Primary and Secondary Rhizobia: Major Stages in Evolution of Nitrogen-Fixing Symbiosis

Nodule bacteria (rhizobia) represent the highly developed model for the evolutionary genetics of symbiotic microorganisms. We propose to divide these polyphyletically originated bacteria into two groups that have arisen through: a) genomic rearrangements in free-living N-2-fixers (primary rhizobia originated via the phyletic evolution strategy); b) transfer of symbiotically specialized (sym) genes from rhizobia to various soil and plant-associated bacteria (secondary rhizobia originated via the reticular evolution strategy). Primary rhizobia are represented by genus Bradyrhizobium close to Rhodopsedomonas. Transformation of these phototrophic N-2-fixers into plant symbionts is evidenced by transitional (ancestral) Bradyrhizobium genotypes that combine the legume nodulation with photosynthesis. A crucial stage in rhizobia evolution was represented by acquisition of the ability to produce lipochitooligosaccharide Nod factors (NFs) eliciting the nodule development. Acquisition of NF synthesis allowed the ancestral Bradyrhizobium strains to switch from autotrophy to assimilation of the plant photosynthesis products resulted in heterotrophic bradyrhizobia (e.g., B. japonicum, B. elkanii) harboring sym genes in chromosomes. The best studied secondary rhizobia are represented by the Rhizobiaceae (Rhizobium, Sinorhizobium, Neorhizobium) species in which sym genes are located in mobile plasmids or chromids. Interactions of these species with legumes may be addressed as altruistic symbiosis based on development of non-reproducible bacteroids which supply hosts with N compounds. Since the rhizobia evolution involves the "gain-and-loss" genetic strategy, constructing highly active strains for legume crop inoculation should be based on activation of positive regulators of symbiotic N-2 fixation and on inactivation of its negative regulators.