Rice Paddy Nitrospirae Carry and Express Genes Related to Sulfate Respiration: Proposal of the New Genus "Candidatus Sulfobium"

Abstract
Nitrospirae spp. distantly related to thermophilic, sulfate-reducing Thermodesulfovibrio species are regularly observed in environmental surveys of anoxic marine and freshwater habitats. Here we present a metaproteogenomic analysis of Nitrospirae bacterium Nbg-4 as a representative of this clade. Its genome was assembled from replicated metagenomes of rice paddy soil that was used to grow rice in the presence and absence of gypsum (CaSO4·2H2O). Nbg-4 encoded the full pathway of dissimilatory sulfate reduction and showed expression of this pathway in gypsum-amended anoxic bulk soil as revealed by parallel metaproteomics. In addition, Nbg-4 encoded the full pathway of dissimilatory nitrate reduction to ammonia (DNRA), with expression of its first step being detected in bulk soil without gypsum amendment. The relative abundances of Nbg-4 were similar under both treatments, indicating that Nbg-4 maintained stable populations while shifting its energy metabolism. Whether Nbg-4 is a strict sulfate reducer or can couple sulfur oxidation to DNRA by operating the pathway of dissimilatory sulfate reduction in reverse could not be resolved. Further genome reconstruction revealed the potential to utilize butyrate, formate, H2, or acetate as an electron donor; the Wood-Ljungdahl pathway was expressed under both treatments. Comparison to publicly available Nitrospirae genome bins revealed the pathway for dissimilatory sulfate reduction also in related Nitrospirae recovered from groundwater. Subsequent phylogenomics showed that such microorganisms form a novel genus within the Nitrospirae, with Nbg-4 as a representative species. Based on the widespread occurrence of this novel genus, we propose for Nbg-4 the name “Candidatus Sulfobium mesophilum,” gen. nov., sp. nov.

Citation
Zecchin, S., Mueller, R. C., Seifert, J., Stingl, U., Anantharaman, K., von Bergen, M., … Pester, M. (2018). Rice Paddy Nitrospirae Carry and Express Genes Related to Sulfate Respiration: Proposal of the New Genus “Candidatus Sulfobium.” Applied and Environmental Microbiology, 84(5). doi:10.1128/aem.02224-17

Acknowledgements
This research was financed by the German Research Foundation (DFG) (PE 2147/1-1, to M.P.) and the European Union (FP7-People-2013-CIG, grant PCIG14-GA-2013-630188, to M.P.). This research was also supported by the Ph.D. Program in Food Systems at the University of Milan, as well as by an Erasmus+ placement studentship, both awarded to S.Z. Funding for U.S. was provided through baseline funds from KAUST and through the USDA National Institute of Food and Agriculture, Hatch project FLA-FTL-005631.

Publisher
AMER SOC MICROBIOLOGY

Journal
APPLIED AND ENVIRONMENTAL MICROBIOLOGY

DOI
10.1128/AEM.02224-17

PubMed ID
29247059

PubMed Central ID
PMC5812927

Additional Links
https://journals.asm.org/doi/10.1128/AEM.02224-17

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