Abstract

Anaerobic ammonium oxidation (anammox) contributes substantially to ocean nitrogen loss, particularly in anoxic marine zones (AMZs). Ammonium is scarce in AMZs, raising the hypothesis that organic nitrogen compounds may be ammonium sources for anammox. Biochemical measurements suggest that the organic compounds urea and cyanate can support anammox in AMZs. However, it is unclear if anammox bacteria degrade these compounds to ammonium themselves, or rely on other organisms for this process. Genes for urea degradation have not been found in anammox bacteria, and genomic evidence for cyanate use for anammox is limited to a cyanase gene recovered from the sediment bacterium Candidatus Scalindua profunda. Here, analysis of Ca. Scalindua single amplified genomes from the Eastern Tropical North Pacific AMZ revealed genes for urea degradation and transport, as well as for cyanate degradation. Urease and cyanase genes were transcribed, along with anammox genes, in the AMZ core where anammox rates peaked. Homologs of these genes were also detected in meta-omic datasets from major AMZs in the Eastern Tropical South Pacific and Arabian Sea. These results suggest that anammox bacteria from different ocean regions can directly access organic nitrogen substrates. Future studies should assess if and under what environmental conditions these substrates contribute to the ammonium budget for anammox.

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Acknowledgements

This work was supported by the National Science Foundation (1151698, 1558916, 1564559 to FJS and 1416673 to KTK), a European Research Council Advanced grant (OXYGEN, 267233 to BT), the Danish National Research Foundation (DNRF53 to BT), a Community Science Program grant from the U.S. Department of Energy (to FJS and KTK), and the Millennium Science Initiative (IC 120019) and Chilean National Scientific and Technological Research Fund (1161483, supporting MA and OU). The work conducted by the DOE Joint Genome Institute, a DOE Office of Science User Facility, is supported under Contract No. DE-AC02-05CH11231. We are grateful to Neha Sarode for help in sequencing analysis, Philipp Hach for help with sample collection, and the captain and crew of the R/V New Horizon for enabling sample collection.

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  1. These authors contributed equally: Sangita Ganesh, Anthony D. Bertagnolli.

Affiliations

  1. School of Biological Sciences, Georgia Institute of Technology, Atlanta, 30332, GA, USA

    • Sangita Ganesh
    • , Anthony D. Bertagnolli
    • , Cory C. Padilla
    •  & Frank J. Stewart
  2. Radiant Genomics, Emeryville, 94608, CA, USA

    • Sangita Ganesh
  3. Biogeochemistry Group, Max Planck Institute for Marine Microbiology, Bremen, Germany

    • Laura A. Bristow
  4. Department of Biology, University of Pennsylvania, Philadelphia, 19104, PA, USA

    • Nigel Blackwood
  5. Graduate Program in Oceanography, Department of Oceanography, Faculty of Natural Sciences and Oceanography, University of Concepción, Casilla 160-C, Concepción, Chile

    • Montserrat Aldunate
  6. Departamento de Oceanografía, Universidad de Concepción, Casilla 160-C, Concepción, 4070386, Chile

    • Montserrat Aldunate
    •  & Osvaldo Ulloa
  7. Marine Chemistry & Geochemistry, Woods Hole Oceanographic Institution, 266 Woods Hole Road, Woods Hole, 02543, MA, USA

    • Annie Bourbonnais
  8. School for Marine Science and Technology, University of Massachusetts Dartmouth, 706 Rodney French Blvd, New Bedford, 02744, MA, USA

    • Annie Bourbonnais
    •  & Mark A. Altabet
  9. Department of Energy Joint Genome Institute, 2800 Mitchell Drive, Walnut Creek, 94598, CA, USA

    • Rex R. Malmstrom
    •  & Tanja Woyke
  10. School of Civil and Environmental Engineering, Georgia Institute of Technology, Atlanta, 30332, GA, USA

    • Konstantinos T. Konstantinidis
  11. Department of Biology and Nordic Center for Earth Evolution (NordCEE), University of Southern Denmark, Odense, Denmark

    • Bo Thamdrup

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https://doi.org/10.1038/s41396-018-0223-9

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