Phylogenomic Rhizobium Species Are Structured by a Continuum of Diversity and Genomic Clusters

Abstract

The bacterial genus Rhizobium comprises diverse symbiotic nitrogen-fixing species associated with the roots of plants in the Leguminosae family. Multiple genomic clusters defined by whole genome comparisons occur within Rhizobium , but their equivalence to species is controversial. In this study we investigated such genomic clusters to ascertain their significance in a species phylogeny context. Phylogenomic inferences based on complete sets of ribosomal proteins and stringent core genome markers revealed the main lineages of Rhizobium . The clades corresponding to R. etli and R. leguminosarum species show several genomic clusters with average genomic nucleotide identities (ANI > 95%), and a continuum of divergent strains, respectively. They were found to be inversely correlated with the genetic distance estimated from concatenated ribosomal proteins. We uncovered evidence of a Rhizobium pangenome that was greatly expanded, both in its chromosomes and plasmids. Despite the variability of extra-chromosomal elements, our genomic comparisons revealed only a few chromid and plasmid families. The presence/absence profile of genes in the complete Rhizobium genomes agreed with the phylogenomic pattern of species divergence. Symbiotic genes were distributed according to the principal phylogenomic Rhizobium clades but did not resolve genome clusters within the clades. We distinguished some types of symbiotic plasmids within Rhizobium that displayed different rates of synonymous nucleotide substitutions in comparison to chromosomal genes. Symbiotic plasmids may have been repeatedly transferred horizontally between strains and species, in the process displacing and substituting pre-existing symbiotic plasmids. In summary, the results indicate that Rhizobium genomic clusters, as defined by whole genomic identities, might be part of a continuous process of evolutionary divergence that includes the core and the extrachromosomal elements leading to species formation.

Host‐specific competitiveness to form nodules in Rhizobium leguminosarum symbiovar viciae

“…These two new genospecies gsF‐1 and gsF‐2 include respectively the R. leguminosarum strain TOM (Firmin et al , ; 5 strains) and the strain R. laguerreae FB206 (Saïdi et al , ; 3 strains). The last two strains (CZP3G4 and SEF4G12) display only low genomic similarities with R. leguminosarum bacteria (88% < ANI < 89%) but are further distinct from other Rhizobium species (González et al , ).…”

Exploring the evolutionary dynamics of Rhizobium plasmids through bipartite network analysis

“…There is no universally conserved gene among all Rhizobium plasmids used to construct their single phylogeny. In spite of this, two genetic markers, repABC operon and conjugative relaxase (MOB), are usually adopted to define the phylogenetic relationship of plasmids (Fernandez‐Lopez et al ., ; González et al ., ). The repABC operon is widely conserved among α‐proteobacteria and the MOB gene provides a robust, universal evolutionary marker for only mobilizable and conjugative plasmids.…”

“…Comparatively, the accessory plasmids have gained limited attention and experimental investigations have been difficult to perform because of their high variability and ability to easily exchange genetic material between and within species (Dresler‐Nurmi et al ., ). Although some studies have been conducted comparing the rhizobial replicons based on their genomic content, traditional technologies of phylogenetics and phylogenomics have limited applicability in the study of the evolutionary relationships and boundaries of these coexisting plasmids due to an absence of universal plasmid genes (González et al ., , ; Orlandini et al ., ; Pérez Carrascal et al ., ; Orlek et al ., ).…”

Bacillus velezensis 83 a bacterial strain from mango phyllosphere, useful for biological control and plant growth promotion

“…Genome analysis was performed following the standard methodology described in González et al ( 2019 ). In short, the pangenome model was obtained with the Bacterial Pangenome Analysis program (BPGA), by setting the USEARCH clustering algorithm to the default values (the minimal identity of 50% and 20 combinations) (Chaudhari et al 2016 ).…”