scholarly journals Metagenomic analysis of nitrogen and methane cycling in the Arabian Sea oxygen minimum zone

PeerJ ◽  
2016 ◽  
Vol 4 ◽  
pp. e1924 ◽  
Author(s):  
Claudia Lüke ◽  
Daan R. Speth ◽  
Martine A.R. Kox ◽  
Laura Villanueva ◽  
Mike S.M. Jetten

Oxygen minimum zones (OMZ) are areas in the global ocean where oxygen concentrations drop to below one percent. Low oxygen concentrations allow alternative respiration with nitrate and nitrite as electron acceptor to become prevalent in these areas, making them main contributors to oceanic nitrogen loss. The contribution of anammox and denitrification to nitrogen loss seems to vary in different OMZs. In the Arabian Sea, both processes were reported. Here, we performed a metagenomics study of the upper and core zone of the Arabian Sea OMZ, to provide a comprehensive overview of the genetic potential for nitrogen and methane cycling. We propose that aerobic ammonium oxidation is carried out by a diverse community ofThaumarchaeotain the upper zone of the OMZ, whereas a low diversity ofScalindua-like anammox bacteria contribute significantly to nitrogen loss in the core zone. Aerobic nitrite oxidation in the OMZ seems to be performed byNitrospina spp. and a novel lineage of nitrite oxidizing organisms that is present in roughly equal abundance asNitrospina. Dissimilatory nitrate reduction to ammonia (DNRA) can be carried out by yet unknown microorganisms harbouring a divergentnrfAgene. The metagenomes do not provide conclusive evidence for active methane cycling; however, a low abundance of novel alkane monooxygenase diversity was detected. Taken together, our approach confirmed the genomic potential for an active nitrogen cycle in the Arabian Sea and allowed detection of hitherto overlooked lineages of carbon and nitrogen cycle bacteria.

2020 ◽  
Vol 17 (23) ◽  
pp. 6051-6080
Author(s):  
Tim Rixen ◽  
Greg Cowie ◽  
Birgit Gaye ◽  
Joaquim Goes ◽  
Helga do Rosário Gomes ◽  
...  

Abstract. Decreasing concentrations of dissolved oxygen in the ocean are considered one of the main threats to marine ecosystems as they jeopardize the growth of higher organisms. They also alter the marine nitrogen cycle, which is strongly bound to the carbon cycle and climate. While higher organisms in general start to suffer from oxygen concentrations < ∼ 63 µM (hypoxia), the marine nitrogen cycle responds to oxygen concentration below a threshold of about 20 µM (microbial hypoxia), whereas anoxic processes dominate the nitrogen cycle at oxygen concentrations of < ∼ 0.05 µM (functional anoxia). The Arabian Sea and the Bay of Bengal are home to approximately 21 % of the total volume of ocean waters revealing microbial hypoxia. While in the Arabian Sea this oxygen minimum zone (OMZ) is also functionally anoxic, the Bay of Bengal OMZ seems to be on the verge of becoming so. Even though there are a few isolated reports on the occurrence of anoxia prior to 1960, anoxic events have so far not been reported from the open northern Indian Ocean (i.e., other than on shelves) during the last 60 years. Maintenance of functional anoxia in the Arabian Sea OMZ with oxygen concentrations ranging between > 0 and ∼ 0.05 µM is highly extraordinary considering that the monsoon reverses the surface ocean circulation twice a year and turns vast areas of the Arabian Sea from an oligotrophic oceanic desert into one of the most productive regions of the oceans within a few weeks. Thus, the comparably low variability of oxygen concentration in the OMZ implies stable balances between the physical oxygen supply and the biological oxygen consumption, which includes negative feedback mechanisms such as reducing oxygen consumption at decreasing oxygen concentrations (e.g., reduced respiration). Lower biological oxygen consumption is also assumed to be responsible for a less intense OMZ in the Bay of Bengal. According to numerical model results, a decreasing physical oxygen supply via the inflow of water masses from the south intensified the Arabian Sea OMZ during the last 6000 years, whereas a reduced oxygen supply via the inflow of Persian Gulf Water from the north intensifies the OMZ today in response to global warming. The first is supported by data derived from the sedimentary records, and the latter concurs with observations of decreasing oxygen concentrations and a spreading of functional anoxia during the last decades in the Arabian Sea. In the Arabian Sea decreasing oxygen concentrations seem to have initiated a regime shift within the pelagic ecosystem structure, and this trend is also seen in benthic ecosystems. Consequences for biogeochemical cycles are as yet unknown, which, in addition to the poor representation of mesoscale features in global Earth system models, reduces the reliability of estimates of the future OMZ development in the northern Indian Ocean.


