The evolutionary processes that drive variation in genome size across the tree of life remain unresolved. Effective population size (Ne) is thought to play an important role in shaping genome size [1-3]-a key example being the reduced genomes of insect endosymbionts, which undergo population bottlenecks during transmission [4]. However, the existence of reduced genomes in marine and terrestrial prokaryote species with large Ne indicate that genome reduction is influenced by multiple processes [3]. One candidate process is enhanced mutation rate, which can increase adaptive capacity but can also promote gene loss. To investigate evolutionary forces associated with prokaryotic genome reduction, we performed molecular evolutionary and phylogenomic analyses of nine lineages from five bacterial and archaeal phyla. We found that gene-loss rate strongly correlated with synonymous substitution rate (a proxy for mutation rate) in seven of the nine lineages. However, gene-loss rate showed weak or no correlation with the ratio of nonsynonymous/synonymous substitution rate (dN/dS). These results indicate that genome reduction is largely associated with increased mutation rate, while the association between gene loss and changes in Ne is less well defined. Lineages with relatively high dS and dN, as well as smaller genomes, lacked multiple DNA repair genes, providing a proximate cause for increased mutation rates. Our findings suggest that similar mechanisms drive genome reduction in both intracellular and free-living prokaryotes, with implications for developing a comprehensive theory of prokaryote genome size evolution.

College of Plant Protection Southwest University No 2 Tiansheng Road Beibei District Chongqing 400716 China

Department of Biological Sciences National University of Singapore Singapore 117543 Singapore

Okinawa Institute of Science and Technology Graduate University 1919 1 Tancha Onna son Okinawa 904 0495 Japan

Okinawa Institute of Science and Technology Graduate University 1919 1 Tancha Onna son Okinawa 904 0495 Japan; Faculty of Tropical AgriSciences Czech University of Life Sciences Kamýcká 129 Prague CZ 165 00 Czech Republic; School of Life and Environmental Sciences University of Sydney Sydney NSW 2006 Australia

RIKEN Bioresource Research Centre Tsukuba 305 0074 Japan

School of Life and Environmental Sciences University of Sydney Sydney NSW 2006 Australia

School of Life Science and Technology Tokyo Institute of Technology Tokyo 152 8550 Japan

Tropical Biosphere Research Center Center of Molecular Biosciences University of the Ryukyus Nishihara Okinawa 903 0213 Japan

Curr Biol. 2020 Oct 5;30(19):R1083-R1085. doi: 10.1016/j.cub.2020.07.093. PubMed

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