Widespread nitrogen fixation in sediments from diverse deep‐sea sites of elevated carbon loading

Dekas, Anne E.; Fike, David A.; Chadwick, Grayson L.; Green‐Saxena, Abigail; Fortney, Julian; Connon, Stephanie A.; Dawson, Katherine S.; Orphan, Victoria J.

doi:10.1111/1462-2920.14342

Title: Widespread nitrogen fixation in sediments from diverse deep‐sea sites of elevated carbon loading

Journal Article · 25 July 2018 · Environmental Microbiology

DOI: https://doi.org/10.1111/1462-2920.14342 · OSTI ID:1461897

^[1]; Fike, David A. ^[2]; Chadwick, Grayson L. ^[3]; Green‐Saxena, Abigail ^[3]; Fortney, Julian ^[4]; Connon, Stephanie A. ^[3]; Dawson, Katherine S. ^[3]; Orphan, Victoria J. ^[3]

Department of Earth System Science Stanford University Stanford CA 94305 USA, Division of Geological and Planetary Sciences California Institute of Technology Pasadena CA 91125 USA
Department of Earth &, Planetary Sciences Washington University in St. Louis St. Louis MO 63130 USA
Division of Geological and Planetary Sciences California Institute of Technology Pasadena CA 91125 USA
Department of Earth System Science Stanford University Stanford CA 94305 USA

Summary Nitrogen fixation, the biological conversion of N ₂ to NH ₃ , is critical to alleviating nitrogen limitation in many marine ecosystems. To date, few measurements exist of N ₂ fixation in deep‐sea sediments. Here, we conducted > 400 bottle incubations with sediments from methane seeps, whale falls and background sites off the western coast of the United States from 600 to 2893 m water depth to investigate the potential rates, spatial distribution and biological mediators of benthic N ₂ fixation. We found that N ₂ fixation was widespread, yet heterogeneously distributed with sediment depth at all sites. In some locations, rates exceeded previous measurements by > 10×, and provided up to 30% of the community anabolic growth requirement for nitrogen. Diazotrophic activity appeared to be inhibited by pore water ammonium: N ₂ fixation was only observed if incubation ammonium concentrations were ≤ 25 μM, and experimental additions of ammonium reduced diazotrophy. In seep sediments, N ₂ fixation was dependent on CH ₄ and coincident with sulphate reduction, consistent with previous work showing diazotrophy by microorganisms mediating sulphate‐coupled methane oxidation. However, the pattern of diazotrophy was different in whale‐fall and associated reference sediments, where it was largely unaffected by CH ₄ , suggesting catabolically different diazotrophs at these sites.

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Sponsoring Organization:: USDOE

Grant/Contract Number:: SC0003940; SC0004949

OSTI ID:: 1461897

Journal Information:: Environmental Microbiology, Journal Name: Environmental Microbiology Journal Issue: 12 Vol. 20; ISSN 1462-2912

Publisher:: Wiley-BlackwellCopyright Statement

Country of Publication:: United Kingdom

Language:: English

References (57)

