1887

Abstract

Common bean ( L.) is the most important legume consumed worldwide; its genetic origins lie in the Mesoamerican (main centre) and Andean regions. It is promiscuous in establishing root-nodule symbioses; however, in the centres of origin/domestication, the predominant association is with . We have previously identified a new lineage (PEL-3) comprising three strains (CNPSo 661, CNPSo 666 and CNPSo 668) isolated from root nodules of common bean in Mexico, and that have now been analysed in more detail. Sequences of the 16S rRNA gene positioned the three strains in a large clade including . Multilocus sequence analysis (MLSA) with four housekeeping genes (, , and ) positioned the three strains in a clade distinct from all other described species, with 100 % bootstrap support, and nucleotide identity (NI) of the four concatenated genes with the closest species was 95.0 %. Average nucleotide identity (ANI) values of the whole genome of CNPSo 668 and the closest species, , was 92.9 %. In the analyses of the symbiotic genes and , the strains comprised a cluster with other rhizobial symbionts of . Other phenotypic and genotypic traits were determined for the new group and our data support the description of the three CNPSo strains as a novel species, for which the name is proposed. The type strain is CNPSo 668 (=UMR 1320=Z87-8=LMG 30030 =U 10001), isolated from a common-bean nodule in Mexico.

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2017-10-01
2024-04-23
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References

  1. Prodanov M, Sierra I, Vidal-Valverde C. Influence of soaking and cooking on the thiamin, riboflavin and niacin contents of legumes. Food Chem 2004; 84:271–277 [View Article]
    [Google Scholar]
  2. CGIAR (Consultative Group on International Agricultural Research) 2012; Common bean. Available at: www.cgiar.org/our-Strategy/crop-Factsheets/beans/ [Accessed 8 March 2017]
  3. Herrera-Cervera JA, Caballero-Mellado J, Laguerre G, Tichy HV, Requena N et al. At least five rhizobial species nodulate Phaseolus vulgaris in a Spanish soil. FEMS Microbiol Ecol 1999; 30:87–97 [View Article]
    [Google Scholar]
  4. Martínez-Romero E. Diversity of Rhizobium-Phaseolus vulgaris symbiosis: overview and perspectives. Plant Soil 2003; 252:11–23 [View Article]
    [Google Scholar]
  5. Aserse AA, Räsänen LA, Assefa F, Hailemariam A, Lindström K. Phylogeny and genetic diversity of native rhizobia nodulating common bean (Phaseolus vulgaris L.) in Ethiopia. Syst Appl Microbiol 2012; 35:120–131 [View Article][PubMed]
    [Google Scholar]
  6. Dall'Agnol RF, Ribeiro RA, Delamuta JR, Ormeño-Orrillo E, Rogel MA et al. Rhizobium paranaense sp. nov., an effective N2-fixing symbiont of common bean (Phaseolus vulgaris L.) with broad geographical distribution in Brazil. Int J Syst Evol Microbiol 2014; 64:3222–3229 [View Article][PubMed]
    [Google Scholar]
  7. Dall'Agnol RF, Ribeiro RA, Ormeño-Orrillo E, Rogel MA, Delamuta JR et al. Rhizobium freirei sp. nov., a symbiont of Phaseolus vulgaris that is very effective at fixing nitrogen. Int J Syst Evol Microbiol 2013; 63:4167–4173 [View Article][PubMed]
    [Google Scholar]
  8. Ribeiro RA, Martins TB, Ormeño-Orrillo E, Marçon Delamuta JR, Rogel MA et al. Rhizobium ecuadorense sp. nov., an indigenous N2-fixing symbiont of the Ecuadorian common bean (Phaseolus vulgaris L.) genetic pool. Int J Syst Evol Microbiol 2015; 65:3162–3169 [View Article][PubMed]
