Incipient Sympatric Speciation and Evolution of Soil Bacteria Revealed by Metagenomic and Structured Non-Coding RNAs Analysis

SIMPLE SUMMARY: The microevolutionary dynamics of soil bacteria under microclimatic differences are largely unexplored in contrast to our improving knowledge of their vast diversity. In this study, we performed a comparative metagenomic analysis of two sharply divergent rocks and soil types at the Evolution Plateau (EP) in eastern Upper Galilee, Israel. We have identified the significant differences in bacterial taxonomic diversity, functions, and patterns of RNA-based gene regulation between the bacteria from two different soil types. Furthermore, we have identified several species with a significant genetic divergence of the same species between the two soil types, highlighting the soil bacteria’s incipient sympatric speciation. ABSTRACT: Soil bacteria respond rapidly to changes in new environmental conditions. For adaptation to the new environment, they could mutate their genome, which impacts the alternation of the functional and regulatory landscape. Sometimes, these genetic and ecological changes may drive the bacterial evolution and sympatric speciation. Although sympatric speciation has been controversial since Darwin suggested it in 1859, there are several strong theoretical or empirical evidences to support it. Sympatric speciation associated with soil bacteria remains largely unexplored. Here, we provide potential evidence of sympatric speciation of soil bacteria by comparison of metagenomics from two sharply contrasting abutting divergence rock and soil types (Senonian chalk and its rendzina soil, and abutting Pleistocene basalt rock and basalt soil). We identified several bacterial species with significant genetic differences in the same species between the two soil types and ecologies. We show that the bacterial community composition has significantly diverged between the two soils; correspondingly, their functions were differentiated in order to adapt to the local ecological stresses. The ecologies, such as water availability and pH value, shaped the adaptation and speciation of soil bacteria revealed by the clear-cut genetic divergence. Furthermore, by a novel analysis scheme of riboswitches, we highlight significant differences in structured non-coding RNAs between the soil bacteria from two divergence soil types, which could be an important driver for functional adaptation. Our study provides new insight into the evolutionary divergence and incipient sympatric speciation of soil bacteria under microclimatic ecological differences.