Net Sediment N2 Fluxes in a Coastal Marine System—Experimental Manipulations and a Conceptual Model Fulweiler, Robinson W.; Nixon, Scott W.; Buckley, Betty A. Ecosystems, Vol. 11, Issue 7 https://doi.org/10.1007/s10021-008-9187-3	journal	September 2008
Nitrogen fixation in Atlantic deep-sea and coastal sediments Hartwig, Eric O.; Stanley, Simon O. Deep Sea Research, Vol. 25, Issue 4 https://doi.org/10.1016/0146-6291(78)90567-2	journal	April 1978
Fluid and chemical fluxes in and out of sediments hosting methane hydrate deposits on Hydrate Ridge, OR, I: Hydrological provinces Torres, M. E.; McManus, J.; Hammond, D. E. Earth and Planetary Science Letters, Vol. 201, Issue 3-4 https://doi.org/10.1016/S0012-821X(02)00733-1	journal	August 2002
Gas hydrate destabilization: enhanced dewatering, benthic material turnover and large methane plumes at the Cascadia convergent margin Suess, E.; Torres, M. E.; Bohrmann, G. Earth and Planetary Science Letters, Vol. 170, Issue 1-2 https://doi.org/10.1016/S0012-821X(99)00092-8	journal	June 1999
Biologic and geologic characteristics of cold seeps in Monterey Bay, California Barry, James P.; Gary Greene, H.; Orange, Daniel L. Deep Sea Research Part I: Oceanographic Research Papers, Vol. 43, Issue 11-12 https://doi.org/10.1016/S0967-0637(96)00075-1	journal	November 1996
Geological, geochemical, and microbiological heterogeneity of the seafloor around methane vents in the Eel River Basin, offshore California Orphan, V. J.; Ussler, W.; Naehr, T. H. Chemical Geology, Vol. 205, Issue 3-4 https://doi.org/10.1016/j.chemgeo.2003.12.035	journal	May 2004
A study of the chemistry of pore fluids and authigenic carbonates in methane seep environments: Kodiak Trench, Hydrate Ridge, Monterey Bay, and Eel River Basin Gieskes, Joris; Mahn, Chris; Day, Shelley Chemical Geology, Vol. 220, Issue 3-4 https://doi.org/10.1016/j.chemgeo.2005.04.002	journal	August 2005
Unusual benthic fauna associated with a whale fall in Monterey Canyon, California Goffredi, Shana K.; Paull, Charles K.; Fulton-Bennett, Kim Deep Sea Research Part I: Oceanographic Research Papers, Vol. 51, Issue 10 https://doi.org/10.1016/j.dsr.2004.05.009	journal	October 2004
Bathymetric and temporal variation among Osedax boneworms and associated megafauna on whale-falls in Monterey Bay, California Braby, Caren E.; Rouse, Greg W.; Johnson, Shannon B. Deep Sea Research Part I: Oceanographic Research Papers, Vol. 54, Issue 10 https://doi.org/10.1016/j.dsr.2007.05.014	journal	October 2007
Time-series analysis of six whale-fall communities in Monterey Canyon, California, USA Lundsten, Lonny; Schlining, Kyra L.; Frasier, Kaitlin Deep Sea Research Part I: Oceanographic Research Papers, Vol. 57, Issue 12 https://doi.org/10.1016/j.dsr.2010.09.003	journal	December 2010
15N2–DNA–stable isotope probing of diazotrophic methanotrophs in soil Buckley, Daniel H.; Huangyutitham, Varisa; Hsu, Shi-Fang Soil Biology and Biochemistry, Vol. 40, Issue 6 https://doi.org/10.1016/j.soilbio.2007.05.006	journal	June 2008
Sensitive Measurement of NH ₄ ⁺ ¹⁵ N/ ¹⁴ N (δ ¹⁵ NH ₄ ⁺ ) at Natural Abundance Levels in Fresh and Saltwaters Zhang, Lin; Altabet, Mark A.; Wu, Taixing Analytical Chemistry, Vol. 79, Issue 14 https://doi.org/10.1021/ac070106d	journal	July 2007
New Developments in the Marine Nitrogen Cycle Brandes, Jay A.; Devol, Allan H.; Deutsch, Curtis Chemical Reviews, Vol. 107, Issue 2 https://doi.org/10.1021/cr050377t	journal	February 2007
