxidizing bacteria (AOB) and archaea (AOA) distributions and maximal autotrophic carbon assimilation rates (1.4 mM C d􀀀1) coincided with a pronounced ammonium concentrationmore »maximum near the top of the OMZ core. In addition, members of the genus Nitrospina, a dominant nitrite-oxidizing bacterial (NOB) clade were present suggesting that both ammonia and nitrite oxidation occur at trace oxygen concentrations. Analysis of similarity test (ANOSIM) and Non-metric Dimensional Scaling (nMDS) revealed that bacterial and archaeal phylogenetic representations were significantly different between size fractions. Based on ANOSIM and iTag profiles, composition of PA assemblages was less influenced by the prevailing depth-dependent biogeochemical regime than the FL fraction. Based on the presence of AOA, NOB and trace oxygen in the OMZ core we suggest that nitrification is an active process in the nitrogen cycle of this region of the ETNP OMZ.« less
  2. Abstract

    Nitrite is a pivotal component of the marine nitrogen cycle. The fate of nitrite determines the loss or retention of fixed nitrogen, an essential nutrient for all organisms. Loss occurs via anaerobic nitrite reduction to gases during denitrification and anammox, while retention occurs via nitrite oxidation to nitrate. Nitrite oxidation is usually represented in biogeochemical models by one kinetic parameter and one oxygen threshold, below which nitrite oxidation is set to zero. Here we find that the responses of nitrite oxidation to nitrite and oxygen concentrations vary along a redox gradient in a Pacific Ocean oxygen minimum zone, indicating niche differentiation of nitrite-oxidizing assemblages. Notably, we observe the full inhibition of nitrite oxidation by oxygen addition and nitrite oxidation coupled with nitrogen loss in the absence of oxygen consumption in samples collected from anoxic waters. Nitrite-oxidizing bacteria, including novel clades with high relative abundance in anoxic depths, were also detected in the same samples. Mechanisms corresponding to niche differentiation of nitrite-oxidizing bacteria across the redox gradient are considered. Implementing these mechanisms in biogeochemical models has a significant effect on the estimated fixed nitrogen budget.

  3. Abstract

    The genusNitrospirais the most widespread group of nitrite-oxidizing bacteria and thrives in diverse natural and engineered ecosystems. Nitrospira marinaNb-295Twas isolated from the ocean over 30 years ago; however, its genome has not yet been analyzed. Here, we investigated the metabolic potential ofN. marinabased on its complete genome sequence and performed physiological experiments to test genome-derived hypotheses. Our data confirm thatN. marinabenefits from additions of undefined organic carbon substrates, has adaptations to resist oxidative, osmotic, and UV light-induced stress and low dissolvedpCO2, and requires exogenous vitamin B12. In addition,N. marinais able to grow chemoorganotrophically on formate, and is thus not an obligate chemolithoautotroph. We further investigated the proteomic response ofN. marinato low (∼5.6 µM) O2concentrations. The abundance of a potentially more efficient CO2-fixing pyruvate:ferredoxin oxidoreductase (POR) complex and a high-affinitycbb3-type terminal oxidase increased under O2limitation, suggesting a role in sustaining nitrite oxidation-driven autotrophy. This putatively more O2-sensitive POR complex might be protected from oxidative damage by Cu/Zn-binding superoxide dismutase, which also increased in abundance under low O2conditions. Furthermore, the upregulation of proteins involved in alternative energy metabolisms, including Group 3b [NiFe] hydrogenase and formate dehydrogenase, indicate a high metabolic versatility to survive conditions unfavorable for aerobic nitrite oxidation. In summary, themore »genome and proteome of the first marineNitrospiraisolate identifies adaptations to life in the oxic ocean and provides insights into the metabolic diversity and niche differentiation of NOB in marine environments.

    « less
  4. Abstract

    Dissolved oxygen (DO) concentrations shape the biogeochemistry and ecological structure of aquatic ecosystems; as a result, understanding how and why DO varies in space and time is of fundamental importance. Using high-resolution,in situDO time-series collected over the course of a year in a novel marine ecosystem (Jellyfish Lake, Palau), we show that DO declined throughout the marine lake and subsequently recovered in the upper water column. These shifts were accompanied by variations in water temperature and were correlated to changes in wind, precipitation, and especially sea surface height that occurred during the 2015–2016 El Niño-Southern Oscillation event. Multiple approaches used to calculate rates of community respiration, net community production, and gross primary production from DO changes showed that DO consumption and production did not accelerate nor collapse; instead, their variance increased during lake deoxygenation and recovery, and then stabilized. Spatial and temporal variations in rates were significantly related to climatic variability and changes in DO, and causality testing indicated that these relationships were both correlative and causative. Our data indicate that climatic, physical, and biogeochemical properties and processes collectively regulated DO, producing linked feedbacks that drove DO decline and recovery.

  5. Abstract. Decreasing concentrations of dissolved oxygen in the ocean are considered one of the main threats to marine ecosystems as they jeopardize the growthof higher organisms. They also alter the marine nitrogen cycle, which isstrongly bound to the carbon cycle and climate. While higher organisms ingeneral start to suffer from oxygen concentrations < ∼ 63 µM (hypoxia), the marine nitrogen cycle responds to oxygenconcentration below a threshold of about 20 µM (microbial hypoxia),whereas anoxic processes dominate the nitrogen cycle at oxygenconcentrations of < ∼ 0.05 µM (functionalanoxia). The Arabian Sea and the Bay of Bengal are home to approximately21 % of the total volume of ocean waters revealing microbial hypoxia.While in the Arabian Sea this oxygen minimum zone (OMZ) is also functionallyanoxic, the Bay of Bengal OMZ seems to be on the verge of becoming so. Eventhough there are a few isolated reports on the occurrence of anoxia prior to1960, anoxic events have so far not been reported from the open northernIndian Ocean (i.e., other than on shelves) during the last 60 years.Maintenance of functional anoxia in the Arabian Sea OMZ with oxygenconcentrations ranging between > 0 and ∼ 0.05 µM is highly extraordinary considering that the monsoon reverses thesurface ocean circulation twice a year and turns vast areas of the ArabianSeamore »from an oligotrophic oceanic desert into one of the most productiveregions of the oceans within a few weeks. Thus, the comparably lowvariability of oxygen concentration in the OMZ implies stable balancesbetween the physical oxygen supply and the biological oxygen consumption,which includes negative feedback mechanisms such as reducing oxygenconsumption at decreasing oxygen concentrations (e.g., reduced respiration).Lower biological oxygen consumption is also assumed to be responsible for aless intense OMZ in the Bay of Bengal. According to numerical model results,a decreasing physical oxygen supply via the inflow of water masses from thesouth intensified the Arabian Sea OMZ during the last 6000 years, whereas areduced oxygen supply via the inflow of Persian Gulf Water from the northintensifies the OMZ today in response to global warming. The first issupported by data derived from the sedimentary records, and the latterconcurs with observations of decreasing oxygen concentrations and aspreading of functional anoxia during the last decades in the Arabian Sea.In the Arabian Sea decreasing oxygen concentrations seem to have initiated aregime shift within the pelagic ecosystem structure, and this trend is alsoseen in benthic ecosystems. Consequences for biogeochemical cycles are asyet unknown, which, in addition to the poor representation of mesoscalefeatures in global Earth system models, reduces the reliability of estimatesof the future OMZ development in the northern Indian Ocean.« less