Unexpectedly high mutation rate of a deep-sea hyperthermophilic anaerobic archaeon

Abstract

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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Fig. 1: Experimental determination of the unbiased mutation rate of the Thermococcus eurythermalis A501 is challenging because this archaeon has unusual physiology (i.e., obligate anaerobic and obligate hyperthermophilic).
Fig. 2: The scaling relationship involving the base-substitution mutation rate per cell division per site (µ), the estimated effective population size (Ne), and genome size across 28 bacterial and two archaeal species.

Data availability

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.

Code availability

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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Acknowledgements

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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HL conceptualized the work and strategy, directed the bioinformatics analyses, interpreted the data, and wrote the main manuscript. XX set up the experimental platform for deep-sea hyperthermophile studies, directed the experimental analyses and related writing, co-interpreted the data, provided comments to the main manuscript, and acquired the strains. JG performed all the experiments with contributions from XM, drafted the related methods in supplementary information and Fig. 1. XW performed all the bioinformatics analyses, co-interpreted the related results, drafted the related methods in supplementary information, Fig. 2 and all supplemental tables. YS contributed the bioinformatics tools for mutation detection and mutation rate calculation.

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Correspondence to Xiang Xiao or Haiwei Luo.

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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

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