Rhizobium leguminosarum has two high-affinity Mn2+transport systems encoded by sitABCD and mntH. In symbiosis, sitABCD and mntH were expressed throughout nodules and also strongly induced in Mn2+-limited cultures of free-living cells. Growth of a sitA mntH double mutant was severely reduced under Mn2+limitation and sitA and mntH single mutants were more sensitive to oxidative stress. The double sitA mntH mutant of R. leguminosarum was unable to fix nitrogen (Fix-) with legumes belonging to the galegoid clade (Pisum sativum, Vicia faba and Vicia hirsuta). The presence of infection thread-like structures and sparsely-packed plant cells in nodules suggest that bacteroid development was blocked, either at a late stage of infection thread progression or during bacteroid-release. In contrast, a double sitA mntH mutant was Fix+on common bean (Phaseoli vulgaris), a member of the phaseoloid clade of legumes, indicating a host-specific symbiotic requirement for Mn2+transport.