    [Google Scholar]
  9. Ribeiro RA, Ormeño-Orrillo E, dall'agnol RF, Graham PH, Martinez-Romero E et al. Novel Rhizobium lineages isolated from root nodules of the common bean (Phaseolus vulgaris L.) in Andean and Mesoamerican areas. Res Microbiol 2013; 164:740–748 [View Article][PubMed]
    [Google Scholar]
  10. Gepts P, Debouck D. Origin, domestication and evolution of the common bean (Phaseolus vulgaris L.). In van Schoonhoven A, Voysest O. (editors) Common Beans, Research for Crop Improvement Wallingford: CAB; 1991 pp. 7–53
    [Google Scholar]
  11. Bitocchi E, Nanni L, Bellucci E, Rossi M, Giardini A et al. Mesoamerican origin of the common bean (Phaseolus vulgaris L.) is revealed by sequence data. Proc Natl Acad Sci USA 2012; 109:E788E796 [View Article][PubMed]
    [Google Scholar]
  12. Martínez-Romero E. Coevolution in Rhizobium-legume symbiosis?. DNA Cell Biol 2009; 28:361–370 [View Article][PubMed]
    [Google Scholar]
  13. Sprent JI, Ardley J, James EK. Biogeography of nodulated legumes and their nitrogen-fixing symbionts. New Phytol 2017; 215:40–56 [View Article][PubMed]
    [Google Scholar]
  14. Aguilar OM, López MV, Riccillo PM, González RA, Pagano M et al. Prevalence of the Rhizobium etli-like allele in genes coding for 16S rRNA among the indigenous rhizobial populations found associated with wild beans from the Southern Andes in Argentina. Appl Environ Microbiol 1998; 64:3250–3524[PubMed]
    [Google Scholar]
  15. Aguilar OM, Riva O, Peltzer E. Analysis of Rhizobium etli and of its symbiosis with wild Phaseolus vulgaris supports coevolution in centers of host diversification. Proc Natl Acad Sci USA 2004; 101:13548–13553 [View Article][PubMed]
    [Google Scholar]
  16. Segovia L, Young J, Martínez-Romero E. Reclassification of American Rhizobium leguminosarum sv. phaseoli type I strains as Rhizobium etli sp. nov. Int J Syst Evol Microbiol 1993; 43:374–37
    [Google Scholar]
  17. Souza V, Bain J, Silva C, Bouchet V, Valera A et al. Ethnomicrobiology: Do agricultural practices modify the population structure of the nitrogen fixing bacteria rhizobium etli biovar phaseoli?. J Ethnobiol 1997; 17:249–266
    [Google Scholar]
  18. López-Guerrero MG, Ormeño-Orrillo E, Velázquez E, Rogel MA, Acosta JL et al. Rhizobium etli taxonomy revised with novel genomic data and analyses. Syst Appl Microbiol 2012; 35:353–358 [View Article][PubMed]
    [Google Scholar]
  19. Yan J, Yan H, Liu LX, Chen WF, Zhang XX et al. Rhizobium hidalgonense sp. nov., a nodule endophytic bacterium of Phaseolus vulgaris in acid soil. Arch Microbiol 2017; 199:97–104 [View Article][PubMed]
    [Google Scholar]
  20. Román-Ponce B, Jing Zhang Y, Soledad Vásquez-Murrieta M, Hua Sui X, Feng Chen W et al. Rhizobium acidisoli sp. nov., isolated from root nodules of Phaseolus vulgaris in acid soils. Int J Syst Evol Microbiol 2016; 66:398–406 [View Article][PubMed]
    [Google Scholar]
  21. Mnasri B, Liu TY, Saidi S, Chen WF, Chen WX et al. Rhizobium azibense sp. nov., a nitrogen fixing bacterium isolated from root-nodules of Phaseolus vulgaris. Int J Syst Evol Microbiol 2014; 64:1501–1506 [View Article][PubMed]
    [Google Scholar]