A global marine-fixed nitrogen isotopic budget: Implications for Holocene nitrogen cycling: NITROGEN ISOTOPIC BUDGET Brandes, Jay A.; Devol, Allan H. Global Biogeochemical Cycles, Vol. 16, Issue 4 https://doi.org/10.1029/2001GB001856	journal	December 2002
Temporal evolution of methane cycling and phylogenetic diversity of archaea in sediments from a deep-sea whale-fall in Monterey Canyon, California Goffredi, Shana K.; Wilpiszeski, Regina; Lee, Ray The ISME Journal, Vol. 2, Issue 2 https://doi.org/10.1038/ismej.2007.103	journal	January 2008
Activity and interactions of methane seep microorganisms assessed by parallel transcription and FISH-NanoSIMS analyses Dekas, Anne E.; Connon, Stephanie A.; Chadwick, Grayson L. The ISME Journal, Vol. 10, Issue 3 https://doi.org/10.1038/ismej.2015.145	journal	September 2015
Spatial coupling of nitrogen inputs and losses in the ocean Deutsch, Curtis; Sarmiento, Jorge L.; Sigman, Daniel M. Nature, Vol. 445, Issue 7124 https://doi.org/10.1038/nature05392	journal	January 2007
Reversal of the net dinitrogen gas flux in coastal marine sediments Fulweiler, R. W.; Nixon, S. W.; Buckley, B. A. Nature, Vol. 448, Issue 7150 https://doi.org/10.1038/nature05963	journal	July 2007
An Earth-system perspective of the global nitrogen cycle Gruber, Nicolas; Galloway, James N. Nature, Vol. 451, Issue 7176 https://doi.org/10.1038/nature06592	journal	January 2008
Doubling of marine dinitrogen-fixation rates based on direct measurements Großkopf, Tobias; Mohr, Wiebke; Baustian, Tina Nature, Vol. 488, Issue 7411 https://doi.org/10.1038/nature11338	journal	August 2012
Global rates of water-column denitrification derived from nitrogen gas measurements DeVries, Tim; Deutsch, Curtis; Primeau, François Nature Geoscience, Vol. 5, Issue 8 https://doi.org/10.1038/ngeo1515	journal	July 2012
Feast and famine — microbial life in the deep-sea bed Jørgensen, Bo Barker; Boetius, Antje Nature Reviews Microbiology, Vol. 5, Issue 10 https://doi.org/10.1038/nrmicro1745	journal	October 2007
Emerging patterns of marine nitrogen fixation Sohm, Jill A.; Webb, Eric A.; Capone, Douglas G. Nature Reviews Microbiology, Vol. 9, Issue 7 https://doi.org/10.1038/nrmicro2594	journal	June 2011
In vitro demonstration of anaerobic oxidation of methane coupled to sulphate reduction in sediment from a marine gas hydrate area Nauhaus, Katja; Boetius, Antje; Kruger, Martin Environmental Microbiology, Vol. 4, Issue 5 https://doi.org/10.1046/j.1462-2920.2002.00299.x	journal	May 2002
Nitrogen Cycling of Active Bacteria within Oligotrophic Sediment of the Mid-Atlantic Ridge Flank Reese, Brandi Kiel; Zinke, Laura A.; Sobol, Morgan S. Geomicrobiology Journal, Vol. 35, Issue 6 https://doi.org/10.1080/01490451.2017.1392649	journal	February 2018
Genetics of Nitrogen Regulation in Methanococcus maripaludis Kessler, Peter S.; Leigh, John A. Genetics, Vol. 152, Issue 4 https://doi.org/10.1093/genetics/152.4.1343	journal	August 1999
The Natural History of Nitrogen Fixation Raymond, Jason; Siefert, Janet L.; Staples, Christopher R. Molecular Biology and Evolution, Vol. 21, Issue 3 https://doi.org/10.1093/molbev/msh047	journal	March 2004
Spatial distribution of nitrogen fixation in methane seep sediment and the role of the ANME archaea: Nitrogen fixation in methane seep sediment Dekas, Anne E.; Chadwick, Grayson L.; Bowles, Marshall W. Environmental Microbiology, Vol. 16, Issue 10 https://doi.org/10.1111/1462-2920.12247	journal	September 2013
Application of stable-isotope labelling techniques for the detection of active diazotrophs: Detecting diazotrophs with stable-isotope techniques Angel, Roey; Panhölzl, Christopher; Gabriel, Raphael Environmental Microbiology, Vol. 20, Issue 1 https://doi.org/10.1111/1462-2920.13954	journal	December 2017
