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

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 associations1,2. Thermodynamic and geochemical considerations indicate that microbial co-metabolisms are likely to play a critical part in sedimentary organic carbon cycling3,4,5. Yet only one association, between methanotrophic archaea and sulphate-reducing bacteria, has been demonstrated in marine sediments in situ6,7, and little is known of the role of microbial symbiotic interactions in other sedimentary biogeochemical cycles8. 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 N2 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.

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Figure 1: Location and geochemistry of the Soledad basin sediments.
Figure 2: Anammox bacteria found in close spatial association with Thioploca sheaths collected in the sediments of Soledad basin.
Figure 3: N cycling by the Thioploca–anammox consortium and associated changes in δ15N of nitrate and ammonium.
Figure 4: Relationship between benthic Nloss/Coxid ratio and bottom-water [O2].

Accession codes

Accessions

GenBank/EMBL/DDBJ

Data deposits

Hzo-gene and partial 16S rRNA gene sequences have been submitted to GenBank (accession numbers JQ234655 to JQ234672 and JX945900 to JX945903, JX945905, JX945907 to JX945908, JX945910, JX945913, JX945915, JX945917 to JX945919, JX945921 to JX945928, JX945930 and JX945932 to JX945963).

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Acknowledgements

This work was supported by NSF OCE grant number OCE-0727123 to W.M.B. and D.M.S. We thank the captain and crew of the RV New Horizon, as well as the members of the at-sea and shore-based science party, N. Rollins, T. Riedel, S. Loyd and H. Grøn Jensen for their assistance during the cruise. We thank P. Rafter for δ15N measurements of bottom water NO3. We thank M. Schmid and G. Kuenen for discussions. We are grateful to D. Valentine for suggestions that improved the manuscript.

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M.G.P. and M.B.H. contributed equally to this work. M.G.P., M.B.H., L.D.B., W.M.B., L.C. and A.T.-S. conducted the field work; L.D.B. and B.T. performed sediment slurry incubation for anammox activity. M.G.P., L.C., B.X.C., J.G. and D.M.S. performed geochemical/isotopic analyses. M.B.H. and S.D. ran FISH experiments and analysis of anammox DNA. D.J.P.L. and E.J.C. conducted phylogenetic analysis of Thioploca and anammox DNA. M.G.P. designed the study and developed the isotope box model. M.G.P., M.B.H. and L.D.B. wrote the paper. W.M.B. and D.M.S. supervised the project.

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Correspondence to M. G. Prokopenko.

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Prokopenko, M., Hirst, M., De Brabandere, L. et al. Nitrogen losses in anoxic marine sediments driven by Thioploca–anammox bacterial consortia. Nature 500, 194–198 (2013). https://doi.org/10.1038/nature12365

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