Skip to main content
Log in

The Spread of Bradyrhizobium Lineages Across Host Legume Clades: from Abarema to Zygia

  • Plant Microbe Interactions
  • Published:
Microbial Ecology Aims and scope Submit manuscript

Abstract

To analyze macroevolutionary patterns in host use by Bradyrhizobium root-nodule bacteria, 420 strains from 75 legume host genera (sampled in 25 countries) were characterized for portions of six housekeeping genes and the nifD locus in the symbiosis island chromosomal region. Most Bradyrhizobium clades utilized very divergent sets of legume hosts. This suggests that Bradyrhizobium spread across the major legume lineages early in its evolution, with only a few derived clades subsequently developing a narrower pattern of host use. Significant modularity existed in the network structure of recent host jumps (inferred from cases where closely related strain pairs were found on different legume taxa). This implies that recent host switching has occurred most often within particular subgroups of legumes. Nevertheless, the observed link structure would allow a bacterial lineage to reach almost any of the 75 legume host genera in a relatively small number of steps. However, permutation tests also showed that symbionts from certain host plant clades were significantly more similar than would be the case if bacteria were distributed at random on the trees. Related legumes thus harbored related sets of symbionts in some cases, indicating some degree of phylogenetic conservatism in partner selection.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  1. Andrus AD, Andam C, Parker MA (2012) American origin of Cupriavidus bacteria associated with invasive Mimosa legumes in the Philippines. FEMS Microbiol Ecol 80:747–50

    Article  CAS  PubMed  Google Scholar 

  2. Ardley JK, Parker MA, De Meyer SE, Trengove RD, O'Hara GW, Reeve WG, Yates RJ, Dilworth MJ, Willems A, Howieson JG (2012) Microvirga lupini sp. nov., Microvirga lotononidis sp. nov., and Microvirga zambiensis sp. nov. are Alphaproteobacterial root nodule bacteria that specifically nodulate and fix nitrogen with geographically and taxonomically separate legume hosts. Int J Syst Evol Microbiol 62:2579–2588

    Article  CAS  PubMed  Google Scholar 

  3. Ardley JK, Reeve WG, O'Hara GW, Yates J, Dilworth MJ, Howieson JG (2013) Nodule morphology, symbiotic specificity and association with unusual rhizobia are distinguishing features of the genus Listia within the Southern African crotalarioid clade Lotononis s.l. Ann Bot 112:1–15

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  4. Aserse AA, Räsänen LA, Aseffa F, Hailemariam A, Lindström K (2012) Phylogenetically diverse groups of Bradyrhizobium isolated from nodules of Crotalaria spp., Indigofera spp., Erythrina brucei and Glycine max growing in Ethiopia. Mol Phy Evol 65:595–609

    Article  Google Scholar 

  5. Benjamini Y, Krieger AM, Yekutieli D (2006) Adaptive linear step-up procedures that control the false discovery rate. Biometrika 93:491–507

    Article  Google Scholar 

  6. Cardoso D, de Queiroz LP, Pennington RT, de Lima HC, Fonty E, Wojciechowski MF, Lavin M (2012) Revisiting the phylogeny of papilionoid legumes: new insights from comprehensively sampled early-branching lineages. Am J Bot 99:1991–2013

    Article  PubMed  Google Scholar 

  7. Chaintreuil C, Arrighi JF, Giraud E, Miche L, Moulin L, Dreyfus B, Munive-Hernandez JA, Villegas-Hernandez M, Bena G (2013) Evolution of symbiosis in the legume genus Aeschynomene. New Phytol 200:1247–1259

    Article  CAS  PubMed  Google Scholar 

  8. Delamuta JRM, Ribeiro RA, Ormeño-Orrillo E, Melo IS, Martinez-Romero E, Hungria M (2013) Polyphasic evidence supporting the reclassification of Bradyrhizobium japonicum group Ia strains as Bradyrhizobium diazoefficiens sp. nov. Int J Syst Evol Microbiol 63:3342–3351

    Article  CAS  PubMed  Google Scholar 

  9. De Meyer SE, Willems A (2011) Genetic diversity of rhizobia associated with indigenous legumes in different regions of Flanders (Belgium). Soil Biol Biochem 43:2384–2396

    Article  Google Scholar 

  10. Doignon-Bourcier F, Sy A, Willems A et al (1999) Diversity of bradyrhizobia from 27 tropical Leguminosae species native of Senegal. Syst Appl Microbiol 22:647–661

