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Two fundamentally different classes of microbial genes

Nature Microbiology volume 2, Article number: 16208 (2017) Cite this article

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Abstract

The evolution of bacterial and archaeal genomes is highly dynamic and involves extensive horizontal gene transfer and gene loss1–4. Furthermore, many microbial species appear to have open pangenomes, where each newly sequenced genome contains more than 10% ORFans, that is, genes without detectable homologues in other species5,6. Here, we report a quantitative analysis of microbial genome evolution by fitting the parameters of a simple, steady-state evolutionary model to the comparative genomic data on the gene content and gene order similarity between archaeal genomes. The results reveal two sharply distinct classes of microbial genes, one of which is characterized by effectively instantaneous gene replacement, and the other consists of genes with finite, distributed replacement rates. These findings imply a conservative estimate of the size of the prokaryotic genomic universe, which appears to consist of at least a billion distinct genes. Furthermore, the same distribution of constraints is shown to govern the evolution of gene complement and gene order, without the need to invoke long-range conservation or the selfish operon concept7.

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Figure 1: Architecture of the genome evolution model.
Figure 2: Gene content similarity between archaea versus distance along the tree.
Figure 3: Gene order similarity between archaea versus distance along the tree.

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  • 14 July 2017

    In the PDF version of this article previously published, the year of publication provided in the footer of each page and in the 'How to cite' section was erroneously given as 2017, it should have been 2016. This error has now been corrected. The HTML version of the article was not affected.

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Acknowledgements

The authors thank P. Higgs (McMaster University), J. Iranzo (NCBI, NIH) and D. Kristensen (NCBI; currently, University of Iowa) for discussions. The authors' research is supported by intramural funds of the US Department of Health and Human Services (to the National Library of Medicine).

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Authors and Affiliations

  1. National Center for Biotechnology Information, National Library of Medicine, National Institute of Health, Bethesda, 20894, Maryland, USA

    Yuri I. Wolf, Kira S. Makarova, Alexander E. Lobkovsky & Eugene V. Koonin

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  1. Yuri I. Wolf
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  2. Kira S. Makarova
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  3. Alexander E. Lobkovsky
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  4. Eugene V. Koonin
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Contributions

Y.I.W. and E.V.K. conceived the study. Y.I.W. performed research. Y.I.W., K.S.M., A.E.L. and E.V.K. analysed the results. Y.I.W. and E.V.K. wrote the manuscript, which was read, edited and approved by all authors.

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Correspondence to Eugene V. Koonin.

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The authors declare no competing financial interests.

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Supplementary Figures 1–15, Supplementary Table 1 (PDF 2154 kb)

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Wolf, Y., Makarova, K., Lobkovsky, A. et al. Two fundamentally different classes of microbial genes. Nat Microbiol 2, 16208 (2017). https://doi.org/10.1038/nmicrobiol.2016.208

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