title: Genome-wide selective sweeps and gene-specific sweeps in natural bacterial populations.
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.
authors.affiliation: DOE Joint Genome Institute, Walnut Creek, CA, USA.
authors.forename: Matthew L
authors.initials: ML
authors.lastname: Bendall
authors.affiliation: Department of Bacteriology, University of Wisconsin-Madison, Madison, WI, USA.
authors.forename: Sarah Lr
authors.initials: SL
authors.lastname: Stevens
authors.affiliation: DOE Joint Genome Institute, Walnut Creek, CA, USA.
authors.forename: Leong-Keat
authors.initials: LK
authors.lastname: Chan
authors.affiliation: DOE Joint Genome Institute, Walnut Creek, CA, USA.
authors.forename: Stephanie
authors.initials: S
authors.lastname: Malfatti
authors.affiliation: DOE Joint Genome Institute, Walnut Creek, CA, USA.
authors.forename: Patrick
authors.initials: P
authors.lastname: Schwientek
authors.affiliation: DOE Joint Genome Institute, Walnut Creek, CA, USA.
authors.forename: Julien
authors.initials: J
authors.lastname: Tremblay
authors.affiliation: DOE Joint Genome Institute, Walnut Creek, CA, USA.
authors.forename: Wendy
authors.initials: W
authors.lastname: Schackwitz
authors.affiliation: DOE Joint Genome Institute, Walnut Creek, CA, USA.
authors.forename: Joel
authors.initials: J
authors.lastname: Martin
authors.affiliation: DOE Joint Genome Institute, Walnut Creek, CA, USA.
authors.forename: Amrita
authors.initials: A
authors.lastname: Pati
authors.affiliation: DOE Joint Genome Institute, Walnut Creek, CA, USA.
authors.forename: Brian
authors.initials: B
authors.lastname: Bushnell
authors.affiliation: DOE Joint Genome Institute, Walnut Creek, CA, USA.
authors.forename: Jeff
authors.initials: J
authors.lastname: Froula
authors.affiliation: DOE Joint Genome Institute, Walnut Creek, CA, USA.
authors.forename: Dongwan
authors.initials: D
authors.lastname: Kang
authors.affiliation: DOE Joint Genome Institute, Walnut Creek, CA, USA.
authors.forename: Susannah G
authors.identifier: 0000-0001-6479-8427
authors.initials: SG
authors.lastname: Tringe
authors.affiliation: Department of Ecology and Genetics, Limnology and Science for Life Laboratory, Uppsala University, Uppsala, Sweden.
authors.forename: Stefan
authors.initials: S
authors.lastname: Bertilsson
authors.affiliation: Department of Marine Sciences, University of Georgia, Athens, GA, USA.
authors.forename: Mary A
authors.identifier: 0000-0002-0702-8167
authors.initials: MA
authors.lastname: Moran
authors.affiliation: Microbiology and Molecular Genetics, Michigan State University, East Lansing, MI, USA.
authors.forename: Ashley
authors.initials: A
authors.lastname: Shade
authors.affiliation: School of Freshwater Sciences, University of Wisconsin-Milwaukee, Milwaukee, WI, USA.
authors.forename: Ryan J
authors.initials: RJ
authors.lastname: Newton
authors.affiliation: Department of Bacteriology, University of Wisconsin-Madison, Madison, WI, USA.|Civil and Environmental Engineering, University of Wisconsin-Madison, Madison, WI, USA.
authors.forename: Katherine D
authors.initials: KD
authors.lastname: McMahon
authors.affiliation: DOE Joint Genome Institute, Walnut Creek, CA, USA.
authors.forename: Rex R
authors.initials: RR
authors.lastname: Malmstrom
mesh_terms: D001419:Bacteria / Q000145:classification / Q000235:genetics* / Q000302:isolation & purification; D005075:Biological Evolution; D005787:Gene Frequency; D014644:Genetic Variation; D016680:Genome, Bacterial / Q000235:genetics*; D056186:Metagenomics; D010802:Phylogeny; D020641:Polymorphism, Single Nucleotide