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


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          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 (CaSO 4·2H 2O). 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, H 2, 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.

          IMPORTANCE Rice paddies are indispensable for the food supply but are a major source of the greenhouse gas methane. If it were not counterbalanced by cryptic sulfur cycling, methane emission from rice paddy fields would be even higher. However, the microorganisms involved in this sulfur cycling are little understood. By using an environmental systems biology approach with Italian rice paddy soil, we could retrieve the population genome of a novel member of the phylum Nitrospirae. This microorganism encoded the full pathway of dissimilatory sulfate reduction and expressed it in anoxic paddy soil under sulfate-enriched conditions. Phylogenomics and comparison to the results of environmental surveys showed that such microorganisms are actually widespread in freshwater and marine environments. At the same time, they represent an undiscovered genus within the little-explored phylum Nitrospirae. Our results will be important for the design of enrichment strategies and postgenomic studies to further understanding of the contribution of these novel Nitrospirae spp. to the global sulfur cycle.

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          Most cited references 59

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          Sulphate-reducing bacteria (SRB) are anaerobic microorganisms that use sulphate as a terminal electron acceptor in, for example, the degradation of organic compounds. They are ubiquitous in anoxic habitats, where they have an important role in both the sulphur and carbon cycles. SRB can cause a serious problem for industries, such as the offshore oil industry, because of the production of sulphide, which is highly reactive, corrosive and toxic. However, these organisms can also be beneficial by removing sulphate and heavy metals from waste streams. Although SRB have been studied for more than a century, it is only with the recent emergence of new molecular biological and genomic techniques that we have begun to obtain detailed information on their way of life.
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              Biochemistry and molecular biology of lithotrophic sulfur oxidation by taxonomically and ecologically diverse bacteria and archaea.

              Lithotrophic sulfur oxidation is an ancient metabolic process. Ecologically and taxonomically diverged prokaryotes have differential abilities to utilize different reduced sulfur compounds as lithotrophic substrates. Different phototrophic or chemotrophic species use different enzymes, pathways and mechanisms of electron transport and energy conservation for the oxidation of any given substrate. While the mechanisms of sulfur oxidation in obligately chemolithotrophic bacteria, predominantly belonging to Beta- (e.g. Thiobacillus) and Gammaproteobacteria (e.g. Thiomicrospira), are not well established, the Sox system is the central pathway in the facultative bacteria from Alphaproteobacteria (e.g. Paracoccus). Interestingly, photolithotrophs such as Rhodovulum belonging to Alphaproteobacteria also use the Sox system, whereas those from Chromatiaceae and Chlorobi use a truncated Sox complex alongside reverse-acting sulfate-reducing systems. Certain chemotrophic magnetotactic Alphaproteobacteria allegedly utilize such a combined mechanism. Sulfur-chemolithotrophic metabolism in Archaea, largely restricted to Sulfolobales, is distinct from those in Bacteria. Phylogenetic and biomolecular fossil data suggest that the ubiquity of sox genes could be due to horizontal transfer, and coupled sulfate reduction/sulfide oxidation pathways, originating in planktonic ancestors of Chromatiaceae or Chlorobi, could be ancestral to all sulfur-lithotrophic processes. However, the possibility that chemolithotrophy, originating in deep sea, is the actual ancestral form of sulfur oxidation cannot be ruled out.

                Author and article information

                Role: Editor
                Appl Environ Microbiol
                Appl. Environ. Microbiol
                Applied and Environmental Microbiology
                American Society for Microbiology (1752 N St., N.W., Washington, DC )
                15 December 2017
                14 February 2018
                1 March 2018
                14 February 2018
                : 84
                : 5
                [a ]Department of Biology, University of Constance, Constance, Germany
                [b ]Dipartimento di Scienze per gli Alimenti, la Nutrizione e l'Ambiente (DeFENS), Università degli Studi di Milano, Milan, Italy
                [c ]Institute of Animal Science, Hohenheim University, Stuttgart, Germany
                [d ]University of Florida, UF/IFAS, Department for Microbiology and Cell Science, Fort Lauderdale Research and Education Center, Davie, Florida, USA
                [e ]Department of Earth and Planetary Science, University of California, Berkeley, California, USA
                [f ]Helmholtz Centre for Environmental Research—UFZ, Department of Molecular Systems Biology, Leipzig, Germany
                [g ]Department of Microorganisms, Leibniz Institute DSMZ—German Collection of Microorganisms and Cell Cultures, Braunschweig, Germany
                University of Bayreuth
                Author notes
                Address correspondence to Michael Pester, Michael.Pester@ 123456dsmz.de .

                S.Z. and R.C.M. contributed equally to this article.

                Citation Zecchin S, Mueller RC, Seifert J, Stingl U, Anantharaman K, von Bergen M, Cavalca L, Pester M. 2018. Rice paddy Nitrospirae carry and express genes related to sulfate respiration: proposal of the new genus “ Candidatus Sulfobium.” Appl Environ Microbiol 84:e02224-17. https://doi.org/10.1128/AEM.02224-17.

                Copyright © 2018 Zecchin et al.

                This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license.

                Page count
                supplementary-material: 2, Figures: 4, Tables: 2, Equations: 0, References: 82, Pages: 15, Words: 9583
                Funded by: ERASMUS+;
                Award Recipient :
                Funded by: Deutsche Forschungsgemeinschaft (DFG), https://doi.org/10.13039/501100001659;
                Award ID: PE 2147/1-1
                Award Recipient :
                Funded by: U.S. Department of Agriculture (USDA), https://doi.org/10.13039/100000199;
                Award ID: FLA-FTL-005631
                Award Recipient :
                Funded by: EC | FP7 | FP7 People: Marie-Curie Actions (PEOPLE), https://doi.org/10.13039/100011264;
                Award ID: PCIG14-GA-2013-630188
                Award Recipient :
                Environmental Microbiology
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                March 2018


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