Metapopulation dominance and genomic-island acquisition ofBradyrhizobiumwith superior catabolic capabilities

Abstract

Root nodule-forming rhizobia exhibit a bipartite lifestyle, replicating in soil and also within plant cells where they fix nitrogen for legume hosts. Host control models posit that legume hosts act as a predominant selective force on rhizobia, but few studies have examined rhizobial fitness in natural populations. Here, we genotyped and phenotyped Bradyrhizobium isolates across more than 800 km of the native Acmispon strigosus host range. We sequenced chromosomal genes expressed under free-living conditions and accessory symbiosis loci expressed in planta and encoded on an integrated 'symbiosis island' (SI). We uncovered a massive clonal expansion restricted to the Bradyrhizobium chromosome, with a single chromosomal haplotype dominating populations, ranging more than 700 km, and acquiring 42 divergent SI haplotypes, none of which were spatially widespread. For focal genotypes, we quantified utilization of 190 sole-carbon sources relevant to soil fitness. Chromosomal haplotypes that were both widespread and dominant exhibited superior growth on diverse carbon sources, whereas these patterns were not mirrored among SI haplotypes. Abundance, spatial range and catabolic superiority of chromosomal, but not symbiosis genotypes suggests that fitness in the soil environment, rather than symbiosis with hosts, might be the key driver of Bradyrhizobium dominance.

Legumes versus rhizobia: a model for ongoing conflict in symbiosis

“…Some rhizobia produce a cocktail of NFs that gives them access to diverse host species in which they frequently fix little or no nitrogen (Pueppke & Broughton, ). Other genotypes of rhizobia dominate host nodules and rhizospheres through mechanisms correlated with antibiotic resistance and catabolic flexibility, which can promote persistence in the soil (Hollowell et al ., , ,b). Finally, some rhizobia evade host control over nodulation specificity by hitchhiking into the nodule alongside NF‐secreting strains without themselves having any of the genes to encode NFs (Gano‐Cohen et al ., ).…”

Interspecific conflict and the evolution of ineffective rhizobia

“…; Hollowell et al . ). Phylogenetic relationships among isolates were reconstructed using the CHR and SI loci with PhyML 3.0 utilising a BioNJ starting tree and subtree pruning and regrafting (Guindon et al .…”

“…The CHR and SI genome regions were analysed separately because the SI can be horizontally transferred (Hollowell et al . ). For each isolate and for each genome region, genotype frequency was calculated as the proportion of isolates from the sampled population that were identified as the focal genotype (Hollowell et al .…”

“…Bradyrhizobium isolates were collected from six A. strigosus populations across California that exhibit diverged Bradyrhizobium communities (Hollowell et al . ,b) and experience ~ 10‐fold variation in soil nitrogen concentrations, driven by anthropogenic nitrogen deposition over the last 70+ years (Regus et al . , ; Wendlandt et al .…”

Novel model‐based clustering reveals ecologically differentiated bacterial genomes across a large climate gradient

“…We delineate ecological differentiation using whole‐genome data of a widely distributed symbiotic nitrogen‐fixing soil bacteria ( Bradyrhizobium japonicum ) which associates with an endemic host legume ( Acacia acuminata ), spanning a climate gradient along a large heterogeneous geographical region in south‐western Australia. Previous studies have identified significant effects of soil chemistry, moisture content, and host demography on rhizobial abundance, diversity and fitness (Thrall et al , ; Hollowell et al ; van Ham et al ; Vuong et al ; Birnbaum et al ; Dinnage et al ), as well as host‐rhizobial co‐adaptation (Barrett et al ) and geographical variation in the functional outcomes of host–rhizobial interactions (Thrall et al ; Barrett et al ). Dispersal limitation has also been identified in Bradyrhizobium (Bissett et al ).…”