Anammox bacteria drive fixed nitrogen loss in hadal trench sediments

Bo Thamdrup*, Clemens Schauberger, Morten Larsen, Blandine Trouche, Lois Maignien, Sophie Arnaud-Haond, Frank Wenzhöfer, Ronnie N. Glud

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Abstract

Benthic N2 production by microbial denitrification and anammox is the largest sink for fixed nitrogen in the oceans. Most N2 production occurs on the continental shelves, where a high flux of reactive organic matter fuels the depletion of nitrate close to the sediment surface. By contrast, N2 production rates in abyssal sediments are low due to low inputs of reactive organics, and nitrogen transformations are dominated by aerobic nitrification and the release of nitrate to the bottom water. Here, we demonstrate that this trend is reversed in the deepest parts of the oceans, the hadal trenches, where focusing of reactive organic matter enhances benthic microbial activity. Thus, at ∼8-km depth in the Atacama Trench, underlying productive surface waters, nitrate is depleted within a few centimeters of the sediment surface, N2 production rates reach those reported from some continental margin sites, and fixed nitrogen loss is mainly conveyed by anammox bacteria. These bacteria are closely related to those known from shallow oxygen minimum zone waters, and comparison of activities measured in the laboratory and in situ suggest they are piezotolerant. Even the Kermadec Trench, underlying oligotrophic surface waters, exhibits substantial fixed N removal. Our results underline the role of hadal sediments as hot spots of deep-sea biological activity, revealing a fully functional benthic nitrogen cycle at high hydrostatic pressure and pointing to hadal sediments as a previously unexplored niche for anaerobic microbial ecology and diagenesis.

OriginalsprogEngelsk
Artikelnummere2104529118
TidsskriftPNAS
Vol/bind118
Udgave nummer46
Antal sider7
ISSN0027-8424
DOI
StatusUdgivet - 16. nov. 2021

Bibliografisk note

Funding Information:
ACKNOWLEDGMENTS. We thank the masters, crews, and scientific parties of RV Tangaroa (TAN1711; ship time partly funded by Coasts and Oceans Centre of New Zealand’s National Institute of Water and Atmospheric Research, awarded to Ashley A. Rowden and R.N.G.) and RV Sonne (SO261; ship time provided by Federal Ministry of Education and Research, Germany, awarded to F.W., Mathias Zabel, and R.N.G.) for help with sampling. We thank Anni Glud, Lene A. Jakobsen, Heidi Grøn Jensen, Erik Laursen, and Louise R. Hansen for help with analyses, Johannes Lemburg for the construction of the Sediment-Lander, and Laura-Maria Bayer from the Vienna Bio-Center Core Facilities for PacBio amplicon sequencing. Laura A. Bristow provided valuable comments on the manuscript. Financial support for the study was provided by European Research Council (ERC) Advanced Grant HADES No. 669947, by the Danish National Research Foundation through the Danish Center for Hadal Research, HADAL (No. DNRF145) awarded to R.N.G., and by ERC Advanced Grant NOVAMOX No. 695599 awarded to B. Thamdrup. RNA amplicon sequencing and analysis was carried out under the eDNAbyss (AP2016-228) Project funded by France Génomique (ANR-10-INBS-09) and Genoscope under the supervision of Julie Poulain and Patrick Wincker.

Publisher Copyright:
© 2021 National Academy of Sciences. All rights reserved.

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