Azospirillum Genomes Reveal Transition of Bacteria from Aquatic to Terrestrial Environments

Abstract

Fossil records indicate that life appeared in marine environments ∼3.5 billion years ago (Gyr) and transitioned to terrestrial ecosystems nearly 2.5 Gyr. Sequence analysis suggests that “hydrobacteria” and “terrabacteria” might have diverged as early as 3 Gyr. Bacteria of the genus Azospirillum are associated with roots of terrestrial plants; however, virtually all their close relatives are aquatic. We obtained genome sequences of two Azospirillum species and analyzed their gene origins. While most Azospirillum house-keeping genes have orthologs in its close aquatic relatives, this lineage has obtained nearly half of its genome from terrestrial organisms. The majority of genes encoding functions critical for association with plants are among horizontally transferred genes. Our results show that transition of some aquatic bacteria to terrestrial habitats occurred much later than the suggested initial divergence of hydro- and terrabacterial clades. The birth of the genus Azospirillum approximately coincided with the emergence of vascular plants on land. Genome sequencing and analysis of plant-associated beneficial soil bacteria Azospirillum spp. reveals that these organisms transitioned from aquatic to terrestrial environments significantly later than the suggested major Precambrian divergence of aquatic and terrestrial bacteria. Separation of Azospirillum from their close aquatic relatives coincided with the emergence of vascular plants on land. Nearly half of the Azospirillum genome has been acquired horizontally, from distantly related terrestrial bacteria. The majority of horizontally acquired genes encode functions that are critical for adaptation to the rhizosphere and interaction with host plants.