Evolutionary Geography of Root Nodule Bacteria: Speciation Directed by the Host Plants

Abstract

Compared to free-living relatives, bacterial symbionts of plants exhibit higher rates of population diversification (microevolution), as well as of speciation and formation of super-species taxa (macroevolution). Analysis of rhizobia, the N2-fixing symbionts of leguminous plants, suggests that both evolutionary modes are determined by the hosts, which have mutagenic and recombinogenic effects on their microsymbionts, apart from activating the selective processes that determine the fate of newly emerged genotypes in their populations. Migration induced by leguminous plants plays a key role in the evolution of rhizobia, including: (1) joint movement of the symbionts and their hosts into new ecological zones and (2) local circulation of the symbionts in plant‒soil systems. In the first case, allopatric speciation occurs in rhizobia due to transfer of the symbiotically specialized (sym) genes from the introduced strains into local bacteria, which are transformed into novel symbionts. In the second case, a sympatric divergence of Rhizobium populations occurs, resulting in formation of intraspecies taxa (biovars and symbiovars) contrasting in their host ranges. In the evolutionarily advanced rhizobia, Rhizobium leguminosarum and Neorhizobium galegae interacting with galegoid legumes (tribes Fabeae, Galegae, and Trifolieae), these processes are associated with diversification of the sym genes representing the accessory genome parts due to the interaction between bacteria and the hosts differing in their symbiotic affinities. In parallel, formation of new cryptic (genomic) species was revealed in local rhizobia populations, which is associated with divergence of the core genome parts. It may be caused either by genetic drift or by selection for resistance against local edaphic stresses, which in combination with disruptive selection can sufficiently enhance the rhizobia diversity and change the structures of their pangenomes.