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Appl Environ Microbiol. 2018 Jan 31;84(4). pii: e01985-17. doi: 10.1128/AEM.01985-17. Print 2018 Feb 15.

Denitrification by Anaeromyxobacter dehalogenans, a Common Soil Bacterium Lacking the Nitrite Reductase Genes nirS and nirK.

Author information

1
Department of Microbiology, University of Tennessee, Knoxville, Tennessee, USA.
2
Department of Biochemistry and Cellular and Molecular Biology, University of Tennessee, Knoxville, Tennessee, USA.
3
Department of Geology, University of Illinois, Champaign, Illinois, USA.
4
Department of Microbiology, University of Tennessee, Knoxville, Tennessee, USA frank.loeffler@utk.edu.
5
Department of Civil and Environmental Engineering, University of Tennessee, Knoxville, Tennessee, USA.
6
Department of Biosystems Engineering & Soil Science, University of Tennessee, Knoxville, Tennessee, USA.
7
Center for Environmental Biotechnology, University of Tennessee, Knoxville, Tennessee, USA.
8
Biosciences Division, Oak Ridge National Laboratory, Oak Ridge, Tennessee, USA.

Abstract

The versatile soil bacterium Anaeromyxobacter dehalogenans lacks the hallmark denitrification genes nirS and nirK (encoding NO2 -→NO reductases) and couples growth to NO3 - reduction to NH4 + (respiratory ammonification) and to N2O reduction to N2 A. dehalogenans also grows by reducing Fe(III) to Fe(II), which chemically reacts with NO2 - to form N2O (i.e., chemodenitrification). Following the addition of 100 μmol of NO3 - or NO2 - to Fe(III)-grown axenic cultures of A. dehalogenans, 54 (±7) μmol and 113 (±2) μmol N2O-N, respectively, were produced and subsequently consumed. The conversion of NO3 - to N2 in the presence of Fe(II) through linked biotic-abiotic reactions represents an unrecognized ecophysiology of A. dehalogenans The new findings demonstrate that the assessment of gene content alone is insufficient to predict microbial denitrification potential and N loss (i.e., the formation of gaseous N products). A survey of complete bacterial genomes in the NCBI Reference Sequence database coupled with available physiological information revealed that organisms lacking nirS or nirK but with Fe(III) reduction potential and genes for NO3 - and N2O reduction are not rare, indicating that NO3 - reduction to N2 through linked biotic-abiotic reactions is not limited to A. dehalogenans Considering the ubiquity of iron in soils and sediments and the broad distribution of dissimilatory Fe(III) and NO3 - reducers, denitrification independent of NO-forming NO2 - reductases (through combined biotic-abiotic reactions) may have substantial contributions to N loss and N2O flux.IMPORTANCE Current attempts to gauge N loss from soils rely on the quantitative measurement of nirK and nirS genes and/or transcripts. In the presence of iron, the common soil bacterium Anaeromyxobacter dehalogenans is capable of denitrification and the production of N2 without the key denitrification genes nirK and nirS Such chemodenitrifiers denitrify through combined biotic and abiotic reactions and have potentially large contributions to N loss to the atmosphere and fill a heretofore unrecognized ecological niche in soil ecosystems. The findings emphasize that the comprehensive understanding of N flux and the accurate assessment of denitrification potential can be achieved only when integrated studies of interlinked biogeochemical cycles are performed.

KEYWORDS:

Anaeromyxobacter; chemodenitrification; coupled Fe- and N-redox processes; denitrification; nitrogen loss

PMID:
29196287
PMCID:
PMC5795083
DOI:
10.1128/AEM.01985-17
[Indexed for MEDLINE]
Free PMC Article

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