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Denitrifying Bacterial Community Composition Changes Associated with Stages of Denitrification in Oxygen Minimum Zones

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Abstract

Denitrification in the ocean is a major sink for fixed nitrogen in the global N budget, but the process is geographically restricted to a few oceanic regions, including three oceanic oxygen minimum zones (OMZ) and hemipelagic sediments worldwide. Here, we describe the diversity and community composition of microbes responsible for denitrification in the OMZ using polymerase chain reaction, sequence and fragment analysis of clone libraries of the signature genes (nirK and nirS) that encode the enzyme nitrite reductase, responsible for key denitrification transformation steps. We show that denitrifying assemblages vary in space and time and exhibit striking changes in diversity associated with the progression of denitrification from initial anoxia through nitrate depletion. The initial denitrifying assemblage is highly diverse, but succession on the scale of 3–12 days leads to a much less diverse assemblage and dominance by one or a few phylotypes. This progression occurs in the natural environment as well as in enclosed incubations. The emergence of dominants from a vast reservoir of rare types has implications for the maintenance of diversity of the microbial population and suggests that a small number of microbial dominants may be responsible for the greatest rates of transformations involving nitrous oxide and global fixed nitrogen loss. Denitrifying blooms, driven by a few types responding to episodic environmental changes and distributed unevenly in time and space, are consistent with the sampling effect model of diversity–function relationships. Canonical denitrification thus appears to have important parallels with both primary production and nitrogen fixation, which are typically dominated by regionally and temporally restricted blooms that account for a disproportionate share of these processes worldwide.

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Acknowledgments

This work was supported by US National Science Foundation grants to BBW and AJ. We thank Hema Naik and P. V. Narvekar for the nutrient analyses and Caroline B. Tuit for assistance with the bag incubations.

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Authors and Affiliations

  1. Department of Geosciences, Guyot Hall, Princeton University, Princeton, NJ, 08544, USA

    A. Jayakumar & B. B. Ward

  2. School of Earth and Environmental Sciences, Queens College, City University of New York, Flushing, NY, 11367, USA

    G. D. O’Mullan

  3. National Institute of Oceanography, Dona Paula, Goa, 403004, India

    S. W. A. Naqvi

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  1. A. Jayakumar
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Correspondence to B. B. Ward.

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Jayakumar, A., O’Mullan, G.D., Naqvi, S.W.A. et al. Denitrifying Bacterial Community Composition Changes Associated with Stages of Denitrification in Oxygen Minimum Zones. Microb Ecol 58, 350–362 (2009). https://doi.org/10.1007/s00248-009-9487-y

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