2010 ◽  
Vol 57 (3) ◽  
pp. 384-393 ◽  
Author(s):  
Silvia E. Bulow ◽  
Jeremy J. Rich ◽  
Hema S. Naik ◽  
Anil K. Pratihary ◽  
Bess B. Ward

2014 ◽  
Vol 11 (20) ◽  
pp. 5733-5747 ◽  
Author(s):  
T. Rixen ◽  
A. Baum ◽  
B. Gaye ◽  
B. Nagel

Abstract. The Arabian Sea plays an important role in the marine nitrogen cycle because of its pronounced mid-water oxygen minimum zone (OMZ) in which bio-available nitrate (NO3−) is reduced to dinitrogen gas (N2). As the nitrogen cycle can respond fast to climate-induced changes in productivity and circulation, the Arabian Sea sediments are an important palaeoclimatic archive. In order to understand seasonal and interannual variations in the nitrogen cycle, nutrient data were obtained from the literature published prior to 1993, evaluated, and compared with data measured during five expeditions carried out in the framework of the Joint Global Ocean Flux Study (JGOFS) in the Arabian Sea in 1995 and during a research cruise of RV Meteor in 2007. The data comparison showed that the area characterized by a pronounced secondary nitrite maximum (SNM) was by 63% larger in 1995 than a similarly determined estimate based on pre-JGOFS data. This area, referred to as the core of the denitrifying zone, showed strong seasonal and interannual variations driven by the monsoon. During the SW monsoon, the SNM retreated eastward due to the inflow of oxygen-enriched Indian Ocean Central Water (ICW). During the NE monsoon, the SNM expanded westward because of the reversal of the current regime. On an interannual timescale, a weaker SW monsoon decreased the inflow of ICW from the equatorial Indian Ocean and increased the accumulation of denitrification tracers by extending the residence time of water in the SNM. This is supported by palaeoclimatic studies showing an enhanced preservation of accumulative denitrification tracers in marine sediments in conjunction with a weakening of the SW monsoon during the late Holocene.


2016 ◽  
Vol 113 (40) ◽  
pp. E5925-E5933 ◽  
Author(s):  
Stilianos Louca ◽  
Alyse K. Hawley ◽  
Sergei Katsev ◽  
Monica Torres-Beltran ◽  
Maya P. Bhatia ◽  
...  

Microorganisms are the most abundant lifeform on Earth, mediating global fluxes of matter and energy. Over the past decade, high-throughput molecular techniques generating multiomic sequence information (DNA, mRNA, and protein) have transformed our perception of this microcosmos, conceptually linking microorganisms at the individual, population, and community levels to a wide range of ecosystem functions and services. Here, we develop a biogeochemical model that describes metabolic coupling along the redox gradient in Saanich Inlet—a seasonally anoxic fjord with biogeochemistry analogous to oxygen minimum zones (OMZs). The model reproduces measured biogeochemical process rates as well as DNA, mRNA, and protein concentration profiles across the redox gradient. Simulations make predictions about the role of ubiquitous OMZ microorganisms in mediating carbon, nitrogen, and sulfur cycling. For example, nitrite “leakage” during incomplete sulfide-driven denitrification by SUP05 Gammaproteobacteria is predicted to support inorganic carbon fixation and intense nitrogen loss via anaerobic ammonium oxidation. This coupling creates a metabolic niche for nitrous oxide reduction that completes denitrification by currently unidentified community members. These results quantitatively improve previous conceptual models describing microbial metabolic networks in OMZs. Beyond OMZ-specific predictions, model results indicate that geochemical fluxes are robust indicators of microbial community structure and reciprocally, that gene abundances and geochemical conditions largely determine gene expression patterns. The integration of real observational data, including geochemical profiles and process rate measurements as well as metagenomic, metatranscriptomic and metaproteomic sequence data, into a biogeochemical model, as shown here, enables holistic insight into the microbial metabolic network driving nutrient and energy flow at ecosystem scales.


