Biogeography of the Sulfolobus islandicus pan-genome

doi:10.1073/pnas.0808945106

Biogeography of the Sulfolobus islandicus pan-genome

^aDepartment of Microbiology and
^bInstitute for Genomic Biology, University of Illinois at Urbana–Champaign, Urbana, IL 61801

Edited by Edward F. DeLong, Massachusetts Institute of Technology, Cambridge, MA, and approved April 2, 2009 (received for review September 8, 2008)

Abstract

Variation in gene content has been hypothesized to be the primary mode of adaptive evolution in microorganisms; however, very little is known about the spatial and temporal distribution of variable genes. Through population-scale comparative genomics of 7 Sulfolobus islandicus genomes from 3 locations, we demonstrate the biogeographical structure of the pan-genome of this species, with no evidence of gene flow between geographically isolated populations. The evolutionary independence of each population allowed us to assess genome dynamics over very recent evolutionary time, beginning ≈910,000 years ago. On this time scale, genome variation largely consists of recent strain-specific integration of mobile elements. Localized sectors of parallel gene loss are identified; however, the balance between the gain and loss of genetic material suggests that S. islandicus genomes acquire material slowly over time, primarily from closely related Sulfolobus species. Examination of the genome dynamics through population genomics in S. islandicus exposes the process of allopatric speciation in thermophilic Archaea and brings us closer to a generalized framework for understanding microbial genome evolution in a spatial context.

Footnotes

¹To whom correspondence should be addressed. E-mail: rwhitaker{at}life.uiuc.edu
Author contributions: R.J.W. designed research; R.J.W. performed research; M.L.R., C.J.F., P.V.B., and R.J.W. contributed new reagents/analytical tools; M.L.R., N.L.H., P.V.B., and R.J.W. analyzed data; and R.J.W. wrote the paper.
The authors declare no conflict of interest.
This article is a PNAS Direct Submission.
Data deposition: Genome sequences are available from the Department of Energy Joint Genome Institute, http://www.jgi.doe.gov. The complete genome sequences have been deposited in GenBank (accession nos. CP001399–CP001405). Annotations of genome dynamics reported here are available at www.life.illinois.edu/Sulfolobus_islandicus.
This article contains supporting information online at www.pnas.org/cgi/content/full/0808945106/DCSupplemental.