Why can the rate of evolution in prokaryotes be so rapid?

  • Why can the rate of evolution in prokaryotes be so rapid?
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Why can the rate of evolution in prokaryotes be so rapid?

Volume 23, Issue 10, October 2015, Pages 598-605

Why can the rate of evolution in prokaryotes be so rapid?

https://doi.org/10.1016/j.tim.2015.07.006Get rights and content

It has long been recognized that even closely related strains of bacteria and archaea can greatly differ in gene content 1, 2, 3. The rate and promiscuity with which genes change residence in prokaryote genomes is of such magnitude that many have rejected the concept of prokaryote species (e.g., [4]) or the possibility of reconstructing a bifurcating tree of prokaryote life (e.g., [5]). The realization of the high rates of gene content turnover has led to the paradigm of a core genome of genes

A plethora of comparative genomics studies have demonstrated the rate of prokaryote gene content turnover to be very high. However, systematic attempts to estimate how fast gene turnover occurs over evolutionary time, expressed per genome per generation or relative to point mutation, have been rare. To our knowledge, the first study to explicitly address this question was by Hao and Golding [18] who used a maximum likelihood method to quantify both insertion and deletion rates of genes relative

The fact that most LGT events are deleterious poses the question why LGT seemingly occurs at high rates. Both rates of mutation and gene content change are controlled by intrinsic factors (i.e., those under genetic control of the cell) and extrinsic factors (i.e., those mediated by the environment, including other biological agents). Mutation rate is in part determined by the fidelity of the replication and repair machinery of the cell, and can be elevated directly by extrinsic stress factors

Although there is a marked lack of available data on rates of LGT [46], analysis of closely related genomes from a variety of species suggests that prokaryote genomes could potentially change more rapidly due to lateral gene transfers than due to point mutation. Understanding the (in)ability of selection to drive LGT rate has important implications for our understanding of a range of topics in evolutionary microbiology, such as adaptation to novel niches (Box 2). It has become commonplace to

M.V. and A.E-W. conceived the paper, performed analyses and wrote the manuscript, M.C.H., T.A.tB. and M.W.J.VP. performed analyses, helped with data interpretation and manuscript revision.

We thank Elze Hesse for helpful discussion and Ruben Nowell and Brian Golding for expounding on their results. This project was in part supported by the BioAssist/BRS programme of the Netherlands Bioinformatics Centre (NBIC). M.V. was supported by investment from the European Regional Development Fund and the European Social Fund Convergence Programme for Cornwall and the Isles of Scilly to the ECEHH.

Distribution of fitness effects (DFE)mutations, as well as lateral gene transfer (LGT) events, have fitness effects that can be broadly divided into three categories. First, there are mutations that decrease fitness. Second, there are ‘neutral’ mutations, which have little or no effect on fitness. Third, there are advantageous mutations, which increase fitness by allowing organisms to adapt to their environment. However, in reality, there is a continuum of selective effects, stretching from

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    • 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, 2, 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.

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