Theory of prokaryotic genome evolution
Itamar Sela a, Yuri I. Wolf a, and Eugene V. Koonin a,1
a National Center for Biotechnology Information, National Library of Medicine, National Institutes of Health, Bethesda, MD 20894
Contributed by Eugene V. Koonin, August 24, 2016 (sent for review June 7, 2016; reviewed by Edo Kussell and Claus O. Wilke)
Bacteria and archaea have small genomes with tightly packed protein-coding genes. Typically, this genome architecture is explained by “genome streamlining” (minimization) under selection for high replication rate. We developed a mathematical model of microbial evolution and tested it against extensive data from multiple genome comparisons to identify the key evolutionary forces. The results indicate that genome evolution is not governed by streamlining but rather, reflects the balance between the benefit of additional genes that diminishes with the genome size and the intrinsic preference for DNA deletion over acquisition. These results explain the observation that, in an apparent contradiction with the population genetic theory, microbes with large genomes reach higher abundance and are subject to stronger selection than small “streamlined” genomes.
Bacteria and archaea typically possess small genomes that are tightly packed with protein-coding genes. The compactness of prokaryotic genomes is commonly perceived as evidence of adaptive genome streamlining caused by strong purifying selection in large microbial populations. In such populations, even the small cost incurred by nonfunctional DNA because of extra energy and time expenditure is thought to be sufficient for this extra genetic material to be eliminated by selection. However, contrary to the predictions of this model, there exists a consistent, positive correlation between the strength of selection at the protein sequence level, measured as the ratio of nonsynonymous to synonymous substitution rates, and microbial genome size. Here, by fitting the genome size distributions in multiple groups of prokaryotes to predictions of mathematical models of population evolution, we show that only models in which acquisition of additional genes is, on average, slightly beneficial yield a good fit to genomic data. These results suggest that the number of genes in prokaryotic genomes reflects the equilibrium between the benefit of additional genes that diminishes as the genome grows and deletion bias (i.e., the rate of deletion of genetic material being slightly greater than the rate of acquisition). Thus, new genes acquired by microbial genomes, on average, appear to be adaptive. The tight spacing of protein-coding genes likely results from a combination of the deletion bias and purifying selection that efficiently eliminates nonfunctional, noncoding sequences.
evolutionary genomics prokaryotic genome size genome streamlining positive selection deletion bias
1 To whom correspondence should be addressed.
This contribution is part of the special series of Inaugural Articles by members of the National Academy of Sciences elected in 2016.
Author contributions: Y.I.W. and E.V.K. designed research; I.S. performed research; I.S., Y.I.W., and E.V.K. analyzed data; and I.S. and E.V.K. wrote the paper.
Reviewers: E.K., New York University; and C.O.W., The University of Texas at Austin.
The authors declare no conflict of interest.
This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1614083113/-/DCSupplemental.
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