Bacterial community shifts in taxa and diversity in response to localized organic loading in the deep sea Goffredi, Shana K.; Orphan, Victoria J. Environmental Microbiology, Vol. 12, Issue 2 https://doi.org/10.1111/j.1462-2920.2009.02072.x	journal	February 2010
Metagenome and mRNA expression analyses of anaerobic methanotrophic archaea of the ANME-1 group Meyerdierks, Anke; Kube, Michael; Kostadinov, Ivaylo Environmental Microbiology, Vol. 12, Issue 2 https://doi.org/10.1111/j.1462-2920.2009.02083.x	journal	February 2010
Nitrogen Fixation at 92 C by a Hydrothermal Vent Archaeon Mehta, M. P.; Baross, J. A. Science, Vol. 314, Issue 5806 https://doi.org/10.1126/science.1134772	journal	December 2006
Deep-Sea Archaea Fix and Share Nitrogen in Methane-Consuming Microbial Consortia Dekas, A. E.; Poretsky, R. S.; Orphan, V. J. Science, Vol. 326, Issue 5951 https://doi.org/10.1126/science.1178223	journal	October 2009
Molecular Characterization of Potential Nitrogen Fixation by Anaerobic Methane-Oxidizing Archaea in the Methane Seep Sediments at the Number 8 Kumano Knoll in the Kumano Basin, Offshore of Japan Miyazaki, J.; Higa, R.; Toki, T. Applied and Environmental Microbiology, Vol. 75, Issue 22 https://doi.org/10.1128/AEM.01184-09	journal	September 2009
Environment-Dependent Distribution of the Sediment nifH -Harboring Microbiota in the Northern South China Sea Dang, Hongyue; Yang, Jinying; Li, Jing Applied and Environmental Microbiology, Vol. 79, Issue 1 https://doi.org/10.1128/AEM.01889-12	journal	October 2012
Diverse and Novel nifH and nifH-Like Gene Sequences in the Deep-Sea Methane Seep Sediments of the Okhotsk Sea Dang, H.; Luan, X.; Zhao, J. Applied and Environmental Microbiology, Vol. 75, Issue 7 https://doi.org/10.1128/AEM.02556-08	journal	January 2009
A Simple, High-Precision, High-Sensitivity Tracer Assay for N(inf2) Fixation. Montoya, J. P.; Voss, M.; Kahler, P. Applied and environmental microbiology, Vol. 62, Issue 3 https://doi.org/10.1128/AEM.62.3.986-993.1996	journal	January 1996
Phylogenetic Diversity of Nitrogenase (nifH) Genes in Deep-Sea and Hydrothermal Vent Environments of the Juan de Fuca Ridge Mehta, M. P.; Butterfield, D. A.; Baross, J. A. Applied and Environmental Microbiology, Vol. 69, Issue 2 https://doi.org/10.1128/AEM.69.2.960-970.2003	journal	February 2003
Growth and Methane Oxidation Rates of Anaerobic Methanotrophic Archaea in a Continuous-Flow Bioreactor Girguis, P. R.; Orphan, V. J.; Hallam, S. J. Applied and Environmental Microbiology, Vol. 69, Issue 9 https://doi.org/10.1128/AEM.69.9.5472-5482.2003	journal	September 2003
Ammonia Switch-Off of Nitrogen Fixation in the Methanogenic Archaeon Methanococcus maripaludis: Mechanistic Features and Requirement for the Novel GlnB Homologues, NifI1 and NifI2 Kessler, P. S.; Daniel, C.; Leigh, J. A. Journal of Bacteriology, Vol. 183, Issue 3 https://doi.org/10.1128/JB.183.3.882-889.2001	journal	February 2001
Inhibition of Methanogenesis in Marine Sediments by Acetylene and Ethylene: Validity of the Acetylene Reduction Assay for Anaerobic Microcosms Oremland, Ronald S.; Taylor, Barrie F. Applied Microbiology, Vol. 30, Issue 4 https://doi.org/10.1128/am.30.4.707-709.1975	journal	January 1975
The Contamination of Commercial 15N2 Gas Stocks with 15N–Labeled Nitrate and Ammonium and Consequences for Nitrogen Fixation Measurements Dabundo, Richard; Lehmann, Moritz F.; Treibergs, Lija PLoS ONE, Vol. 9, Issue 10 https://doi.org/10.1371/journal.pone.0110335	journal	October 2014
