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ISME J. 2016 Jul;10(7):1589-601. doi: 10.1038/ismej.2015.241. Epub 2016 Jan 8.

Genome-wide selective sweeps and gene-specific sweeps in natural bacterial populations.

Author information

1
DOE Joint Genome Institute, Walnut Creek, CA, USA.
2
Department of Bacteriology, University of Wisconsin-Madison, Madison, WI, USA.
3
Department of Ecology and Genetics, Limnology and Science for Life Laboratory, Uppsala University, Uppsala, Sweden.
4
Department of Marine Sciences, University of Georgia, Athens, GA, USA.
5
Microbiology and Molecular Genetics, Michigan State University, East Lansing, MI, USA.
6
School of Freshwater Sciences, University of Wisconsin-Milwaukee, Milwaukee, WI, USA.
7
Civil and Environmental Engineering, University of Wisconsin-Madison, Madison, WI, USA.

Abstract

Multiple models describe the formation and evolution of distinct microbial phylogenetic groups. These evolutionary models make different predictions regarding how adaptive alleles spread through populations and how genetic diversity is maintained. Processes predicted by competing evolutionary models, for example, genome-wide selective sweeps vs gene-specific sweeps, could be captured in natural populations using time-series metagenomics if the approach were applied over a sufficiently long time frame. Direct observations of either process would help resolve how distinct microbial groups evolve. Here, from a 9-year metagenomic study of a freshwater lake (2005-2013), we explore changes in single-nucleotide polymorphism (SNP) frequencies and patterns of gene gain and loss in 30 bacterial populations. SNP analyses revealed substantial genetic heterogeneity within these populations, although the degree of heterogeneity varied by >1000-fold among populations. SNP allele frequencies also changed dramatically over time within some populations. Interestingly, nearly all SNP variants were slowly purged over several years from one population of green sulfur bacteria, while at the same time multiple genes either swept through or were lost from this population. These patterns were consistent with a genome-wide selective sweep in progress, a process predicted by the 'ecotype model' of speciation but not previously observed in nature. In contrast, other populations contained large, SNP-free genomic regions that appear to have swept independently through the populations prior to the study without purging diversity elsewhere in the genome. Evidence for both genome-wide and gene-specific sweeps suggests that different models of bacterial speciation may apply to different populations coexisting in the same environment.

PMID:
26744812
PMCID:
PMC4918448
DOI:
10.1038/ismej.2015.241
[Indexed for MEDLINE]
Free PMC Article

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