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Aerobic Microbial Respiration In Oceanic Oxygen Minimum Zones.

Kalvelage T, Lavik G, Jensen MM, Revsbech NP, Löscher C, Schunck H, Desai DK, Hauss H, Kiko R, Holtappels M, LaRoche J, Schmitz RA, Graco MI, Kuypers MM - PLoS ONE (2015)

Bottom Line: Consistently observed oxygen consumption in samples retrieved throughout the lower OMZs hints at efficient exploitation of vertically and laterally advected, oxygenated waters in this zone by aerobic microorganisms.In accordance, metagenomic and metatranscriptomic analyses identified genes encoding for aerobic terminal oxidases and demonstrated their expression by diverse microbial communities, even in virtually anoxic waters.Our results suggest that microaerobic respiration is a major mode of organic matter remineralization and source of ammonium (~45-100%) in the upper oxygen minimum zones, and reconcile hitherto observed mismatches between ammonium producing and consuming processes therein.

View Article: PubMed Central - PubMed

Affiliation: Biogeochemistry Department, Max Planck Institute for Marine Microbiology, Bremen, Germany.

ABSTRACT
Oxygen minimum zones are major sites of fixed nitrogen loss in the ocean. Recent studies have highlighted the importance of anaerobic ammonium oxidation, anammox, in pelagic nitrogen removal. Sources of ammonium for the anammox reaction, however, remain controversial, as heterotrophic denitrification and alternative anaerobic pathways of organic matter remineralization cannot account for the ammonium requirements of reported anammox rates. Here, we explore the significance of microaerobic respiration as a source of ammonium during organic matter degradation in the oxygen-deficient waters off Namibia and Peru. Experiments with additions of double-labelled oxygen revealed high aerobic activity in the upper OMZs, likely controlled by surface organic matter export. Consistently observed oxygen consumption in samples retrieved throughout the lower OMZs hints at efficient exploitation of vertically and laterally advected, oxygenated waters in this zone by aerobic microorganisms. In accordance, metagenomic and metatranscriptomic analyses identified genes encoding for aerobic terminal oxidases and demonstrated their expression by diverse microbial communities, even in virtually anoxic waters. Our results suggest that microaerobic respiration is a major mode of organic matter remineralization and source of ammonium (~45-100%) in the upper oxygen minimum zones, and reconcile hitherto observed mismatches between ammonium producing and consuming processes therein.

No MeSH data available.


Related in: MedlinePlus

Oxygen sensitivity of aerobic respiration and OMZ particle size distributions.(a) O2 sensitivity assays in the Namibian (station 225) and Peruvian OMZ (stations 13 and 28) during cruises M76 and M77-3, respectively. Oxygen consumption rates are given as percentages of the highest rate observed (= 100%) among all O2 treatments (see S2 Table for absolute rates). Error bars for O2 consumption rates are standard errors calculated from linear regression. Isolines (grey) indicate diffusion-limited respiration rates inside aggregates of 0.01–25 mm in diameter. A detailed description of how aggregate-size-dependent rates were calculated is included in the S1 File. (b) Vertical distribution of particle volumes (20 m bins) for six size classes between 0.06 and 5.32 mm (ESD) in the central Peruvian OMZ (12.62°S/77.55°W) during cruise M93. Color shading indicates diffusion limitation of aerobic respiration inside particles. For clarity, particles >5.32 mm are not depicted here. A more general overview of particle size distributions in the ETSP OMZ is given in S2 Fig.
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pone.0133526.g003: Oxygen sensitivity of aerobic respiration and OMZ particle size distributions.(a) O2 sensitivity assays in the Namibian (station 225) and Peruvian OMZ (stations 13 and 28) during cruises M76 and M77-3, respectively. Oxygen consumption rates are given as percentages of the highest rate observed (= 100%) among all O2 treatments (see S2 Table for absolute rates). Error bars for O2 consumption rates are standard errors calculated from linear regression. Isolines (grey) indicate diffusion-limited respiration rates inside aggregates of 0.01–25 mm in diameter. A detailed description of how aggregate-size-dependent rates were calculated is included in the S1 File. (b) Vertical distribution of particle volumes (20 m bins) for six size classes between 0.06 and 5.32 mm (ESD) in the central Peruvian OMZ (12.62°S/77.55°W) during cruise M93. Color shading indicates diffusion limitation of aerobic respiration inside particles. For clarity, particles >5.32 mm are not depicted here. A more general overview of particle size distributions in the ETSP OMZ is given in S2 Fig.

Mentions: At the upper OMZ boundaries, steep O2 gradients mark the transition from oxic to anoxic environments. Experiments simulating changing O2 concentrations (~0.5–20 μmol l-1) in this transition zone, revealed a near-linear decrease of O2 consumptions rates with decreasing levels of O2 in the Namibian and Peruvian OMZ (Fig 3a and S2 Table); a surprising result, given that Km values of aerobic respiratory oxidases are two to three orders of magnitude lower than ambient O2 concentrations in the incubations. Recent studies targeting aerobic NH3 and NO2- oxidation, showed both processes to be also mostly insensitive to decreasing O2 concentrations over the same range [14,24,25]. Assuming O2 consumption in our experiments to be largely coupled to heterotrophic activity, the apparent high O2 sensitivity observed here may result from O2 diffusion limitation of aggregate-associated organic matter respiration [29].


