Structured Populations of Sulfolobus acidocaldarius with Susceptibility to Mobile Genetic Elements

Abstract

The impact of a structured environment on genome evolution can be determined through comparative population genomics of species that live in the same habitat. Recent work comparing three genome sequences of Sulfolobus acidocaldarius suggested that highly structured, extreme, hot spring environments do not limit dispersal of this thermoacidophile, in contrast to other co-occurring Sulfolobus species. Instead, a high level of conservation among these three S. acidocaldarius genomes was hypothesized to result from rapid, global-scale dispersal promoted by low susceptibility to viruses that sets S. acidocaldarius apart from its sister Sulfolobus species. To test this hypothesis, we conducted a comparative analysis of 47 genomes of S. acidocaldarius from spatial and temporal sampling of two hot springs in Yellowstone National Park. While we confirm the low diversity in the core genome, we observe differentiation among S. acidocaldarius populations, likely resulting from low migration among hot spring "islands" in Yellowstone National Park. Patterns of genomic variation indicate that differing geological contexts result in the elimination or preservation of diversity among differentiated populations. We observe multiple deletions associated with a large genomic island rich in glycosyltransferases, differential integrations of the Sulfolobus turreted icosahedral virus, as well as two different plasmid elements. These data demonstrate that neither rapid dispersal nor lack of mobile genetic elements result in low diversity in the S. acidocaldarius genomes. We suggest instead that significant differences in the recent evolutionary history, or the intrinsic evolutionary rates, of sister Sulfolobus species result in the relatively low diversity of the S. acidocaldarius genome.

Keywords: Sulfolobus species; genome divergence; geothermal habitat; immigration; pangenome; population dynamics.

Fig. 1.—

Clonal phylogeny with large genomic insertions and deletions. (A) Phylogenetic tree constructed by concatenating SNPs identified in the core genome. The colored lines of the tree indicate each of the five clades we identified among the Sulfolobus acidocaldarius genomes isolated in 2012. Leaves are color-coded according to the hot spring from which they were isolated. Circles to the right of leaves indicate the presence or absence of genomic islands. First column; glycosyltransferase island; second column, STIV; third and fourth columns, plasmids 1 and 2, respectively. The colors in the glycosyltransferase island correspond to the deletion patterns shown in part (B). Trees were visualized using the interactive tree of life (ITOL) program (itol.embl.de). (B) Complete open reading frames found in the large genomic island encoding glycosyltransferases. We observed six different deletion patterns in this genomic island; the letters to the left indicate the designated deletion pattern. These correspond to the deletion pattern letters shown in supplementary table S7, Supplementary Material online. The numbers at the top indicate the ORF number of the ORF in S. acidocaldarius DSM639, with “Saci_” preceding the number in the ORF label. These genes are described in supplementary table S6, Supplementary Material online. Purple: glycosyltransferases, yellow: membrane proteins, light blue: methyltransferases, green: cell envelope, surface polysaccharides and lipopolysaccharides, orange: metabolite transport-related protein, gray: hypothetical protein.

Fig. 2.—

Map of chromosome features for genome GG12_C01_01 and NG05B_C06_03. Outer ring: location of single nucleotide polymorphisms (SNPs) in the core genome. Middle ring: location of small insertions and deletions (indels) in the core genome. Inner ring: large insertions (>100 bp) relative to Sulfolobus acidocaldarius DSM 639. The width of the green line represents the size of the insertion, with a minimum line width of 0.25 pt.