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. 2005 Nov 1;102(44):15924-9.
doi: 10.1073/pnas.0507944102. Epub 2005 Oct 25.

Adaptation and incipient sympatric speciation of Bacillus simplex under microclimatic contrast at "Evolution Canyons" I and II, Israel

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Adaptation and incipient sympatric speciation of Bacillus simplex under microclimatic contrast at "Evolution Canyons" I and II, Israel

Johannes Sikorski et al. Proc Natl Acad Sci U S A. .

Abstract

The microevolutionary dynamics of prokaryotes in natural habitats, such as soil, is poorly understood in contrast to our increasing knowledge on their immense diversity. We performed microevolutionary analyses on 945 soil isolates of Bacillus simplex from "Evolution Canyons" I (Carmel, Israel) and II (Galilee, Israel). These canyons represent similar ecological replicates, separated by 40 km, with highly contrasting interslope abiotic and biotic conditions in each (within a distance of only 100-400 m). Strains representing genetic groups were identical in their 16S sequences, suggesting high genetic similarity and monophyletic origin. Parallel and nested phylogenetic structures correlated with ecological contrasts rather than geographical distance. Additionally, slope-specific populations differed substantially in their diversity. The levels of DNA repair (determined by UV sensitivity) and spontaneous mutation rate (resistance to rifampicin) relate to ecological stress and phylogeny. Altogether, the results suggest adaptive radiation at a microscale. We discuss the observed adaptive population structures in the context of incipient sympatric speciation in soil bacteria. We conclude that, despite different biology, prokaryotes, like sexually reproducing eukaryotes, may consist of true species and parallel ecological speciation in eukaryotes.

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Figures

Fig. 1.
Fig. 1.
Evolutionary lineages in the metapopulation of B. simplex and their physiological properties of UV survival and mutation rate. (a) Neighbor-joining tree (Jukes–Cantor distances) from RAPD data of all isolates. Thin horizontal lines to the right of the tree indicate origin from African-like slope (SFS, red), valley bottom (VB, black), and European-like slope (NFS, blue). For each lineage, six characteristic values are given and denoted with the numbers of strains (i), the ECI/ECII ratio of strains (ii), the ratio of African-like to European-like strains (iii), the ratio of isolates to haplotypes (iv), the genetic diversity given as mean number of pairwise differences of the RAPD sequence (v), and the variance of RAPD pattern diversity (vi). The depicted RAPD clusters are supported by unweighted pair group method with arithmetic mean and maximum parsimony analyses (data not shown). (b) Representative RAPD cluster strains chosen from both canyons and their phylogenies of portions of the gapA, pgk, and uvrA genes. Names of the strains reflect their origin and are explained in Supporting Materials and Methods. The 16S sequence was determined from strains marked with an arrow. The phylogenetic trees were reconstructed from the results of neighbor-joining, minimum evolution, maximum parsimony, and maximum likelihood analyses of the gene sequences. Only nodes that were unambiguously resolved in the same way in all four reconstruction methods are shown. Divergence values are given in Table 5, which is published as supporting information on the PNAS web site. Outgroup sequences (which are not shown) were obtained from Bacillus subtilis, Bacillus cereus, Bacillus halodurans, Bacillus licheniformis, and Oceanobacillus iheyiensis. (c) Phylogenetic tree of ecological genomic evolutionary lineages summarizing the results from the gene tree topologies and of the RAPD tree. (d and e) UV-C survival (percentage) (d) and spontaneous mutation rates to rifampicin resistance of representative isolates from the evolutionary lineages A-E (e). Experiments were done twice, and results are given as mean and deviation from the mean.
Fig. 2.
Fig. 2.
Genomic divergence of B. simplex across and within two ECs, as estimated from pairwise station comparisons of RAPD data within slopes (n = 3) (columns a–d), between slopes of same ecology but different canyon (n = 9) (columns e and f), and of interslope stations within canyons (n = 9) (columns g and h). Open circles indicate a pairwise station comparison; bars indicate the mean of all pairwise station comparisons. I and II denote ECI and ECII, respectively; and A and E denote African-like and European-like slopes, respectively. The P values (Mann–Whitney U test) between the indicated columns are as follows: a–e, P = 0.100; c–e, P = 0.482; b–f, P = 0.372; d–f, P = 0.036; a–g, b–g, c–g, d–g, a–h, b–h, c–h, and d–h, P < 0.0001; e–g, P = 0.018; f–g, P = 0.003; e–h and f–h, P < 0.0001.
Fig. 3.
Fig. 3.
Genomic diversity of B. simplex in stations of ECI and ECII and of shady (s) and sunny (o) microniches on ECI. Black denotes stations 5–7 of European-like slopes; gray denotes valley bottom station 4; and white denotes stations 1–3 of the African-like slopes.

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