  22. Debouck DG, Toro O, Paredes OM, Johnson WC, Gepts P. Genetic diversity and ecological distribution of Phaseolus vulgaris (Fabaceae) in northwestern South America. Econ Bot 1993; 47:408–423 [View Article]
    [Google Scholar]
  23. Hungria M, O’Hara GW, Zilli JE, Araujo RS, Deaker R et al. Isolation and growth or rhizobia. In Howieson JG, Dilworth JG. (editors) Working with Rhizobia Canberra, Australia: ACIAR; 2016 pp. 39–60
    [Google Scholar]
  24. Felsenstein J. Evolutionary trees from DNA sequences: a maximum likelihood approach. J Mol Evol 1981; 17:368–376 [View Article][PubMed]
    [Google Scholar]
  25. Kumar S, Stecher G, Tamura K. MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 2016; 33:1870–1874 [View Article][PubMed]
    [Google Scholar]
  26. Tamura K, Nei M. Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol Biol Evol 1993; 10:512–526[PubMed]
    [Google Scholar]
  27. Edgar RC. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 2004; 32:1792–1797 [View Article][PubMed]
    [Google Scholar]
  28. Felsenstein J. Confidence limits on phylogenies: an approach using the bootstrap. Evolution 1985; 39:783–791 [View Article][PubMed]
    [Google Scholar]
  29. Stackebrandt E, Frederiksen W, Garrity GM, Grimont PA, Kämpfer P et al. Report of the ad hoc committee for the re-evaluation of the species definition in bacteriology. Int J Syst Evol Microbiol 2002; 52:1043–1047 [View Article][PubMed]
    [Google Scholar]
  30. Berrada H, Fikri-Benbrahim K. Taxonomy of the rhizobia: current perspectives. Br Microbiol Res J 2014; 4:616–639 [View Article]
    [Google Scholar]
  31. Bontemps C, Rogel MA, Wiechmann A, Mussabekova A, Moody S et al. Endemic Mimosa species from Mexico prefer alphaproteobacterial rhizobial symbionts. New Phytol 2016; 209:319–333 [View Article][PubMed]
    [Google Scholar]
  32. Jiao YS, Yan H, Ji ZJ, Liu YH, Sui XH et al. Rhizobium sophorae sp. nov. and Rhizobium sophoriradicis sp. nov., nitrogen-fixing rhizobial symbionts of the medicinal legume Sophora flavescens. Int J Syst Evol Microbiol 2015; 65:497–503 [View Article][PubMed]
    [Google Scholar]
  33. Delamuta JR, Ribeiro RA, Araújo JL, Rouws LF, Zilli et al. Bradyrhizobium stylosanthis sp. nov., comprising nitrogen-fixing symbionts isolated from nodules of the tropical forage legume Stylosanthes spp. Int J Syst Evol Microbiol 2016; 66:3078–3087 [View Article][PubMed]
    [Google Scholar]
  34. Helene LC, Delamuta JR, Ribeiro RA, Ormeño-Orrillo E, Rogel MA et al. Bradyrhizobium viridifuturi sp. nov., encompassing nitrogen-fixing symbionts of legumes used for green manure and environmental services. Int J Syst Evol Microbiol 2015; 65:4441–4448 [View Article][PubMed]
    [Google Scholar]
  35. Hall TA. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 1999; 41:95–98
    [Google Scholar]
  36. Konstantinidis KT, Ramette A, Tiedje JM. Toward a more robust assessment of intraspecies diversity, using fewer genetic markers. Appl Environ Microbiol 2006; 72:7286–7293 [View Article][PubMed]
    [Google Scholar]
  37. Stackebrandt E, Ebers J. Taxonomic parameters revisited: tarnished gold standards. Microbiol Today 2006; 33:152–155
    [Google Scholar]
  38. Durán D, Rey L, Mayo J, Zúñiga-Dávila D, Imperial J et al. Bradyrhizobium paxllaeri sp. nov. and Bradyrhizobium icense sp. nov., nitrogen-fixing rhizobial symbionts of Lima bean (Phaseolus lunatus L.) in Peru. Int J Syst Evol Microbiol 2014; 64:2072–2078 [View Article][PubMed]
