Population genomics of Vibrionaceae isolated from an endangered oasis reveals local adaptation after an environmental perturbation

Abstract

Background: In bacteria, pan-genomes are the result of an evolutionary "tug of war" between selection and horizontal gene transfer (HGT). High rates of HGT increase the genetic pool and the effective population size (N_e), resulting in open pan-genomes. In contrast, selective pressures can lead to local adaptation by purging the variation introduced by HGT and mutation, resulting in closed pan-genomes and clonal lineages. In this study, we explored both hypotheses, elucidating the pan-genome of Vibrionaceae isolates after a perturbation event in the endangered oasis of Cuatro Ciénegas Basin (CCB), Mexico, and looking for signals of adaptation to the environments in their genomes.

Results: We obtained 42 genomes of Vibrionaceae distributed in six lineages, two of them did not showed any close reference strain in databases. Five of the lineages showed closed pan-genomes and were associated to either water or sediment environment; their high N_e estimates suggest that these lineages are not from a recent origin. The only clade with an open pan-genome was found in both environments and was formed by ten genetic groups with low N_e, suggesting a recent origin. The recombination and mutation estimators (r/m) ranged from 0.005 to 2.725, which are similar to oceanic Vibrionaceae estimations. However, we identified 367 gene families with signals of positive selection, most of them found in the core genome; suggesting that despite recombination, natural selection moves the Vibrionaceae CCB lineages to local adaptation, purging the genomes and keeping closed pan-genome patterns. Moreover, we identify 598 SNPs associated with an unstructured environment; some of the genes associated with these SNPs were related to sodium transport.

Conclusions: Different lines of evidence suggest that the sampled Vibrionaceae, are part of the rare biosphere usually living under famine conditions. Two of these lineages were reported for the first time. Most Vibrionaceae lineages of CCB are adapted to their micro-habitats rather than to the sampled environments. This pattern of adaptation is concordant with the association of closed pan-genomes and local adaptation.

Keywords: Effective population size; Pan-genome; Population genomics; Recombination; Selection; Vibrionaceae.

Fig. 1

Study site, Pozas Rojas in Los Hundidos within Cuatro Ciénegas Basin, Mexico. Sampling sites are signaled in yellow. Cuatro Ciénegas location is also shown in a map (Pozas Rojas photos were provided by David Jaramillo, a map showing the location of Cuatro Ciénegas Valley was obtained from Google Earth, earth.google.com/web/)

Fig. 2

Core gene phylogeny of the 1254 orthologs. Maximum-likelihood phylogenetic reconstruction of core genes, supporting branch values are shown. Each square represents the isolation environment, water or sediment, while yellow stars indicate reference strains. Isolation pond is indicated by its number. Clades are distinguished with colors. Clades IV and V which are likely to be exclusive to CCB are highlighted with an asterisk

Fig. 3

Patterns of recombination events among isolated strains. Heatmap of the frequency of recombination events among different strains; red colors indicate more recombination events within strains while blue events indicate few recombination events. Distances were estimated with the Jaccard dissimilarity index

Fig. 4

UPGMA of the 598 SNPs associated with the isolation environment. Tip colors represent clade membership, for Clade II, Sub-clades are also indicated. Squares represent the isolation environment. Distances were calculated with the bitwise distance function of poppr v2.8.1