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.

深海热液喷口与早期地球相似，因此占据古菌树进化基础位置并采取专性厌氧超嗜热自由生活生活方式的主要热球菌科居民可能是研究早期生命进化的优秀模型。在这里，我们确定代表性物种的无偏突变率，Thermococcus eurytheralis，超过所有已知的自由生活原核生物的 1-2 个数量级，因此拒绝了长期存在的假设，即低突变率在嗜热菌中有选择性地受到青睐. 我们进一步对该物种的多个不同分离物进行了测序，并计算出T. eurythermalis有效种群规模比其他自由生活的原核生物低 1-2 个数量级。这些数据共同表明，该物种的高突变率并非有选择地受到青睐，而是由随机遗传漂移驱动。这些不寻常数据的可用性也有助于探索微生物基因组大小进化的潜在机制。我们发现基因组大小与突变率呈负相关，与 30 个细菌和古细菌谱系的有效种群大小呈正相关，这表明突变率增加和随机遗传漂变可能是推动微生物基因组减少的两个重要机制。未来确定基因组高度减少的更具代表性的谱系的无偏突变率，如Prochlorococcus和在海洋微生物群落中占主导地位的Pelagibacterales对检验这些假设至关重要。