Aerobic Microbial Respiration In Oceanic Oxygen Minimum Zones.

Kalvelage T, Lavik G, Jensen MM, Revsbech NP, Löscher C, Schunck H, Desai DK, Hauss H, Kiko R, Holtappels M, LaRoche J, Schmitz RA, Graco MI, Kuypers MM - PLoS ONE (2015)

Oxygen sensitivity of aerobic respiration and OMZ particle size distributions.(a) O2 sensitivity assays in the Namibian (station 225) and Peruvian OMZ (stations 13 and 28) during cruises M76 and M77-3, respectively. Oxygen consumption rates are given as percentages of the highest rate observed (= 100%) among all O2 treatments (see S2 Table for absolute rates). Error bars for O2 consumption rates are standard errors calculated from linear regression. Isolines (grey) indicate diffusion-limited respiration rates inside aggregates of 0.01–25 mm in diameter. A detailed description of how aggregate-size-dependent rates were calculated is included in the S1 File. (b) Vertical distribution of particle volumes (20 m bins) for six size classes between 0.06 and 5.32 mm (ESD) in the central Peruvian OMZ (12.62°S/77.55°W) during cruise M93. Color shading indicates diffusion limitation of aerobic respiration inside particles. For clarity, particles >5.32 mm are not depicted here. A more general overview of particle size distributions in the ETSP OMZ is given in S2 Fig.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4507870&req=5

pone.0133526.g003: Oxygen sensitivity of aerobic respiration and OMZ particle size distributions.(a) O2 sensitivity assays in the Namibian (station 225) and Peruvian OMZ (stations 13 and 28) during cruises M76 and M77-3, respectively. Oxygen consumption rates are given as percentages of the highest rate observed (= 100%) among all O2 treatments (see S2 Table for absolute rates). Error bars for O2 consumption rates are standard errors calculated from linear regression. Isolines (grey) indicate diffusion-limited respiration rates inside aggregates of 0.01–25 mm in diameter. A detailed description of how aggregate-size-dependent rates were calculated is included in the S1 File. (b) Vertical distribution of particle volumes (20 m bins) for six size classes between 0.06 and 5.32 mm (ESD) in the central Peruvian OMZ (12.62°S/77.55°W) during cruise M93. Color shading indicates diffusion limitation of aerobic respiration inside particles. For clarity, particles >5.32 mm are not depicted here. A more general overview of particle size distributions in the ETSP OMZ is given in S2 Fig.
Mentions: At the upper OMZ boundaries, steep O2 gradients mark the transition from oxic to anoxic environments. Experiments simulating changing O2 concentrations (~0.5–20 μmol l-1) in this transition zone, revealed a near-linear decrease of O2 consumptions rates with decreasing levels of O2 in the Namibian and Peruvian OMZ (Fig 3a and S2 Table); a surprising result, given that Km values of aerobic respiratory oxidases are two to three orders of magnitude lower than ambient O2 concentrations in the incubations. Recent studies targeting aerobic NH3 and NO2- oxidation, showed both processes to be also mostly insensitive to decreasing O2 concentrations over the same range [14,24,25]. Assuming O2 consumption in our experiments to be largely coupled to heterotrophic activity, the apparent high O2 sensitivity observed here may result from O2 diffusion limitation of aggregate-associated organic matter respiration [29].

Bottom Line: Consistently observed oxygen consumption in samples retrieved throughout the lower OMZs hints at efficient exploitation of vertically and laterally advected, oxygenated waters in this zone by aerobic microorganisms.In accordance, metagenomic and metatranscriptomic analyses identified genes encoding for aerobic terminal oxidases and demonstrated their expression by diverse microbial communities, even in virtually anoxic waters.Our results suggest that microaerobic respiration is a major mode of organic matter remineralization and source of ammonium (~45-100%) in the upper oxygen minimum zones, and reconcile hitherto observed mismatches between ammonium producing and consuming processes therein.

View Article: PubMed Central - PubMed

Affiliation: Biogeochemistry Department, Max Planck Institute for Marine Microbiology, Bremen, Germany.

ABSTRACT
Oxygen minimum zones are major sites of fixed nitrogen loss in the ocean. Recent studies have highlighted the importance of anaerobic ammonium oxidation, anammox, in pelagic nitrogen removal. Sources of ammonium for the anammox reaction, however, remain controversial, as heterotrophic denitrification and alternative anaerobic pathways of organic matter remineralization cannot account for the ammonium requirements of reported anammox rates. Here, we explore the significance of microaerobic respiration as a source of ammonium during organic matter degradation in the oxygen-deficient waters off Namibia and Peru. Experiments with additions of double-labelled oxygen revealed high aerobic activity in the upper OMZs, likely controlled by surface organic matter export. Consistently observed oxygen consumption in samples retrieved throughout the lower OMZs hints at efficient exploitation of vertically and laterally advected, oxygenated waters in this zone by aerobic microorganisms. In accordance, metagenomic and metatranscriptomic analyses identified genes encoding for aerobic terminal oxidases and demonstrated their expression by diverse microbial communities, even in virtually anoxic waters. Our results suggest that microaerobic respiration is a major mode of organic matter remineralization and source of ammonium (~45-100%) in the upper oxygen minimum zones, and reconcile hitherto observed mismatches between ammonium producing and consuming processes therein.

No MeSH data available.


Related in: MedlinePlus