Nitrogen losses in anoxic marine sediments driven by Thioploca–anammox bacterial consortia

Maria G. Prokopenko, Marissa B. Hirst, Loreto De Brabandere, Daniel J. Lawrence, William L. Berelson, Julie Granger, Bonnie X. Chang, Scott Dawson, Edward J. Crane III, Laurie Chong, Bo Thamdrup, Amy Townsend-Small, Daniel L. Sigman

Publikation: Bidrag til tidsskriftLetterForskningpeer review

Resumé

Ninety per cent of marine organic matter burial occurs in continental margin sediments, where a substantial fraction of organic carbon escapes oxidation and enters long-term geologic storage within sedimentary rocks. In such environments, microbial metabolism is limited by the diffusive supply of electron acceptors. One strategy to optimize energy yields in a resource-limited habitat is symbiotic metabolite exchange among microbial associations. Thermodynamic and geochemical considerations indicate that microbial co-metabolisms are likely to play a critical part in sedimentary organic carbon cycling. Yet only one association, between methanotrophic archaea and sulphate-reducing bacteria, has been demonstrated in marine sediments in situ, and little is known of the role of microbial symbiotic interactions in other sedimentary biogeochemical cycles. Here we report in situ molecular and incubation-based evidence for a novel symbiotic consortium between two chemolithotrophic bacteria - anaerobic ammonium-oxidizing (anammox) bacteria and the nitrate-sequestering sulphur-oxidizing Thioploca species - in anoxic sediments of the Soledad basin at the Mexican Pacific margin. A mass balance of benthic solute fluxes and the corresponding nitrogen isotope composition of nitrate and ammonium fluxes indicate that anammox bacteria rely on Thioploca species for the supply of metabolic substrates and account for about 57 ± 21 per cent of the total benthic N 2 production. We show that Thioploca-anammox symbiosis intensifies benthic fixed nitrogen losses in anoxic sediments, bypassing diffusion-imposed limitations by efficiently coupling the carbon, nitrogen and sulphur cycles.

OriginalsprogEngelsk
TidsskriftNature
Vol/bind500
Sider (fra-til)194-198
ISSN0028-0836
DOI
StatusUdgivet - 2013

Fingeraftryk

anoxic sediment
marine sediment
ammonium
nitrogen
bacterium
metabolism
organic carbon
nitrate
sulfur cycle
nitrogen cycle
biogeochemical cycle
sulfate-reducing bacterium
nitrogen isotope
symbiosis
carbon cycle
continental margin
sedimentary rock
solute
mass balance
metabolite

Citer dette

Prokopenko, M. G., Hirst, M. B., De Brabandere, L., Lawrence, D. J., Berelson, W. L., Granger, J., ... Sigman, D. L. (2013). Nitrogen losses in anoxic marine sediments driven by Thioploca–anammox bacterial consortia. Nature, 500, 194-198. https://doi.org/10.1038/nature12365
Prokopenko, Maria G. ; Hirst, Marissa B. ; De Brabandere, Loreto ; Lawrence, Daniel J. ; Berelson, William L. ; Granger, Julie ; Chang, Bonnie X. ; Dawson, Scott ; Crane III, Edward J. ; Chong, Laurie ; Thamdrup, Bo ; Townsend-Small, Amy ; Sigman, Daniel L. / Nitrogen losses in anoxic marine sediments driven by Thioploca–anammox bacterial consortia. I: Nature. 2013 ; Bind 500. s. 194-198.
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abstract = "Ninety per cent of marine organic matter burial occurs in continental margin sediments, where a substantial fraction of organic carbon escapes oxidation and enters long-term geologic storage within sedimentary rocks. In such environments, microbial metabolism is limited by the diffusive supply of electron acceptors. One strategy to optimize energy yields in a resource-limited habitat is symbiotic metabolite exchange among microbial associations. Thermodynamic and geochemical considerations indicate that microbial co-metabolisms are likely to play a critical part in sedimentary organic carbon cycling. Yet only one association, between methanotrophic archaea and sulphate-reducing bacteria, has been demonstrated in marine sediments in situ, and little is known of the role of microbial symbiotic interactions in other sedimentary biogeochemical cycles. Here we report in situ molecular and incubation-based evidence for a novel symbiotic consortium between two chemolithotrophic bacteria - anaerobic ammonium-oxidizing (anammox) bacteria and the nitrate-sequestering sulphur-oxidizing Thioploca species - in anoxic sediments of the Soledad basin at the Mexican Pacific margin. A mass balance of benthic solute fluxes and the corresponding nitrogen isotope composition of nitrate and ammonium fluxes indicate that anammox bacteria rely on Thioploca species for the supply of metabolic substrates and account for about 57 ± 21 per cent of the total benthic N 2 production. We show that Thioploca-anammox symbiosis intensifies benthic fixed nitrogen losses in anoxic sediments, bypassing diffusion-imposed limitations by efficiently coupling the carbon, nitrogen and sulphur cycles.",
author = "Prokopenko, {Maria G.} and Hirst, {Marissa B.} and {De Brabandere}, Loreto and Lawrence, {Daniel J.} and Berelson, {William L.} and Julie Granger and Chang, {Bonnie X.} and Scott Dawson and {Crane III}, {Edward J.} and Laurie Chong and Bo Thamdrup and Amy Townsend-Small and Sigman, {Daniel L.}",
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Prokopenko, MG, Hirst, MB, De Brabandere, L, Lawrence, DJ, Berelson, WL, Granger, J, Chang, BX, Dawson, S, Crane III, EJ, Chong, L, Thamdrup, B, Townsend-Small, A & Sigman, DL 2013, 'Nitrogen losses in anoxic marine sediments driven by Thioploca–anammox bacterial consortia', Nature, bind 500, s. 194-198. https://doi.org/10.1038/nature12365