    [Google Scholar]
  39. Kim M, Oh HS, Park SC, Chun J. Towards a taxonomic coherence between average nucleotide identity and 16S rRNA gene sequence similarity for species demarcation of prokaryotes. Int J Syst Evol Microbiol 2014; 64:346–351 [View Article][PubMed]
    [Google Scholar]
  40. Goris J, Konstantinidis KT, Klappenbach JA, Coenye T, Vandamme P et al. DNA–DNA hybridization values and their relationship to whole-genome sequence similarities. Int J Syst Evol Microbiol 2007; 57:81–91 [View Article][PubMed]
    [Google Scholar]
  41. Richter M, Rosselló-Móra R. Shifting the genomic gold standard for the prokaryotic species definition. Proc Natl Acad Sci USA 2009; 106:19126–19131 [View Article][PubMed]
    [Google Scholar]
  42. Ormeño-Orrillo E, Servín-Garcidueñas LE, Rogel MA, González V, Peralta H et al. Taxonomy of rhizobia and agrobacteria from the Rhizobiaceae family in light of genomics. Syst Appl Microbiol 2015; 38:287–291 [View Article][PubMed]
    [Google Scholar]
  43. Varghese NJ, Mukherjee S, Ivanova N, Konstantinidis KT, Mavrommatis K et al. Microbial species delineation using whole genome sequences. Nucleic Acids Res 2015; 43:6761–6771 [View Article][PubMed]
    [Google Scholar]
  44. Rashid MH, Young JP, Everall I, Clercx P, Willems A et al. Average nucleotide identity of genome sequences supports the description of Rhizobium lentis sp. nov., Rhizobium bangladeshense sp. nov. and Rhizobium binae sp. nov. from lentil (Lens culinaris) nodules. Int J Syst Evol Microbiol 2015; 65:3037–3045 [View Article][PubMed]
    [Google Scholar]
  45. Kurtz S, Phillippy A, Delcher AL, Smoot M, Shumway M et al. Versatile and open software for comparing large genomes. Genome Biol 2004; 5:R12 [View Article][PubMed]
    [Google Scholar]
  46. Kaschuk G, Hungria M, Andrade DS, Campo RJ. Genetic diversity of rhizobia associated with common bean (Phaseolus vulgaris L.) grown under no-tillage and conventional systems in Southern Brazil. Appl Soil Ecol 2006; 32:210–220 [View Article]
    [Google Scholar]
  47. Sneath PHA, Sokal RR. Numerical Taxonomy: The Principles and Practice of Numerical Classification San Francisco, USA: W. H. Freeman and Company; 1973 p. 573
    [Google Scholar]
  48. Jaccard P. The distribution of the flora in the alpine zone.1. New Phytol 1912; 11:37–50 [View Article]
    [Google Scholar]
  49. Tighe SW, de Lajudie P, Dipietro K, Lindström K, Nick G et al. Analysis of cellular fatty acids and phenotypic relationships of Agrobacterium, Bradyrhizobium, Mesorhizobium, Rhizobium and Sinorhizobium species using the Sherlock Microbial Identification System. Int J Syst Evol Microbiol 2000; 50:787–801 [View Article][PubMed]
    [Google Scholar]
  50. Laguerre G, Nour SM, Macheret V, Sanjuan J, Drouin P et al. Classification of rhizobia based on nodC and nifH gene analysis reveals a close phylogenetic relationship among Phaseolus vulgaris symbionts. Microbiology 2001; 147:981–993 [View Article][PubMed]
    [Google Scholar]
  51. Hungria M, Chueire LMO, Coca RG, Megías M. Preliminary characterization of fast growing rhizobial strains isolated from soyabean nodules in Brazil. Soil Biol Biochem 2001; 33:1349–1361 [View Article]
    [Google Scholar]
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