Rice paddyNitrospiraeencode and express genes related to sulfate respiration: proposal of the new genusCandidatusSulfobium

Zecchin et al. (2017).
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AbstractNitrospiraespp. distantly related to thermophilic, sulfate-reducingThermodesulfovibriospecies are regularly observed in environmental surveys of anoxic marine and freshwater habitats. However, little is known about their genetic make-up and physiology. Here, we present the draft genome ofNitrospiraebacterium Nbg-4 as a representative of this clade and analyzed itsin situprotein expression under sulfate-enriched and sulfate-depleted conditions in rice paddy soil. The genome of Nbg-4 was assembled from replicated metagenomes of rice paddy soil that was used to grow rice plants in the presence and absence of gypsum (CaSO4×2H2O). Nbg-4 encoded the full pathway of dissimilatory sulfate reduction and showed expression thereof 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, which was expressed in bulk soil without gypsum amendment. The relative abundance of Nbg-4-related metagenome reads was similar under both treatments indicating that it maintained stable populations while shifting its energy metabolism. Further genome reconstruction revealed the potential to utilize butyrate, formate, H2, or acetate as electron donor, with the Wood-Ljungdahl pathway being expressed under both conditions. Comparison to publicly availableNitrospiraegenome bins confirmed that the pathway for dissimilatory sulfate reduction is also present in relatedNitrospiraerecovered from groundwater. Subsequent phylogenomics showed that such microorganisms form a novel genus within the phylumNitrospirae, with Nbg-4 as a representative species. Based on the widespread occurrence of this novel genus, we propose for Nbg-4 the nameCandidatusSulfobium mesophilum, gen. nov., spec. nov.ImportanceRice paddies are indispensable for food supply but are a major source of the greenhouse gas methane. If 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 of Italian rice paddy soil, we could retrieve the population genome of a novel member of the phylumNitrospirae. This microorganism encoded the full pathway of dissimilatory sulfate reduction and expressed itin situunder sulfate-enriched and anoxic conditions. Phylogenomics and comparison to environmental surveys showed that such microorganisms are actually widespread in freshwater and marine environments. At the same time, they represent a yet undiscovered genus within the little exploredNitrospirae. Our results will be important to design enrichment strategies and postgenomic studies to fully understand the contribution of these novelNitrospiraeto the global sulfur cycle.
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