Acid fumigation of soils to remove carbonates prior to total organic carbon or CARBON-13 isotopic analysis Harris, David; Horwáth, William R.; van Kessel, Chris Soil Science Society of America Journal, Vol. 65, Issue 6 https://doi.org/10.2136/sssaj2001.1853	journal	January 2001
The conundrum of marine N2 fixation Mahaffey, C. American Journal of Science, Vol. 305, Issue 6-8 https://doi.org/10.2475/ajs.305.6-8.546	journal	June 2005
Biogeochemistry of a deep-sea whale fall: sulfate reduction, sulfide efflux and methanogenesis Treude, T.; Smith, Cr; Wenzhöfer, F. Marine Ecology Progress Series, Vol. 382 https://doi.org/10.3354/meps07972	journal	April 2009
Burrowing deeper into benthic nitrogen cycling: the impact of bioturbation on nitrogen fixation coupled to sulfate reduction Bertics, Vj; Sohm, Ja; Treude, T. Marine Ecology Progress Series, Vol. 409 https://doi.org/10.3354/meps08639	journal	June 2010
Evidence and a conceptual model for the co‑occurrence of nitrogen fixation and denitrification in heterotrophic marine sediments Fulweiler, Rw; Brown, Sm; Nixon, Sw Marine Ecology Progress Series, Vol. 482 https://doi.org/10.3354/meps10240	journal	May 2013
Anaerobic oxidation of methane above gas hydrates at Hydrate Ridge, NE Pacific Ocean Treude, T.; Boetius, A.; Knittel, K. Marine Ecology Progress Series, Vol. 264 https://doi.org/10.3354/meps264001	journal	January 2003
Benthic Dinitrogen Fixation Traversing the Oxygen Minimum Zone Off Mauritania (NW Africa) Gier, Jessica; Löscher, Carolin R.; Dale, Andrew W. Frontiers in Marine Science, Vol. 4 https://doi.org/10.3389/fmars.2017.00390	journal	December 2017
The sensitivity of marine N2 fixation to dissolved inorganic nitrogen Knapp, Angela N. Frontiers in Microbiology, Vol. 3 https://doi.org/10.3389/fmicb.2012.00374	journal	January 2012
Examining the impact of acetylene on N-fixation and the active sediment microbial community Fulweiler, Robinson W.; Heiss, Elise M.; Rogener, Mary Kate Frontiers in Microbiology, Vol. 6 https://doi.org/10.3389/fmicb.2015.00418	journal	May 2015
Spectrophotometric Determination Of Hydrogen Sulfide In Natural Waters Cline, Joel D. Limnology and Oceanography, Vol. 14, Issue 3, p. 454-458 https://doi.org/10.4319/lo.1969.14.3.0454	journal	May 1969
Occurrence of benthic microbial nitrogen fixation coupled to sulfate reduction in the seasonally hypoxic Eckernförde Bay, Baltic Sea Bertics, V. J.; Löscher, C. R.; Salonen, I. Biogeosciences, Vol. 10, Issue 3 https://doi.org/10.5194/bg-10-1243-2013	journal	January 2013
Nitrogen cycling in the deep sedimentary biosphere: nitrate isotopes in porewaters underlying the oligotrophic North Atlantic Wankel, S. D.; Buchwald, C.; Ziebis, W. Biogeosciences, Vol. 12, Issue 24 https://doi.org/10.5194/bg-12-7483-2015	journal	January 2015
Nitrogen fixation in sediments along a depth transect through the Peruvian oxygen minimum zone Gier, Jessica; Sommer, Stefan; Löscher, Carolin R. Biogeosciences, Vol. 13, Issue 14 https://doi.org/10.5194/bg-13-4065-2016	journal	January 2016
An oceanic fixed nitrogen sink exceeding 400 Tg N a⁻¹ vs the concept of homeostasis in the fixed-nitrogen inventory Codispoti, L. A. Biogeosciences, Vol. 4, Issue 2 https://doi.org/10.5194/bg-4-233-2007	journal	January 2007
Constraints on oceanic N balance/imbalance from sedimentary ¹⁵N records Altabet, M. A. Biogeosciences, Vol. 4, Issue 1 https://doi.org/10.5194/bg-4-75-2007	journal	January 2007

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