Deep-sea hydrothermal vents resemble the early Earth, and thus the dominant Thermococcaceae inhabitants, which occupy an evolutionarily basal position of the archaeal tree and take an obligate anaerobic hyperthermophilic free-living lifestyle, are likely excellent models to study the evolution of early life. Here, we determined that unbiased mutation rate of a representative species, Thermococcus eurythermalis, exceeded that of all known free-living prokaryotes by 1-2 orders of magnitude, and thus rejected the long-standing hypothesis that low mutation rates were selectively favored in hyperthermophiles. We further sequenced multiple and diverse isolates of this species and calculated that T. eurythermalis has a lower effective population size than other free-living prokaryotes by 1-2 orders of magnitude. These data collectively indicate that the high mutation rate of this species is not selectively favored but instead driven by random genetic drift. The availability of these unusual data also helps explore mechanisms underlying microbial genome size evolution. We showed that genome size is negatively correlated with mutation rate and positively correlated with effective population size across 30 bacterial and archaeal lineages, suggesting that increased mutation rate and random genetic drift are likely two important mechanisms driving microbial genome reduction. Future determinations of the unbiased mutation rate of more representative lineages with highly reduced genomes such as Prochlorococcus and Pelagibacterales that dominate marine microbial communities are essential to test these hypotheses.
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All the datasets generated, analyzed, and presented in the current study are available in the Supplementary Information. Genomic sequences of the eight Thermococcus eurythermalis strains are available at the JGI IMG under the GOLD study id Gs0142375. Raw reads of the eight strains are available at the NCBI SRA under the accession number PRJNA679699.
The custom scripts used in this study have been deposited in the online repository (https://github.com/luolab-cuhk/Thermococcus-mut-genome-size).
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This research is supported by the National Key R&D Program of China (2018YFC0309800), National Nature of Science China (NSFC 41530967), China Ocean Mineral Resources R & D Association DY125-22-04, the Hong Kong Branch of Southern Marine Science and Engineering Guangdong Laboratory (Guangzhou) (SMSEGL20SC02), and the Hong Kong Research Grants Council Area of Excellence Scheme (AoE/M-403/16).
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Gu, J., Wang, X., Ma, X. et al. Unexpectedly high mutation rate of a deep-sea hyperthermophilic anaerobic archaeon. ISME J (2021). https://doi.org/10.1038/s41396-020-00888-5