Publications

4369

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.

Summary Anaerobic ammonium‐oxidizing (anammox) bacteria affiliated with the genus ‘ Candidatus Scalindua’ are responsible for significant nitrogen loss in oceans, and thus their ecophysiology is of great interest. Here, we enriched a marine anammox bacterium, ‘ Ca . S. japonica’ from a Hiroshima bay sediment in Japan, and comparative genomic and proteomic analyses of ‘ Ca . S. japonica’ were conducted. Sequence of the 4.81‐Mb genome containing 4019 coding regions of genes (CDSs) composed of 47 contigs was determined. In the proteome, 1762 out of 4019 CDSs in the ‘ Ca . S. japonica’ genome were detected. Based on the genomic and proteomic data, the core anammox process and carbon fixation of ‘ Ca . S. japonica’ were further investigated. Additionally, the present study provides the first detailed insights into the genetic background responsible for iron acquisition and menaquinone biosynthesis in anammox bacterial cells. Comparative analysis of the ‘ Ca . Scalindua’ genomes revealed that the 1502 genes found in the ‘ Ca . S. japonica’ genome were not present in the ‘ Ca . S. profunda’ and ‘ Ca . S. rubra’ genomes, showing a high genomic diversity. This result may reflect a high phylogenetic diversity of the genus ‘ Ca . Scalindua’.

AbstractChallenges in cultivating microorganisms have limited the phylogenetic diversity of currently available microbial genomes. This is being addressed by advances in sequencing throughput and computational techniques that allow for the cultivation-independent recovery of genomes from metagenomes. Here, we report the reconstruction of 7,903 bacterial and archaeal genomes from >1,500 public metagenomes. All genomes are estimated to be ≥50% complete and nearly half are ≥90% complete with ≤5% contamination. These genomes increase the phylogenetic diversity of bacterial and archaeal genome trees by >30% and provide the first representatives of 17 bacterial and three archaeal candidate phyla. We also recovered 245 genomes from the Patescibacteria superphylum (also known as the Candidate Phyla Radiation) and find that the relative diversity of this group varies substantially with different protein marker sets. The scale and quality of this data set demonstrate that recovering genomes from metagenomes provides an expedient path forward to exploring microbial dark matter.

Significance Gastrointestinal symbionts of organisms are important in the breakdown of food for the host, particularly for herbivores requiring exogenous enzymes to digest complex polysaccharides in their diet. However, their role in the digestion of algae in marine piscine herbivores remains unresolved. Here, we show that the diversity of food sources available to herbivorous surgeonfishes is directly linked with the genetic makeup of their enteric microbiota. Importantly, the genomic blueprint of dominant enteric symbionts belonging to diverse Epulopiscium clades differs according to the host diet. Thus, the acquisition of a unique enteric microbiota specialized to their diets likely shapes the nutritional ecology of piscine herbivores, in turn facilitating the coexistence of a high diversity of marine species within coral reefs.