Recombination Shapes the Natural Population Structure of the Hyperthermophilic Archaeon Sulfolobus islandicus

Abstract

Although microorganisms make up the preponderance of the biodiversity on Earth, the ecological and evolutionary factors that structure microbial populations are not well understood. We investigated the genetic structure of a thermoacidophilic crenarchaeal species, Sulfolobus islandicus, using multilocus sequence analysis of six variable protein-coding loci on a set of 60 isolates from the Mutnovsky region of Kamchatka, Russia. We demonstrate significant incongruence among gene genealogies and a lack of association between alleles consistent with recombination rates greater than the rate of mutation. The observation of high relative rates of recombination suggests that the structure of this natural population does not fit the periodic selection model often used to describe populations of asexual microorganisms. We propose instead that frequent recombination among closely related individuals prevents periodic selection from purging diversity and provides a fundamental cohesive mechanism within this and perhaps other archaeal species.

Biogeography of theSulfolobus islandicuspan-genome

“…Strains were chosen to represent different geothermal areas within LNP and YNP, as shown in Table 1. Mutnovsky strains were chosen to represent parental and recombinant members of the population, as described by Whitaker et al (72). Each genome was sequenced by the Department of Energy (DOE) Joint Genome Institute through standard Sanger sequencing methods.…”

Microbial Speciation

“…Such a rapid drop in frequency should limit efficient exchange of DNA to closely related genomes, as expected within genotypic clusters, and might play a role in maintaining the cohesion of clusters. Although such relationships have been shown for several, divergent groups of bacteria, in some archaea, the requirement for short, identical DNA stretches seems to be absent (Grogan and Stengel 2008;Naor et al 2012), even though environmental observations support decreased rates of recombination across clusters (Whitaker et al 2005;Williams et al 2012). Moreover, recent comparison of very closely related genomes has also shown that very little sequence similarity appears to be required for integration of long stretches of highly divergent DNA (including single nucleotide changes and structural variants) into the genome (Mell et al 2011;Cordero et al 2012a), although the mechanisms remain unclear.…”

Genome dynamics in a natural archaeal population

“…Subsequently, MLST-based analyses provided evidence for genetic recombination in the halophilic archaeon Halorubrum sp (25) and the thermoacidophilic archaeon Sulfolobus islandicus (7). Results documenting recombination in F. acidarmanus suggest that mosaic genome structure may be a common feature of natural archaeal populations.…”