Biogeographical Patterns of Legume-Nodulating Burkholderia spp.: from African Fynbos to Continental Scales

Abstract

Rhizobia of the genus Burkholderia have large-scale distribution ranges and are usually associated with South African papilionoid and South American mimosoid legumes, yet little is known about their genetic structuring at either local or global geographic scales. To understand variation at different spatial scales, from individual legumes in the fynbos (South Africa) to a global context, we analyzed chromosomal (16S rRNA, recA) and symbiosis (nifH, nodA, nodC) gene sequences. We showed that the global diversity of nodulation genes is generally grouped according to the South African papilionoid or South American mimosoid subfamilies, whereas chromosomal sequence data were unrelated to biogeography. While nodulation genes are structured on a continental scale, a geographic or host-specific distribution pattern was not detected in the fynbos region. In host range experiments, symbiotic promiscuity of Burkholderia tuberum STM678 T and B. phymatum STM815 T was discovered in selected fynbos species. Finally, a greenhouse experiment was undertaken to assess the ability of mimosoid (Mimosa pudica) and papilionoid (Dipogon lignosus, Indigofera filifolia, Macroptilium atropurpureum, and Podalyria calyptrata) species to nodulate in South African (fynbos) and Malawian (savanna) soils. While the Burkholderia-philous fynbos legumes (D. lignosus, I. filifolia, and P. calyptrata) nodulated only in their native soils, the invasive neotropical species M. pudica did not develop nodules in the African soils. The fynbos soil, notably rich in Burkholderia, seems to retain nodulation genes compatible with the local papilionoid legume flora but is incapable of nodulating mimosoid legumes that have their center of diversity in South America. IMPORTANCEThis study is the most comprehensive phylogenetic assessment of root-nodulating Burkholderia and investigated biogeographic and host-related patterns of the legume-rhizobial symbiosis in the South African fynbos biome, as well as at global scales, including native species from the South American Caatinga and Cerrado biomes. While a global investigation of the rhizobial diversity revealed distinct nodulation and nitrogen fixation genes among South African and South American legumes, regionally distributed species in the Cape region were unrelated to geographic and host factors.

The Structure and Evolution of Beta-Rhizobial Symbiotic Genes Deduced from Their Complete Genomes

“…Lebeckia spp. ), such as B. dilworthii and B. sprentiae, which was to be expected in consideration of other reports [14][15][16]41,61]. Also reported that the fixNOQP and fixGHIS nitrogenase production and assembly genes are missing in all the Burkholderia strains that they examined, but after further analysis of the products of these genes we found their protein products were annotated on the published genome for B. phymatum STM815 T , but there were no relevant annotation gene names in GenBank.…”

“…Although they are generally considered to be symbionts of Mimosa, the Beta-rhizobia, especially the Burkholderia members, are versatile and the legume nodulation host range of this group has recently been extended into the papilionideae sub-family [12,[14][15][16]40,41]. This group contains B. tuberum, the only nodulating Burkholderia species so far described that is common to both Africa and America, and which exists as two symbiovars that can nodulate either mimosoid (sv.…”

“…In addition, host selective pressures and lateral gene transfer in the soil are the main mechanisms that shape the genetic structure of symbiotic microorganisms [14][15][16]31,79,92] and these confound the use of 16S rDNA phylogenies to describe symbiotic bacterial relationships with their hosts and each other, thus making study of the evolutionary history of symbiosis difficult. On the other hand, nif and nod genes are selectively lost, duplicated, and horizontally transferred [93].…”

“…are associated with two very different clades of bacteria i.e. Burkholderia and Mesorhizobium/Rhizobium [14][15][16]. The nodZ gene (Nod factor fucosyl transferase) was observed in Mesorhizobium loti, and was not found to be present in Beta-rhizobia.…”

“…However, B. tuberum STM678 T and related South African strains which nodulate papilionoid legumes and which cannot nodulate Mimosa, appear to be more closely-related to Alpha-rhizobia and are distant from other beta-rhizobia in terms of their nod genes [5,[12][13][14][15][16]41]. Burkholderia species with nod genes that are related to B. tuberum STM678 T include B. sprentiae, B. rhynchosiae, B. dilworthii and B. dipogonis, as well as several other strains from papilionoid legumes from South Africa; the similarity in their nod genes suggests that they may have an origin common to some Alpha-rhizobia from papilionoid legumes, such as Bradyrhizobium.…”