Abstract
Mesorhizobium is a genus of soil bacteria, some isolates of which form an endosymbiotic relationship with diverse legumes of the Loteae tribe. The symbiotic genes of these mesorhizobia are generally carried on integrative and conjugative elements termed symbiosis islands (ICESyms). Mesorhizobium strains that nodulate Lotus spp. have been divided into host-range groupings. Group I (GI) strains nodulate L. corniculatus and L. japonicus ecotype Gifu, while group II (GII) strains have a broader host range, which includes L. pedunculatus. To identify the basis of this extended host range, and better understand Mesorhizobium and ICESym genomics, the genomes of eight Mesorhizobium strains were completed using hybrid long- and short-read assembly. Bioinformatic comparison with previously sequenced mesorhizobia genomes indicated host range was not predicted by Mesorhizobium genospecies but rather by the evolutionary relationship between ICESym symbiotic regions. Three radiating lineages of Loteae ICESyms were identified on this basis, which correlate with Lotus spp. host-range grouping and have lineage-specific nod gene complements. Pangenomic analysis of the completed GI and GII ICESyms identified 155 core genes (on average 30.1 % of a given ICESym). Individual GI or GII ICESyms carried diverse accessory genes with an average of 34.6 % of genes unique to a given ICESym. Identification and comparative analysis of NodD symbiotic regulatory motifs – nod boxes – identified 21 branches across the NodD regulons. Four of these branches were associated with seven genes unique to the five GII ICESyms. The nod boxes preceding the host-range gene nodZ in GI and GII ICESyms were disparate, suggesting regulation of nodZ may differ between GI and GII ICESyms. The broad host-range determinant(s) of GII ICESyms that confer nodulation of L. pedunculatus are likely present amongst the 53 GII-unique genes identified.
Highlights
The genus Mesorhizobium encompasses a group of ubiquitous saprophytic soil bacteria
Ten Mesorhizobium strains with well-defined nodulation host ranges were selected for detailed functional genomic comparison: five Group I (GI) strains that nodulate L. corniculatus but only formed uninfected nodule primordia on L. pedunculatus, and five group II (GII) strains that nodulate both L. corniculatus and L. pedunculatus effectively (Table 1)
Completion of GI and GII Lotus-nodulating Mesorhizobium genome sequences allowed extraction of contiguous ICESym regions for exhaustive structural and pangenomic analysis. Comparison of their ICESyms using a host-range framework identified a pattern of evolutionary relatedness, which described the origin and possible genetic basis for the expanded host range conferred by GII ICESyms, which was not apparent from comparison of their complete genome sequences
Summary
The genus Mesorhizobium encompasses a group of ubiquitous saprophytic soil bacteria. Mesorhizobia can evolve the ability to engage in nitrogen-fixing endosymbiosis with leguminous plants of the genus Lotus via the horizontal acquisition of a genetic element termed a symbiosis island [1, 2]. Symbiosis islands (ICESyms) are a specific phenotypic category of integrative and conjugative element, which carry the genes necessary for symbiotic signalling and nitrogen fixation [3,4,5]. ICESyms have been shown to transfer in the environment, resulting in the acquisition of symbiotic potential by native Mesorhizobium populations [1, 2, 6]. ICESym fitness is dictated by the success of the mesorhizobia in which it resides in the soil microbial community. ICESym transfer to saprophytic mesorhizobia followed by clonal expansion
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