Symbiosis islands of Loteae-nodulating Mesorhizobium comprise three radiating lineages with concordant nod gene complements and nodulation host-range groupings

Abstract

Mesorhizobiumis 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).Mesorhizobiumstrains that nodulateLotusspp. have been divided into host-range groupings. Group I (GI) strains nodulateL. corniculatusandL. japonicusecotype Gifu, while group II (GII) strains have a broader host range, which includesL. pedunculatus. To identify the basis of this extended host range, and better understandMesorhizobiumand ICESym genomics, the genomes of eightMesorhizobiumstrains were completed using hybrid long- and short-read assembly. Bioinformatic comparison with previously sequenced mesorhizobia genomes indicated host range was not predicted byMesorhizobiumgenospecies but rather by the evolutionary relationship between ICESym symbiotic regions. Three radiating lineages of Loteae ICESyms were identified on this basis, which correlate withLotusspp. host-range grouping and have lineage-specificnodgene 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 –nodboxes – identified 21 branches across the NodD regulons. Four of these branches were associated with seven genes unique to the five GII ICESyms. Thenodboxes preceding the host-range genenodZin GI and GII ICESyms were disparate, suggesting regulation ofnodZmay differ between GI and GII ICESyms. The broad host-range determinant(s) of GII ICESyms that confer nodulation ofL. pedunculatusare likely present amongst the 53 GII-unique genes identified.