    Article  PubMed  Google Scholar 

  11. Doyle JJ (2011) Phylogenetic perspectives on the origins of nodulation. Mol Plant-Microbe Interact 1:1289–1295

    Article  Google Scholar 

  12. Dupuy N, Willems A, Pot B, Dewettinck D, Vandenbruane I, Maestrojuan G, Dreyfus B, Kersters K, Collins MD, Gillis M (1994) Phenotypic and genotypic characterization of bradyrhizobia nodulating the leguminous tree Acacia albida. Int J Syst Evol Microbiol 44:461–473

    CAS  Google Scholar 

  13. Ehinger M, Mohr TJ, Starcevich JB, Sachs JL, Porter SS, Simms EL (2014) Specialization-generalization trade-off in a Bradyrhizobium symbiosis with wild legume hosts. BMC Ecol 14:8

    Article  PubMed Central  PubMed  Google Scholar 

  14. Fonseca MB, Peix A, de Faria SM, Mateos PF, Rivera LP, Simoes-Araujo JL, Giovanni M, Franc C, dos Santos Isaias RM, Cruz C, Velazquez E, Scotti MR, Sprent JI, James EK (2012) Nodulation in Dimorphandra wilsonii Rizz. (Caesalpinioideae), a threatened species native to the Brazilian cerrado. PLoS One 7:e49520

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  15. Fraser C, Alm EJ, Polz MF, Spratt BG, Hanage WP (2009) The bacterial species challenge: making sense of genetic and ecological diversity. Science 323:741–746

    Article  CAS  PubMed  Google Scholar 

  16. Guerrouj K, Ruíz-Díez B, Chahboune R, Ramírez-Bahena MH, Abdelmoumen H, Quiñones MA, El Idrissi MM, Velázquez E, Fernández-Pascual M, Bedmar EJ, Peix A (2013) Definition of a novel symbiovar (sv. retamae) within Bradyrhizobium retamae sp. nov., nodulating Retama sphaerocarpa and Retama monosperma. Syst Appl Microbiol 36:218–223

    Article  CAS  PubMed  Google Scholar 

  17. Gueye F, Moulin L, Sylla S, Ndoye I, Bena G (2009) Genetic diversity and distribution of Bradyrhizobium and Azorhizobium strains associated with the herb legume Zornia glochidiata sampled from across Senegal. Syst Appl Microbiol 32:387–399

    Article  CAS  PubMed  Google Scholar 

  18. Guimera R, Amaral LAN (2005) Cartography of complex networks: modules and universal roles. J Stat Mech P02001–1–P02001–13

  19. Gyaneshwar P, Hirsch AM, Moulin L, Chen WM, Elliot GN, Bontemps C, Estrada-de los Santos P, Gross E, dos Reis FB, Sprent JI, Young JP, James EK (2011) Legume-nodulating betaproteobacteria: diversity, host range, and future prospects. Mol Plant-Microbe Int 24:1276–1288

    Article  CAS  Google Scholar 

  20. Horn K, Parker I, Małek W, Rodríguez-Echeverría S, Parker MA (2014) Disparate origins of Bradyrhizobium symbionts for invasive populations of Cytisus scoparius (Leguminosae) in North America. FEMS Microbiol Ecol 89:89–98

    Article  CAS  PubMed  Google Scholar 

  21. Jaftha JB, Strijdom BW, Steyn PL (2002) Characterization of pigmented methylotrophic bacteria which modulate Lotononis bainesii. Syst Appl Microbiol 25:440–449

    Article  CAS  PubMed  Google Scholar 

  22. Kaneko T, Nakamura Y, Sato S et al (2002) Complete genomic sequence of nitrogen-fixing symbiotic bacterium Bradyrhizobium japonicum USDA110. DNA Res 9:189–97

    Article  PubMed  Google Scholar 

  23. Kautz DR, Taber P (2004) Land resource regions and major land resource areas of Alaska. United States Department of Agriculture - NRCS Alaska, Palmer

    Google Scholar 

  24. Koppell JH, Parker MA (2012) Phylogenetic clustering of Bradyrhizobium symbionts on legumes indigenous to North America. Microbiology 158:2050–2059

    Article  CAS  PubMed  Google Scholar 

  25. Koponen P, Nygren P, Domenach AM, Le Roux C, Saur E, Roggy JC (2003) Nodulation and dinitrogen fixation of legume trees in a tropical freshwater swamp forest in French Guiana. J Trop Ecol 19:655–666

