Excess of non-conservative amino acid changes in marine bacterioplankton lineages with reduced genomes

Abstract

Surface ocean waters are dominated by planktonic bacterial lineages with highly reduced genomes. The best examples are the cyanobacterial genus Prochlorococcus, the alphaproteobacterial clade SAR11 and the gammaproteobacterial clade SAR86, which together represent over 50% of the cells in surface oceans. Several studies have identified signatures of selection on these lineages in today's ocean and have postulated selection as the primary force throughout their evolutionary history. However, massive loss of genomic DNA in these lineages often occurred in the distant past, and the selective pressures underlying these ancient events have not been assessed. Here, we probe ancient selective pressures by computing %GC-corrected rates of conservative and radical nonsynonymous nucleotide substitutions. Surprisingly, we found an excess of radical changes in several of these lineages in comparison to their relatives with larger genomes. Furthermore, analyses of allelic genome sequences of several populations within these lineages consistently supported that radical replacements are more likely to be deleterious than conservative changes. Our results suggest coincidence of massive genomic DNA losses and increased power of genetic drift, but we also suggest that additional evidence independent of the nucleotide substitution analyses is needed to support a primary role of genetic drift driving ancient genome reduction of marine bacterioplankton lineages.

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Figure 1: Analysis of conservative and radical nonsynonymous nucleotide substitution among Prochlorococcus lineages.
Figure 2: Analysis of conservative and radical nonsynonymous nucleotide substitution between SAR86 and other Gammaproteobacterial lineages.
Figure 3: Analysis of conservative and radical nonsynonymous nucleotide substitution between SAG-O19 and other Roseobacter lineages.
Figure 4: Analysis of conservative and radical nonsynonymous nucleotide substitution between SAR11 and other Alphaproteobacterial lineages.

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Acknowledgements

This research was funded by the National Natural Science Foundation of China (41576141), the Hong Kong RGC Early Career Scheme (24101015), the Hong Kong Environment and Conservation Fund (15/2016), the Chinese University of Hong Kong (Direct Grants 4930062 and 4053105) and the US National Science Foundation (IIS 1161586 to J.T. and OCE-1232982 and DEB-1441717 to R.S.).

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H.L. conceived and designed the study. Y.H. performed the research. R.S. and J.T. contributed reagent and analytic tools. H.L., Y.H., R.S. and J.T. analysed the data. H.L. wrote the paper.

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Correspondence to Haiwei Luo.

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The authors declare no competing financial interests.

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Supplementary Methods, Supplementary Figures, Supplementary Table and Supplementary References. (PDF 8419 kb)

Supplementary Data

(1) Summary of simulation parameters used to estimate the dR/dC ratio based on charge classification of the 20 amino acids. (2) Summary of simulation parameters used to estimate the dR/dC ratio based on volume and polarity classification of the 20 amino acids. (XLSX 290 kb)

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Luo, H., Huang, Y., Stepanauskas, R. et al. Excess of non-conservative amino acid changes in marine bacterioplankton lineages with reduced genomes. Nat Microbiol 2, 17091 (2017). https://doi.org/10.1038/nmicrobiol.2017.91

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