Nitrogen losses in anoxic marine sediments driven by Thioploca–anammox bacterial consortia. / Prokopenko, Maria G.; Hirst, Marissa B.; De Brabandere, Loreto; Lawrence, Daniel J.; Berelson, William L.; Granger, Julie; Chang, Bonnie X.; Dawson, Scott; Crane III, Edward J.; Chong, Laurie; Thamdrup, Bo; Townsend-Small, Amy; Sigman, Daniel L.

I: Nature, Bind 500, 2013, s. 194-198.

Publikation: Bidrag til tidsskriftLetterForskningpeer review

TY - JOUR

T1 - Nitrogen losses in anoxic marine sediments driven by Thioploca–anammox bacterial consortia

AU - Prokopenko, Maria G.

AU - Hirst, Marissa B.

AU - De Brabandere, Loreto

AU - Lawrence, Daniel J.

AU - Berelson, William L.

AU - Granger, Julie

AU - Chang, Bonnie X.

AU - Dawson, Scott

AU - Crane III, Edward J.

AU - Chong, Laurie

AU - Thamdrup, Bo

AU - Townsend-Small, Amy

AU - Sigman, Daniel L.

PY - 2013

Y1 - 2013

N2 - Ninety per cent of marine organic matter burial occurs in continental margin sediments, where a substantial fraction of organic carbon escapes oxidation and enters long-term geologic storage within sedimentary rocks. In such environments, microbial metabolism is limited by the diffusive supply of electron acceptors. One strategy to optimize energy yields in a resource-limited habitat is symbiotic metabolite exchange among microbial associations. Thermodynamic and geochemical considerations indicate that microbial co-metabolisms are likely to play a critical part in sedimentary organic carbon cycling. Yet only one association, between methanotrophic archaea and sulphate-reducing bacteria, has been demonstrated in marine sediments in situ, and little is known of the role of microbial symbiotic interactions in other sedimentary biogeochemical cycles. Here we report in situ molecular and incubation-based evidence for a novel symbiotic consortium between two chemolithotrophic bacteria - anaerobic ammonium-oxidizing (anammox) bacteria and the nitrate-sequestering sulphur-oxidizing Thioploca species - in anoxic sediments of the Soledad basin at the Mexican Pacific margin. A mass balance of benthic solute fluxes and the corresponding nitrogen isotope composition of nitrate and ammonium fluxes indicate that anammox bacteria rely on Thioploca species for the supply of metabolic substrates and account for about 57 ± 21 per cent of the total benthic N 2 production. We show that Thioploca-anammox symbiosis intensifies benthic fixed nitrogen losses in anoxic sediments, bypassing diffusion-imposed limitations by efficiently coupling the carbon, nitrogen and sulphur cycles.

AB - Ninety per cent of marine organic matter burial occurs in continental margin sediments, where a substantial fraction of organic carbon escapes oxidation and enters long-term geologic storage within sedimentary rocks. In such environments, microbial metabolism is limited by the diffusive supply of electron acceptors. One strategy to optimize energy yields in a resource-limited habitat is symbiotic metabolite exchange among microbial associations. Thermodynamic and geochemical considerations indicate that microbial co-metabolisms are likely to play a critical part in sedimentary organic carbon cycling. Yet only one association, between methanotrophic archaea and sulphate-reducing bacteria, has been demonstrated in marine sediments in situ, and little is known of the role of microbial symbiotic interactions in other sedimentary biogeochemical cycles. Here we report in situ molecular and incubation-based evidence for a novel symbiotic consortium between two chemolithotrophic bacteria - anaerobic ammonium-oxidizing (anammox) bacteria and the nitrate-sequestering sulphur-oxidizing Thioploca species - in anoxic sediments of the Soledad basin at the Mexican Pacific margin. A mass balance of benthic solute fluxes and the corresponding nitrogen isotope composition of nitrate and ammonium fluxes indicate that anammox bacteria rely on Thioploca species for the supply of metabolic substrates and account for about 57 ± 21 per cent of the total benthic N 2 production. We show that Thioploca-anammox symbiosis intensifies benthic fixed nitrogen losses in anoxic sediments, bypassing diffusion-imposed limitations by efficiently coupling the carbon, nitrogen and sulphur cycles.

U2 - 10.1038/nature12365

DO - 10.1038/nature12365

M3 - Letter

VL - 500

SP - 194

EP - 198

JO - Nature

JF - Nature

SN - 0028-0836

ER -

Prokopenko MG, Hirst MB, De Brabandere L, Lawrence DJ, Berelson WL, Granger J et al. Nitrogen losses in anoxic marine sediments driven by Thioploca–anammox bacterial consortia. Nature. 2013;500:194-198. https://doi.org/10.1038/nature12365