    Article  Google Scholar 

  26. Lafay B, Burdon JJ (1998) Molecular diversity of rhizobia occurring on native shrubby legumes in southeastern Australia. Appl Environ Microbiol 64:3989–3997

    PubMed Central  CAS  PubMed  Google Scholar 

  27. Le Roux C, Muller F, Bouvet JM, Dreyfus B, Béna G, Galiana A, Bâ AM (2014) Genetic diversity patterns and functional traits of Bradyrhizobium strains associated with Pterocarpus officinalis Jacq. in Caribbean islands and Amazonian forest (French Guiana). Microb Ecol 68:329–338

    Article  PubMed  Google Scholar 

  28. Lewis G, Schrire B, Mackinder B, Lock M (2005) Legumes of the world. Royal Botanic Gardens, Kew

    Google Scholar 

  29. LPWG [The Legume Phylogeny Working Group] (2013) Legume phylogeny and classification in the 21st century: progress, prospects and lessons for other species-rich clades. Taxon 62:217–248

    Article  Google Scholar 

  30. Miché L, Moulin L, Chaintreuil C, Contreras-Jimenez JL, Munive-Hernández JA, Del Carmen Villegas-Hernandez M, Crozier F, Béna G (2010) Diversity analyses of Aeschynomene symbionts in Tropical Africa and Central America reveal that nod-independent stem nodulation is not restricted to photosynthetic bradyrhizobia. Environ Microbiol 12:2152–64

    PubMed  Google Scholar 

  31. Moulin L, Bena G, Boivin-Masson C, Stepkowski T (2004) Phylogenetic analyses of symbiotic nodulation genes support vertical and lateral gene co-transfer within the Bradyrhizobium genus. Mol Phylogenet Evol 30:720–732

    Article  CAS  PubMed  Google Scholar 

  32. Parker MA (2012) Legumes select symbiosis island sequence variants in Bradyrhizobium. Molec Ecol 21:1769–1778

    Article  Google Scholar 

  33. Parker MA, Doyle JL, Doyle JJ (2004) Comparative phylogeography of Amphicarpaea legumes and their root-nodule symbionts in Japan and North America. J Biogeog 31:425–434

    Article  Google Scholar 

  34. Parker MA, Rousteau A (2014) Mosaic origins of Bradyrhizobium legume symbionts on the Caribbean island of Guadeloupe. Mol Phylogenet Evol 77:110–5

    Article  PubMed  Google Scholar 

  35. Qian J, Kwon SW, Parker MA (2003) rRNA and nifD phylogeny of Bradyrhizobium from sites across the Pacific Basin. FEMS Microbiol Let 219:159–165

    Article  CAS  Google Scholar 

  36. Rivas R, Martens M, de Lajudie P, Willems A (2009) Multilocus sequence analysis of the genus Bradyrhizobium. Syst Appl Microbiol 32:101–110

    Article  CAS  PubMed  Google Scholar 

  37. Rodríguez-Echeverría S (2010) Rhizobial hitchhikers from down under: invasional meltdown in a plant-bacteria mutualism? J Biogeog 37:1611–1622

    Google Scholar 

  38. Rodríguez-Echeverría S, Moreno S, Bedmar EJ (2014) Genetic diversity of root nodulating bacteria associated with Retama sphaerocarpa in sites with different soil and environmental conditions. Syst Appl Microbiol 37:305–10

    Article  PubMed  Google Scholar 

  39. Ronquist F, Huelsenbeck JP (2003) MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574

    Article  CAS  PubMed  Google Scholar 

  40. Stefanovic S, Pfeil BE, Palmer JD, Doyle JJ (2009) Relationships among phaseoloid legumes based on sequences from eight chloroplast regions. Syst Bot 34:115–128

    Article  Google Scholar 

  41. Stepkowski T, Hughes CE, Law IJ, Markiewicz L, Gurda D, Chlebicka A, Moulin L (2007) Diversification of lupine Bradyrhizobium strains: evidence from nodulation gene trees. Appl Env Microbiol 73:3254–3264

    Article  CAS  Google Scholar 

  42. Stepkowski T, Watkin E, McInnes A, Gurda D, Gracz J, Steenkamp ET (2012) Distinct Bradyrhizobium communities nodulate legumes native to temperate and tropical monsoon Australia. Mol Phylogenet Evol 63:265–277

