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Marine Oxygen-Deficient Zones Harbor Depauperate Denitrifying Communities Compared to Novel Genetic Diversity in Coastal Sediments

  • Microbiology of Aquatic Systems
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Abstract

Denitrification is a critically important biogeochemical pathway that removes fixed nitrogen from ecosystems and thus ultimately controls the rate of primary production in nitrogen-limited systems. We examined the community structure of bacteria containing the nirS gene, a signature gene in the denitrification pathway, from estuarine and salt marsh sediments and from the water column of two of the world’s largest marine oxygen-deficient zones (ODZs). We generated over 125,000 nirS gene sequences, revealing a large degree of genetic diversity including 1,815 unique taxa, the vast majority of which formed clades that contain no cultured representatives. These results underscore how little we know about the genetic diversity of metabolisms underlying this critical biogeochemical pathway. Marine sediments yielded 1,776 unique taxa when clustered at 95 % sequence identity, and there was no single nirS denitrifier that was a competitive dominant; different samples had different highly abundant taxa. By contrast, there were only 39 unique taxa identified in samples from the two ODZs, and 99 % of the sequences belonged to 5 or fewer taxa. The ODZ samples were often dominated by nirS sequences that shared a 92 % sequence identity to a nirS found in the anaerobic ammonium-oxidizing (anammox) genus Scalindua. This sequence was abundant in both ODZs, accounting for 38 and 59 % of all sequences, but it was virtually absent in marine sediments. Our data indicate that ODZs are remarkably depauperate in nirS genes compared to the remarkable genetic richness found in coastal sediments.

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Acknowledgments

Funding for this work came from multiple NSF grants to BBW and from the following NSF grants: DEB-0717155 (to John Hobbie) and DBI-0400819 (to Jennifer L. Bowen). Additional support was provided via start-up funds from University of Massachusetts Boston to JLB. We would like to acknowledge the Salt Pond Sanctuaries and Dr. E. F. X. Hughes and family for allowing us to have access to the Great Sippewissett marsh plots, and Ivan Valiela for providing support and maintenance of the plots. Christopher Jones and Sara Hallin provided us with their curated nirS alignment. Comments from anonymous reviewers greatly improved the quality of this manuscript.

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Bowen, J.L., Weisman, D., Yasuda, M. et al. Marine Oxygen-Deficient Zones Harbor Depauperate Denitrifying Communities Compared to Novel Genetic Diversity in Coastal Sediments. Microb Ecol 70, 311–321 (2015). https://doi.org/10.1007/s00248-015-0582-y

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