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.

Highlights

  • Fossil records indicate that life appeared in marine environments,3.5–3.8 billion years ago (Gyr) [1] and transitioned to terrestrial ecosystems,2.6 Gyr [2]

  • The lack of fossil records for bacteria makes it difficult to assess the timing of their transition to terrestrial environments; sequence analysis suggests that a large clade of prokaryotic phyla might have evolved on land as early as 3 Gyr, with some lineages later reinvading marine habitats [3]

  • Which genes does Azospirillum share with its aquatic relatives, and what is the origin of its additional genes? To answer this question, we developed a robust scheme for detecting ancestral and horizontally transferred (HGT) genes (Figure 3) using bioinformatics tools, classified most protein coding genes in the Azospirillum genomes as ancestral or horizontally transferred with quantified degrees of confidence (Figure 4A and Table S6)

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Summary

Introduction

Fossil records indicate that life appeared in marine environments ,3.5–3.8 billion years ago (Gyr) [1] and transitioned to terrestrial ecosystems ,2.6 Gyr [2]. The lack of fossil records for bacteria makes it difficult to assess the timing of their transition to terrestrial environments; sequence analysis suggests that a large clade of prokaryotic phyla (termed ‘‘terrabacteria’’) might have evolved on land as early as 3 Gyr, with some lineages later reinvading marine habitats [3]. Bacteria of the genus Azospirillum are found primarily in terrestrial habitats, where they colonize roots of important cereals and other grasses and promote plant growth by several mechanisms including nitrogen fixation and phytohormone secretion [5,6]. Azospirillum belong to proteobacteria, one of the

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