Abstract
Bacteria of the NC10 phylum link anaerobic methane oxidation to nitrite denitrification through a unique O2-producing intra-aerobic methanotrophy pathway. A niche for NC10 in the pelagic ocean has not been confirmed. We show that NC10 bacteria are present and transcriptionally active in oceanic oxygen minimum zones (OMZs) off northern Mexico and Costa Rica. NC10 16S rRNA genes were detected at all sites, peaking in abundance in the anoxic zone with elevated nitrite and methane concentrations. Phylogenetic analysis of particulate methane monooxygenase genes further confirmed the presence of NC10. rRNA and mRNA transcripts assignable to NC10 peaked within the OMZ and included genes of the putative nitrite-dependent intra-aerobic pathway, with high representation of transcripts containing the unique motif structure of the nitric oxide (NO) reductase of NC10 bacteria, hypothesized to participate in O2-producing NO dismutation. These findings confirm pelagic OMZs as a niche for NC10, suggesting a role for this group in OMZ nitrogen, methane and oxygen cycling.
Similar content being viewed by others
Log in or create a free account to read this content
Gain free access to this article, as well as selected content from this journal and more on nature.com
or
References
Babbin AR, Keil RG, Devol AH, Ward BB . (2014). Organic matter stoichiometry, flux, and oxygen control nitrogen loss in the ocean. Science 344: 406–408.
Chen J, Jiang XW, Gu JD . (2015). Existence of novel phylotypes of nitrite-dependent anaerobic methane-oxidizing bacteria in surface and subsurface sediments of the South China Sea. Geomicrobiol J 32: 1–9.
Dalsgaard T, Stewart FJ, Tahmdrup B, De Brabandere L, Revsbech NP, Ulloa O et al. (2014). Oxygen at nanomolar levels reversibly suppresses process rates and gene expression in anammox and denitrification in the oxygen minimum zone off Northern Chile. Mbio 5: 10–1128.
Deutzmann JS, Stief P, Brandes J, Schink B . (2014). Anaerobic methane oxidation coupled to denitrification is the dominant methane sink in a deep lake. Proc Natl Acad Sci USA 111: 18273–18278.
DeVries T, Deutsch C, Primeau F, Chang B, Devol A . (2012). Global rates of water-column denitrification derived from nitrogen gas measurements. Nat Geosci 5: 547–550.
Ettwig KF, Butler MK, Le Paslier D, Pelletier E, Mangenot S, Kuypers MMM et al. (2010). Nitrite-driven anaerobic methane oxidation by oxygenic bacteria. Nature 464: 543–548.
Ettwig KF, Speth DR, Reimann J, Wu ML, Jetten MS, Keltjens JT . (2012). Bacterial oxygen production in the dark. Front Microbiol 3: 273.
Ettwig KF, van Alen T, van de Pas-Schoonen KT, Jetten MSM, Strous M . (2009). Enrichment and molecular detection of denitrifying methanotrophic bacteria of the NC10 Phylum. Appl Environ Microbiol 75: 3656–3662.
Ganesh S, Bristow LA, Larsen M, Sarode N, Thamdrup B, Stewart FJ . (2015). Size-fraction partitioning of community gene transcription and nitrogen metabolism in a marine oxygen minimum zone. ISME J 9: 2682–2696.
Haroon MF, Hu S, Shi Y, Imelfort M, Keller J, Hugenholtz P et al. (2013). Anaerobic oxidation of methane coupled to nitrate reduction in a novel archaeal lineage. Nature 500: 567–570.
Hu BL, Shen LD, Lian X, Zhu Q, Liu S, Huang Q et al. (2014). Evidence for nitrite-dependent anaerobic methane oxidation as a previously overlooked microbial methane sink in wetlands. Proc Natl Acad Sci USA 111: 4495–4500.
Naqvi SWA, Bange HW, Farias L, Monteiro PMS, Scranton MI, Zhang J . (2010). Marine hypoxia/anoxia as a source of CH4 and N2O. Biogeosciences 7: 2159–2190.
Norði KA, Thamdrup B . (2014). Nitrate-dependent anaerobic methane oxidation in a freshwater sediment. Geochim Cosmochim Acta 132: 141–150.
Pack MA, Heintz MB, Reeburgh WS, Trumbore SE, Valentine DL, Xu X et al. (2015). Methane oxidation in the eastern tropical North Pacific Ocean water column. J Geophys Res Biogeosci 120: 1078–1092.
Raghoebarsing AA, Pol A, van de PasSchoonen KT, Smolders AJP, Ettwig KF, Rijpstra WIC et al. (2006). A microbial consortium couples anaerobic methane oxidation to denitrification. Nature 440: 918–921.
Reeburgh WS . (2007). Oceanic methane biogeochemistry. Chem Rev 107: 486–513.
Sansone FJ, Popp BN, Gasc A, Graham AW, Rust TM . (2001). Highly elevated methane in the eastern tropical North Pacific and associated isotopically enriched fluxes to the atmosphere. Geophys Res Lett 28: 4567–4570.
Shen LD, Wu HS, Gao ZQ . (2015). Distribution and environmental significance of nitrite-dependent anaerobic methane-oxidising bacteria in natural ecosystems. Appl Microbiol Biotechnol 99: 133–142.
Thamdrup B, Dalsgaard T, Revsbech NP . (2012). Widespread functional anoxia in the oxygen minimum zone of the Eastern South Pacific. Deep Sea Res Pt I 65: 36–45.
Tiano L, Garcia-Robledo E, Dalsgaard T, Devol AH, Ward BB, Ulloa O et al. (2014). Oxygen distribution and aerobic respiration in the north and southeastern tropical Pacific oxygen minimum zones. Deep Sea Res Pt I 94: 173–183.
Acknowledgements
We thank the crew of the R/V New Horizon for help in sample collection, Niels Peter Revsbech and Morten Larsen for oxygen concentration analysis in the GD, and Alvaro Morales for coordinating and supporting work at the GD field site. This work was supported by the National Science Foundation (1151698 to FJS), the Sloan Foundation (RC944 to FJS), the Danish National Research Foundation DNRF53, the Danish Council of Independent Research, and the European Research Council ‘Oxygen’ grant (267233; supporting LAB and BT).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Competing interests
The authors declare no conflict of interest.
Additional information
Supplementary Information accompanies this paper on The ISME Journal website
Supplementary information
Rights and permissions
About this article
Cite this article
Padilla, C., Bristow, L., Sarode, N. et al. NC10 bacteria in marine oxygen minimum zones. ISME J 10, 2067–2071 (2016). https://doi.org/10.1038/ismej.2015.262
Received:
Revised:
Accepted:
Published:
Issue date:
DOI: https://doi.org/10.1038/ismej.2015.262
This article is cited by
-
Water column dynamics control nitrite-dependent anaerobic methane oxidation by Candidatus “Methylomirabilis” in stratified lake basins
The ISME Journal (2023)
-
Vertical Microbial Profiling of Arabian Sea Oxygen Minimal Zone Reveals Complex Bacterial Communities and Distinct Functional Implications
Microbial Ecology (2023)
-
The marine nitrogen cycle: new developments and global change
Nature Reviews Microbiology (2022)
-
Active methane processing microbes and the disproportionate role of NC10 phylum in methane mitigation in Amazonian floodplains
Biogeochemistry (2021)
-
Pelagic denitrification and methane oxidation in oxygen-depleted waters of the Louisiana shelf
Biogeochemistry (2021)
