Mobile genetic elements shape the evolution of wild bacterial pangenomes in the face of biotic and abiotic selective pressures in the soil

Mobile genetic elements (MGEs) provide a critical reservoir of diversity that potentiates bacterial local adaptation. However, the degree to which natural populations of MGEs and the chromosomes that host them share congruent or divergent evolutionary histories remains an open question. MGE and host chromosome phylogenies could show congruence or independence, depending on rates of MGE gain and loss, costs and benefit of MGE carriage, compatibility, and gene flow. We investigated phylogenetic congruence for two critical niche-expanding MGEs and host chromosomes using 302 genomes of wild symbiotic nitrogen-fixing Mesorhizobium bacteria. The MGEs comprise: 1) a nickel resistance island (NRI), which confers adaptation to nickel-enriched serpentine soils across replicated natural populations, and 2) a more extensive symbiosis island (SI), which enables symbiotic nitrogen fixation with a host legume. We demonstrate that the NRI, like the SI, is transmissible and its acquisition confers nickel adaptation. NRI acquisition often incurs no detectable cost, consistent with conditional neutrality during MGE-mediated adaptation. Phylogenies for the NRI, SI, and chromosome are congruent across wild strains, consistent with a history of vertical co-inheritance and/or MGE transmission primarily among close relatives. This congruence does not appear to result from barriers to gene flow, as diverse MGE and host chromosome haplotypes are broadly distributed and co-occur. Thus, despite ample ecological opportunity for admixture, distant relatives rarely transmitted MGEs, consistent with selection to maintain co-adapted genomic compartments. The SI has stronger phylogenetic congruence with the chromosome than does the smaller NRI, supporting the hypothesis that MGE complexity limits horizontal transfer among more divergent lineages. However, rare horizontal NRI transmission events among distant relatives and NRI loss appear to occur when haplotypes migrate across environments. Thus, environmentally dependent selection on migrants may periodically disrupt co-adapted MGE and chromosome haplotypes and serve as an engine of diversity.