Genome evolution in bacteria isolated from million-year-old subseafloor sediment

Abstract

Beneath the seafloor, microbial life subsists in isolation from the surface world under persistent energy limitation. The nature and extent of genomic evolution in subseafloor microbes has been unknown. Here we show that the genomes of Thalassospira bacterial populations cultured from million-year-old subseafloor sediments evolve by point mutation, with a relatively low rate of homologous recombination and a high frequency of pseudogenes. Ratios of synonymous to non-synonymous mutation rates correlate with the accumulation of pseudogenes, consistent with a dominant role for genetic drift in the subseafloor strains, but not in type strains of Thalassospira isolated from the surface world. Our findings demonstrate that the long term physical isolation of these bacteria, in the absence of recombination, has resulted in clonal populations that evolve consistent with ‘Mullers Ratchet’, whereby reduced access to novel genetic material from neighbors has resulted in fixation of new mutations that accumulate in genomes over millions of years.Significance statementThe nature and extent of genomic evolution in subseafloor microbial populations subsisting for millions of years below the seafloor is unknown. Subseafloor populations have ultra-slow metabolic rates that are hypothesized to restrict reproduction and, consequently, the spread of new traits. Our findings demonstrate that genomes of cultivated bacterial strains from the genus Thalassospira isolated from million-year-old abyssal sediment exhibit greatly reduced levels of homologous recombination, elevated numbers of pseudogenes, and genome-wide evidence of relaxed purifying selection. These substitutions and pseudogenes are fixed into the population, suggesting the genome evolution of these bacteria has been dominated by genetic drift, whereby under long-term physical isolation in small population sizes, and in the absence of homologous recombination, newly acquired mutations accumulate in the genomes of clonal populations over millions of years.

Molecular Evolutionary Dynamics of Energy Limited Microorganisms

“…However, the evolutionary effect of energy limitation is not limited to the quantity and rate of change of genetic diversity. Rather, certain genes repeatedly acquire mutations in energy limited environments ( Zambrano et al 1993 ; Zambrano and Kolter 1996 ; Finkel and Kolter 1999 ; Zinser and Kolter 2004 ; Finkel 2006 ; Kram et al 2017 ; Katz et al 2021 ; Orsi et al 2021 ). These repeated evolutionary outcomes (i.e., parallel evolution) consistently occur across phylogenetically distant taxa ( Martínez-García et al 2003 ; Bacun-Druzina et al 2007 ; Bruno and Freitag 2011 ; Sewell et al 2011 ; Helmus et al 2012 ; Ratib et al 2021 ), suggesting that adaptation continues as the environment becomes increasingly depleted of exploitable energy.…”