Biogeography of the Sulfolobus islandicus pan-genome

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 approximately 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.

Fig. 1.

Pairwise bANI for the 7 S. islandicus genomes. Comparisons between LNP (Lassen) strains (black), YNP (Yellowstone) strains (orange), and Mutnovsky strains (green) yield an average identity of 99.73%. Comparisons between North American strains (LNP vs. YNP, dark blue) give an average identity of 99.54%, whereas comparisons between each North American and Mutnovsky strain (magenta and light blue) yield an average identity of 98.89%.

Fig. 2.

Maximum parsimony phylogenies inferred from the concatenated core nucleotide genome (A) and presence/absence of gene content matrix (B). Numbers above each branch correspond to bootstrap support for that node in percentage. *, 100%; >, Mutnovsky subpopulation.

Fig. 3.

Physical map of genome dynamics for the L.S.2.15 genome. Rings are numbered beginning with the outer ring. Ring 1 shows the location of S. islandicus core (light gray) and noncore (dark gray) clusters. Ring 2 shows the locations of viral and plasmid homologs. Ring 3 shows the location of clusters whose distribution cannot be determined by parsimony criteria. Colors represent average pairwise nucleotide identity within each cluster, ranging from less than 70% to greater than 95%, as shown in legend to the left. Ring 4 shows designations of gene gain by L.S.2.15 (red), gene loss by any other strain or group of strains (blue), and multiple events (orange) (e.g., gain by North American ancestor followed by loss in L.D.8.5). Innermost arcs denote the location of the variable region.

Fig. 4.

Tally of genome dynamics by strains and populations. Gene gain (red), gene loss (blue), and net change (gain − loss; gray). Strain names are abbreviated as follows: L1, L.D.8.5; L2, L.S.2.15; M1, M.14.25; M2, M.16.27; M3, M.16.4; Y1, Y.G.57.14; Y2, Y.N.15.51; L, Lassen; Y, Yellowstone; M, Mutnovsky; M-sub, Mutnovsky subpopulation; NA, North America.