mBio ◽  
2014 ◽  
Vol 5 (6) ◽  
Author(s):  
Tage Dalsgaard ◽  
Frank J. Stewart ◽  
Bo Thamdrup ◽  
Loreto De Brabandere ◽  
Niels Peter Revsbech ◽  
...  

ABSTRACTA major percentage (20 to 40%) of global marine fixed-nitrogen loss occurs in oxygen minimum zones (OMZs). Concentrations of O2and the sensitivity of the anaerobic N2-producing processes of anammox and denitrification determine where this loss occurs. We studied experimentally how O2at nanomolar levels affects anammox and denitrification rates and the transcription of nitrogen cycle genes in the anoxic OMZ off Chile. Rates of anammox and denitrification were reversibly suppressed, most likely at the enzyme level. Fifty percent inhibition of N2and N2O production by denitrification was achieved at 205 and 297 nM O2, respectively, whereas anammox was 50% inhibited at 886 nM O2. Coupled metatranscriptomic analysis revealed that transcripts encoding nitrous oxide reductase (nosZ), nitrite reductase (nirS), and nitric oxide reductase (norB) decreased in relative abundance above 200 nM O2. This O2concentration did not suppress the transcription of other dissimilatory nitrogen cycle genes, including nitrate reductase (narG), hydrazine oxidoreductase (hzo), and nitrite reductase (nirK). However, taxonomic characterization of transcripts suggested inhibition ofnarGtranscription in gammaproteobacteria, whereas the transcription of anammoxnarG, whose gene product is likely used to oxidatively replenish electrons for carbon fixation, was not inhibited. The taxonomic composition of transcripts differed among denitrification enzymes, suggesting that distinct groups of microorganisms mediate different steps of denitrification. Sulfide addition (1 µM) did not affect anammox or O2inhibition kinetics but strongly stimulated N2O production by denitrification. These results identify new O2thresholds for delimiting marine nitrogen loss and highlight the utility of integrating biogeochemical and metatranscriptomic analyses.IMPORTANCEThe removal of fixed nitrogen via anammox and denitrification associated with low O2concentrations in oceanic oxygen minimum zones (OMZ) is a major sink in oceanic N budgets, yet the sensitivity and dynamics of these processes with respect to O2are poorly known. The present study elucidated how nanomolar O2concentrations affected nitrogen removal rates and expression of key nitrogen cycle genes in water from the eastern South Pacific OMZ, applying state-of-the-art15N techniques and metatranscriptomics. Rates of both denitrification and anammox responded rapidly and reversibly to changes in O2, but denitrification was more O2sensitive than anammox. The transcription of key nitrogen cycle genes did not respond as clearly to O2, although expression of some of these genes decreased. Quantifying O2sensitivity of these processes is essential for predicting through which pathways and in which environments, from wastewater treatment to the open oceans, nitrogen removal may occur.


2007 ◽  
Vol 52 (2) ◽  
pp. 780-786 ◽  
Author(s):  
Andrea Jaeschke ◽  
Ellen C. Hopmans ◽  
Stuart G. Wakeham ◽  
Stefan Schouten ◽  
Jaap S. Sinninghe Damsté

2016 ◽  
Vol 113 (38) ◽  
pp. 10601-10606 ◽  
Author(s):  
Laura A. Bristow ◽  
Tage Dalsgaard ◽  
Laura Tiano ◽  
Daniel B. Mills ◽  
Anthony D. Bertagnolli ◽  
...  

