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

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...

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Published inApplied and environmental microbiology Vol. 82; no. 17; pp. 5099 - 5115
Main Authors Lemaire, Benny, Chimphango, Samson B. M., Stirton, Charles, Rafudeen, Suhail, Honnay, Olivier, Smets, Erik, Chen, Wen-Ming, Sprent, Janet, James, Euan K., Muasya, A. Muthama
Format Journal Article
LanguageEnglish
Published United States American Society for Microbiology 01.09.2016
Subjects
Bacteria
Biogeography
Burkholderia
Burkholderia - classification
Burkholderia - genetics
Burkholderia - isolation & purification
Burkholderia - physiology
Dipogon
Distribution patterns
Evolutionary and Genomic Microbiology
Fabaceae - classification
Fabaceae - microbiology
Flora
Fynbos
Genetic diversity
Gram-negative bacteria
Host Specificity
Indigofera
Legumes
Mimosa pudica
Phylogeny
Root Nodules, Plant - microbiology
Soil sciences
South Africa
South America
Symbiosis
Online AccessGet full text
ISSN0099-2240
1098-5336
1098-5336
DOI10.1128/AEM.00591-16

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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. IMPORTANCE This 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.
AbstractList 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 STM678T and B. phymatum STM815T 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. IMPORTANCE This 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.
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. IMPORTANCE This 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.
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.UNLABELLEDRhizobia 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.This 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.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.
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^sup T^ and B. phymatum STM815^sup 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.
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. This 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.
Author Lemaire, Benny
Rafudeen, Suhail
Smets, Erik
Honnay, Olivier
Chimphango, Samson B. M.
Stirton, Charles
Chen, Wen-Ming
James, Euan K.
Sprent, Janet
Muasya, A. Muthama
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  organization: Department of Biological Sciences, University of Cape Town, Cape Town, South Africa
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  organization: Department of Molecular and Cell Biology, University of Cape Town, Cape Town, South Africa
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  fullname: Honnay, Olivier
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  givenname: Wen-Ming
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  fullname: Chen, Wen-Ming
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  fullname: Muasya, A. Muthama
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BackLink https://www.ncbi.nlm.nih.gov/pubmed/27316955$$D View this record in MEDLINE/PubMed
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Copyright Copyright © 2016, American Society for Microbiology. All Rights Reserved.
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Copyright © 2016, American Society for Microbiology. All Rights Reserved. 2016 American Society for Microbiology
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DocumentTitleAlternate Biogeography of the Burkholderia-Legume Interaction
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Citation Lemaire B, Chimphango SBM, Stirton C, Rafudeen S, Honnay O, Smets E, Chen W-M, Sprent J, James EK, Muasya AM. 2016. Biogeographical patterns of legume-nodulating Burkholderia spp.: from African fynbos to continental scales. Appl Environ Microbiol 82:5099–5115. doi:10.1128/AEM.00591-16.
OpenAccessLink https://aem.asm.org/content/aem/82/17/5099.full.pdf
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PublicationTitle Applied and environmental microbiology
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Snippet Rhizobia of the genus Burkholderia have large-scale distribution ranges and are usually associated with South African papilionoid and South American mimosoid...
Rhizobia of the genus Burkholderia have large-scale distribution ranges and are usually associated with South African papilionoid and South American mimosoid...
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StartPage 5099
SubjectTerms Bacteria
Biogeography
Burkholderia
Burkholderia - classification
Burkholderia - genetics
Burkholderia - isolation & purification
Burkholderia - physiology
Dipogon
Distribution patterns
Evolutionary and Genomic Microbiology
Fabaceae - classification
Fabaceae - microbiology
Flora
Fynbos
Genetic diversity
Gram-negative bacteria
Host Specificity
Indigofera
Legumes
Mimosa pudica
Phylogeny
Root Nodules, Plant - microbiology
Soil sciences
South Africa
South America
Symbiosis
Title Biogeographical Patterns of Legume-Nodulating Burkholderia spp.: from African Fynbos to Continental Scales
URI https://www.ncbi.nlm.nih.gov/pubmed/27316955
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https://pubmed.ncbi.nlm.nih.gov/PMC4988186
Volume 82
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