Genomic comparisons of a bacterial lineage that inhabits both marine and terrestrial deep subsurface systems

Abstract

It is generally accepted that diverse, poorly characterized microorganisms reside deep within Earth’s crust. One such lineage of deep subsurface-dwelling bacteria is an uncultivated member of the Firmicutes phylum that can dominate molecular surveys from both marine and continental rock fracture fluids, sometimes forming the sole member of a single-species microbiome. Here, we reconstructed a genome from basalt-hosted fluids of the deep subseafloor along the eastern Juan de Fuca Ridge flank and used a phylogenomic analysis to show that, despite vast differences in geographic origin and habitat, it forms a monophyletic clade with the terrestrial deep subsurface genome of “Candidatus Desulforudis audaxviator” MP104C. While a limited number of differences were observed between the marine genome of “Candidatus Desulfopertinax cowenii” modA32 and its terrestrial relative that may be of potential adaptive importance, here it is revealed that the two are remarkably similar thermophiles possessing the genetic capacity for motility, sporulation, hydrogenotrophy, chemoorganotrophy, dissimilatory sulfate reduction, and the ability to fix inorganic carbon via the Wood-Ljungdahl pathway for chemoautotrophic growth. Our results provide insights into the genetic repertoire within marine and terrestrial members of a bacterial lineage that is widespread in the global deep subsurface biosphere, and provides a natural means to investigate adaptations specific to these two environments.

Domestication of previously uncultivated Candidatus Desulforudis audaxviator from a deep aquifer in Siberia sheds light on its physiology and evolution

“…Consistently with an observation of the gas vesicles, the CDA genome contains a cluster of gvp genes, including gvpA, gvpL/gvpF, gvpK, gvpG, gvpN, and gvpR. The gvp cluster is absent in Candidatus Desulfopertinax cowenii, the closest relative of CDA whose composite genome was obtained from basalt-hosted fluids of the deep subseafloor at Juan de Fuca Ridge [32].…”

MEBS, a software platform to evaluate large (meta)genomic collections according to their metabolic machinery: unraveling the sulfur cycle

“…Another 59 Sur organisms have been isolated from Sulfur-rich environments, such as hot springs or solfataric muds. Remarkably, some of this species include hard-to culture genomes reconstructed from metagenomic sequences such as Candidatus Desulforudis audaxviator MP104C isolated from basalt-hosted fluids of the deep subsea floor [ 6 ], an unnamed endosymbiont of a scaly snail from a black smoker chimney [ 57 ], and archaeon Geoglobus ahangari , sampled from a 2000-meter-deep hydrothermal vent [ 58 ]. Furthermore, we also confirmed within Sur the implication of S-cycle of 20 species of the genus Campylobacter.…”

“…Nowadays, accessing the total repertoire of genomes within complex communities by means of metagenomics is becoming a standard and routine procedure in order to attain the full insight of the diversity, ecology, evolution, and functional makeup of the microbial world [ 5 ]. Furthermore, the accurate reconstruction of microbial genomes and draft-populations from environmental metagenomic studies has been shown to be a powerful approach [ 6 – 10 ], providing clues about the potential metabolic strategies of hard-to-culture microbial lineages by linking the functional mechanisms that support specific metabolisms with taxonomic, systematic, and ecological contexts of that lineage [ 8 ].…”

Carbon fixation and energy metabolisms of a subseafloor olivine biofilm

“…3; Supplementary Table 2) [52]. These organisms are common deep subsurface inhabitants of both the JdFR aquifer and continental aquifers [12,14,15,50,52], and though uncultivated, possess a suite of energy and carbon metabolisms, including the potential to fix carbon via the Wood-Ljungdahl pathway [50,52]. The most abundant archaeal lineage in the JdFR aquifer community is Archaeoglobaceae [1,12,14,16,47].…”

“…The co-dominance of Clostridia and Archaeoglobaceae lineages has been described in terrestrial deep subsurface environments such as continental mines and fractures as well as marine aquifers [1,15,16,50,[52][53][54], and we are just beginning to understand their role in cycling carbon and producing energy in the deep crust. Their presence here in this JdFR community indicates there may be a shared hydrogen-based functional role for these microorganisms in deep thermal aquifers.…”