Abstract
Sulfate-reducing bacteria Candidatus Desulforudis audaxviator (CDA) were originally discovered in deep fracture fluids accessed via South African gold mines and have since been found in geographically widespread deep subsurface locations. In order to constrain models for subsurface microbial evolution, we compared CDA genomes from Africa, North America and Eurasia using single cell genomics. Unexpectedly, 126 partial single amplified genomes from the three continents, a complete genome from of an isolate from Eurasia, and metagenome-assembled genomes from Africa and Eurasia shared >99.2% average nucleotide identity, low frequency of SNP’s, and near-perfectly conserved prophages and CRISPRs. Our analyses reject sample cross-contamination, recent natural dispersal, and unusually strong purifying selection as likely explanations for these unexpected results. We therefore conclude that the analyzed CDA populations underwent only minimal evolution since their physical separation, potentially as far back as the breakup of Pangea between 165 and 55 Ma ago. High-fidelity DNA replication and repair mechanisms are the most plausible explanation for the highly conserved genome of CDA. CDA presents a stark contrast to the current model organisms in microbial evolutionary studies, which often develop adaptive traits over far shorter periods of time.
Highlights
Knowledge of mechanisms, rates and consequences of microbial evolution is critical to a wide range of scientific and practical endeavors, such as prevention and treatment of human diseases, environmental bioremediation, studies of global biogeochemical cycles and understanding the diversity of life
Of the 150 Candidatus Desulforudis audaxviator (CDA) single amplified genomes (SAGs) obtained in this study, 136 yielded a 16S rRNA gene 100% identical to that of the CDA MP104C metagenome-assembled genome (MAG), whereas 14 had 97–99% 16S rRNA gene identity
PhnDEIMJ had 33–70% Average nucleotide identity (ANI) to Betaproteobacteria Thiobacillus denitrificans, while phnCGHK had 40–50% ANI to a Firmicutes Peptococcaceae lineage, both of which were found among SAGs from the nearby Tau Tona site (Fig. S3)
Summary
Deep fracture water was collected on January 21, 2011 from a borehole drilled at a depth of 1,339 m in Beatrix. Tau Tona Mines are within ~2.7 km of each other and are 200 km from Beatrix Mine. Ground water samples from BLM1 (Fig. 1A) were collected at pressure from 755 mbls. The BLM1 water samples for chemistry and other measurements were collected and analyzed as described elsewhere [20]. Samples from Byelii Yar borehole 1-R (BY-1R) were collected on April 30, 2016 (Fig. 1A). Sampling and characteristics of the water chemistry have been described previously [16, 21]. All samples for SAG analyses were preserved with 5% glycerol and 1x TE buffer (final concentrations), frozen on site, and placed in a −80 °C freezer the same day upon receipt at Bigelow
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