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

Abstract

An enigmatic uncultured member of Firmicutes, Candidatus Desulforudis audaxviator (CDA), is known by its genome retrieved from the deep gold mine in South Africa, where it formed a single-species ecosystem fuelled by hydrogen from water radiolysis. It was believed that in situ conditions CDA relied on scarce energy supply and did not divide for hundreds to thousand years. We have isolated CDA strain BYF from a 2-km-deep aquifer in Western Siberia and obtained a laboratory culture growing with a doubling time of 28.5 h. BYF uses not only H 2 but also various organic electron donors for sulfate respiration. Growth required elemental iron, and ferrous iron did not substitute for it. A complex intracellular organization included gas vesicles, internal membranes, and electron-dense structures enriched in phosphorus, iron, and calcium. Genome comparison of BYF with the South African CDA revealed minimal differences mostly related to mobile elements and prophage insertions. Two genomes harbored <800 single-nucleotide polymorphisms and had nearly identical CRISPR loci. We suggest that spores with the gas vesicles may facilitate global distribution of CDA followed by colonization of suitable subsurface environments. Alternatively, a slow evolution rate in the deep subsurface could result in high genetic similarity of CDA populations at two sites spatially separated for hundreds of millions of years.

Diversification of methanogens into hyperalkaline serpentinizing environments through adaptations to minimize oxidant limitation

“…For example, seven Sulfolobus islandicus genomes recovered from globally distributed locations that diverged recently in evolutionary time (~910,000 years ago) shared a core genome including housekeeping genes, but also encoded variable genomic regions containing small inversions and rearrangements, many of which were also associated with CRISPR-Cas genes [95]. Like the Methanobacterium populations from 85 m depth in NSHQ14, other subsurface communities include population level genomic diversity that was proposed to have been generated via the activity of mobile elements [97][98][99]. Similar to the ISNCY transposase, genes flanking a protein belonging to the C39 peptidase family that is suggested to have contributed to recent diversification of Type II Methanobacterium cells (Supplementary Table 2) were largely syntenic among closely related proteins but not among those encoding more divergent orthologs, and rearrangement of genes co-localized with this peptidase were also observed ( Supplementary Fig.…”

Sulfur and Methane-Oxidizing Microbial Community in a Terrestrial Mud Volcano Revealed by Metagenomics

“…The second MAG (Kmv41) was phylogenetically related to Ca. Desulforudis audaxviator (72.5% AAI, 77.1% ANI), an enigmatic chemolithoautotrophic sulfate-reducing Firmicutes, thriving in terrestrial deep subsurface environments [ 60 , 61 ], and to Ca. Desulfopertinax cowenii (77.2% AAI, 78.8% AN) from basalt-hosted fluids of the deep subseafloor [ 62 ].…”

“…Thermodesulfovibrio species are widespread in different hydrothermal habitats, including the deep thermal aquifers [ 78 ], while Ca. Desulforudis have been detected exclusively in the deep subsurface [ 60 , 61 , 62 ]. Interestingly, other typical members of the microbial communities of the deep subsurface ecosystems, thermophilic methanogenic archaea [ 79 ], were not found.…”

Microbial Life in the Deep Subsurface Aquifer Illuminated by Metagenomics

“…Riflebacteria and BRC1 ( Kadnikov et al, 2018 , 2019a , b ) and cultivation of an enigmatic uncultured firmicute, Ca. Desulforudis audaxviator ( Karnachuk et al, 2019 ), previously known by its genome retrieved from a deep gold mine in South Africa, where it formed a single-species hydrogen-driven ecosystem ( Chivian et al, 2008 ).…”