Cell Biology

AbstractAlthough bacteria within the Verrucomicrobia phylum are pervasive in soils around the world, they are under-represented in both isolate collections and genomic databases. Here, we describe a single verrucomicrobial group within the class Spartobacteria that is not closely related to any previously described taxa. We examined more than 1,000 soils and found this spartobacterial phylotype to be ubiquitous and consistently one of the most abundant soil bacterial phylotypes, particularly in grasslands, where it was typically the most abundant. We reconstructed a nearly complete genome of this phylotype from a soil metagenome for which we propose the provisional name ‘Candidatus Udaeobacter copiosus’. The Ca. U. copiosus genome is unusually small for a cosmopolitan soil bacterium, estimated by one measure to be only 2.81 Mbp, compared to the predicted effective mean genome size of 4.74 Mbp for soil bacteria. Metabolic reconstruction suggests that Ca. U. copiosus is an aerobic heterotroph with numerous putative amino acid and vitamin auxotrophies. The large population size, relatively small genome and multiple putative auxotrophies characteristic of Ca. U. copiosus suggest that it may be undergoing streamlining selection to minimize cellular architecture, a phenomenon previously thought to be restricted to aquatic bacteria. Although many soil bacteria need relatively large, complex genomes to be successful in soil, Ca. U. copiosus appears to use an alternative strategy, sacrificing metabolic versatility for efficiency to become dominant in the soil environment.

AbstractThe shallow water bivalve Codakia orbicularis lives in symbiotic association with a sulfur-oxidizing bacterium in its gills. The endosymbiont fixes CO2 and thus generates organic carbon compounds, which support the host's growth. To investigate the uncultured symbiont's metabolism and symbiont–host interactions in detail we conducted a proteogenomic analysis of purified bacteria. Unexpectedly, our results reveal a hitherto completely unrecognized feature of the C. orbicularis symbiont's physiology: the symbiont's genome encodes all proteins necessary for biological nitrogen fixation (diazotrophy). Expression of the respective genes under standard ambient conditions was confirmed by proteomics. Nitrogenase activity in the symbiont was also verified by enzyme activity assays. Phylogenetic analysis of the bacterial nitrogenase reductase NifH revealed the symbiont's close relationship to free-living nitrogen-fixing Proteobacteria from the seagrass sediment. The C. orbicularis symbiont, here tentatively named ‘Candidatus Thiodiazotropha endolucinida’, may thus not only sustain the bivalve's carbon demands. C. orbicularis may also benefit from a steady supply of fixed nitrogen from its symbiont—a scenario that is unprecedented in comparable chemoautotrophic symbioses.

AbstractMethanogenesis is the primary biogenic source of methane in the atmosphere and a key contributor to climate change. The long-standing dogma that methanogenesis originated within the Euryarchaeota was recently challenged by the discovery of putative methane-metabolizing genes in members of the Bathyarchaeota, suggesting that methanogenesis may be more phylogenetically widespread than currently appreciated. Here, we present the discovery of divergent methyl-coenzyme M reductase genes in population genomes recovered from anoxic environments with high methane flux that belong to a new archaeal phylum, the Verstraetearchaeota. These archaea encode the genes required for methylotrophic methanogenesis, and may conserve energy using a mechanism similar to that proposed for the obligate H2-dependent methylotrophic Methanomassiliicoccales and recently described Candidatus ‘Methanofastidiosa’. Our findings indicate that we are only beginning to understand methanogen diversity and support an ancient origin for methane metabolism in the Archaea, which is changing our understanding of the global carbon cycle.

AbstractThe subsurface biosphere is largely unexplored and contains a broad diversity of uncultured microbes1. Despite being one of the few prokaryotic lineages that is cosmopolitan in both the terrestrial and marine subsurface2–4, the physiological and ecological roles of SAGMEG (South-African Gold Mine Miscellaneous Euryarchaeal Group) Archaea are unknown. Here, we report the metabolic capabilities of this enigmatic group as inferred from genomic reconstructions. Four high-quality (63–90% complete) genomes were obtained from White Oak River estuary and Yellowstone National Park hot spring sediment metagenomes. Phylogenomic analyses place SAGMEG Archaea as a deeply rooting sister clade of the Thermococci, leading us to propose the name Hadesarchaea for this new Archaeal class. With an estimated genome size of around 1.5 Mbp, the genomes of Hadesarchaea are distinctly streamlined, yet metabolically versatile. They share several physiological mechanisms with strict anaerobic Euryarchaeota. Several metabolic characteristics make them successful in the subsurface, including genes involved in CO and H2 oxidation (or H2 production), with potential coupling to nitrite reduction to ammonia (DNRA). This first glimpse into the metabolic capabilities of these cosmopolitan Archaea suggests they are mediating key geochemical processes and are specialized for survival in the subsurface biosphere.