A major percentage of fixed nitrogen (N) loss in the oceans occurs within nitrite-rich oxygen minimum zones (OMZs) via denitrification and anammox. It remains unclear to what extent ammonium and nitrite oxidation co-occur, either supplying or competing for substrates involved in nitrogen loss in the OMZ core. Assessment of the oxygen (O2) sensitivity of these processes down to the O2concentrations present in the OMZ core (<10 nmol⋅L−1) is therefore essential for understanding and modeling nitrogen loss in OMZs. We determined rates of ammonium and nitrite oxidation in the seasonal OMZ off Concepcion, Chile at manipulated O2levels between 5 nmol⋅L−1and 20 μmol⋅L−1. Rates of both processes were detectable in the low nanomolar range (5–33 nmol⋅L−1O2), but demonstrated a strong dependence on O2concentrations with apparent half-saturation constants (Kms) of 333 ± 130 nmol⋅L−1O2for ammonium oxidation and 778 ± 168 nmol⋅L−1O2for nitrite oxidation assuming one-component Michaelis–Menten kinetics. Nitrite oxidation rates, however, were better described with a two-component Michaelis–Menten model, indicating a high-affinity component with aKmof just a few nanomolar. As the communities of ammonium and nitrite oxidizers were similar to other OMZs, these kinetics should apply across OMZ systems. The high O2affinities imply that ammonium and nitrite oxidation can occur within the OMZ core whenever O2is supplied, for example, by episodic intrusions. These processes therefore compete with anammox and denitrification for ammonium and nitrite, thereby exerting an important control over nitrogen loss.


2013 ◽  
Vol 10 (6) ◽  
pp. 3559-3591 ◽  
Author(s):  
E. Gutknecht ◽  
I. Dadou ◽  
B. Le Vu ◽  
G. Cambon ◽  
J. Sudre ◽  
...  

Abstract. The Eastern Boundary Upwelling Systems (EBUS) contribute to one fifth of the global catches in the ocean. Often associated with Oxygen Minimum Zones (OMZs), EBUS represent key regions for the oceanic nitrogen (N) cycle. Important bioavailable N loss due to denitrification and anammox processes as well as greenhouse gas emissions (e.g, N2O) occur also in these EBUS. However, their dynamics are currently crudely represented in global models. In the climate change context, improving our capability to properly represent these areas is crucial due to anticipated changes in the winds, productivity, and oxygen content. We developed a biogeochemical model (BioEBUS) taking into account the main processes linked with EBUS and associated OMZs. We implemented this model in a 3-D realistic coupled physical/biogeochemical configuration in the Namibian upwelling system (northern Benguela) using the high-resolution hydrodynamic ROMS model. We present here a validation using in situ and satellite data as well as diagnostic metrics and sensitivity analyses of key parameters and N2O parameterizations. The impact of parameter values on the OMZ off Namibia, on N loss, and on N2O concentrations and emissions is detailed. The model realistically reproduces the vertical distribution and seasonal cycle of observed oxygen, nitrate, and chlorophyll a concentrations, and the rates of microbial processes (e.g, NH4+ and NO2− oxidation, NO3− reduction, and anammox) as well. Based on our sensitivity analyses, biogeochemical parameter values associated with organic matter decomposition, vertical sinking, and nitrification play a key role for the low-oxygen water content, N loss, and N2O concentrations in the OMZ. Moreover, the explicit parameterization of both steps of nitrification, ammonium oxidation to nitrate with nitrite as an explicit intermediate, is necessary to improve the representation of microbial activity linked with the OMZ. The simulated minimum oxygen concentrations are driven by the poleward meridional advection of oxygen-depleted waters offshore of a 300 m isobath and by the biogeochemical activity inshore of this isobath, highlighting a spatial shift of dominant processes maintaining the minimum oxygen concentrations off Namibia. In the OMZ off Namibia, the magnitude of N2O outgassing and of N loss is comparable. Anammox contributes to about 20% of total N loss, an estimate lower than currently assumed (up to 50%) for the global ocean.


2016 ◽  
Vol 186 ◽  
pp. 24-32 ◽  
Author(s):  
Parthasarathi Chakraborty ◽  
Robert P. Mason ◽  
Saranya Jayachandran ◽  
Krushna Vudamala ◽  
Kazip Armoury ◽  
...  

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