    Article  PubMed  Google Scholar 

  43. Studebaker S (2010) Wildflowers and other plant life of the Kodiak archipelago. Sense of Place, Kodiak

    Google Scholar 

  44. Vinuesa P, Leon-Barrios M, Silva C, Willems A, Jarabo-Lorenzo A, Perez-Galdona R, Werner D, Martinez-Romero E (2005) Bradyrhizobium canariense sp. nov., an acid-tolerant endosymbiont from the nodules of endemic woody legume species (Papilionoideae: Genisteae) growing in the Canary Islands along with B. japonicum bv. genistearum, Bradyrhizobium genospecies a and Bradyrhizobium genospecies b. Int J Syst Evol Microbiol 55:569–75

    Article  CAS  PubMed  Google Scholar 

  45. Webb CO, Ackerly DD, Kembel SW (2008) Phylocom: software for the analysis of phylogenetic community structure and trait evolution. Bioinformatics 24:2098–2100

    Article  CAS  PubMed  Google Scholar 

  46. Wiedenbeck J, Cohan FM (2011) Origins of bacterial diversity through horizontal genetic transfer and adaptation to new ecological niches. FEMS Microbiol Rev 35:957–976

    Article  CAS  PubMed  Google Scholar 

  47. Willems A (2006) The taxonomy of rhizobia: an overview. Plant Soil 287:3–14

    Article  CAS  Google Scholar 

  48. Wolde-Meskel E, Terefework Z, Frostegård A, Lindström K (2005) Genetic diversity and phylogeny of rhizobia isolated from agroforestry legume species in southern Ethiopia. Int J Syst Evol Microbiol 55:1439–52

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

For providing strains, I am very grateful to Alexis Andrus, Julie Ardley, Craig Barrett, John Bishop, Dulal Borthakur, Jeremy Burdon, Euan James, Christine Le Roux, Kristina Lindström, Wanda Malek, Stephen Mondo, Ingrid Parker, Alvaro Peix, Riley Pratt, Raul Rivas, Susana Rodríguez-Echeverría, Encarna Velazquez, Pablo Vinuesa, and Anne Willems. Financial support was provided by US National Science Foundation grant MCB-0640246.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Matthew A. Parker.

Electronic Supplementary Material

Below is the link to the electronic supplementary material.

Table S1

Source information for 113 Bradyrhizobium strains. (DOCX 118 kb)

Table S2

GenBank accession numbers for 420 Bradyrhizobium strains. (DOCX 131 kb)

Table S3

Geographic distribution for 20 Bradyrhizobium clades in the housekeeping gene tree. (DOCX 70 kb)

Fig. S1

Bayesian tree for six concatenated housekeeping loci (with clade posterior probability values) in 420 Bradyrhizobium strains. (PDF 46 kb)

Fig. S2

Phylogenetic network for recA sequences from type strains of 21 Bradyrhizobium species and 1–2 representative strains for each of the 20 clades in the concatenated housekeeping tree (Fig. 2; clades are designated by a letter after the strain name). Network was inferred by the NeighborNet algorithm (Huson DH, Bryant D [2006], Application of phylogenetic networks in evolutionary studies, Mol Biol Evol 23: 254–267). (PDF 7 kb)

Fig. S3

Bayesian tree for nifD sequences from 420 Bradyrhizobium strains. Stains whose host belonged to one of the nine major legume clades (Fig. 1) are marked with different color highlights. (PDF 771 kb)

Fig. S4

Relative nucleotide divergence in nifD vs. six concatenated housekeeping loci, plotted for Bradyrhizobium strains from two different legume host genera (n = 85,878 strain pairs), and strain pairs associated with the same legume host genus (n = 2112). In 10,000 bootstrap samples of linear regression coefficients, there was zero overlap of slope or intercept estimates for the two data sets. (PDF 587 kb)

Fig. S5

Network of Bradyrhizobium host shifts across 75 legume genera in the nifD tree (Fig. S3). Each edge linking two legume genera represents a single bacterial strain from one host whose closest relative in the nifD tree came from the other legume genus. Modules in the network are indicated by different colors. (PDF 39 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Parker, M.A. The Spread of Bradyrhizobium Lineages Across Host Legume Clades: from Abarema to Zygia . Microb Ecol 69, 630–640 (2015). https://doi.org/10.1007/s00248-014-0503-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00248-014-0503-5

Keywords

Navigation