Current Microbiology

, Volume 67, Issue 1, pp 51–60 | Cite as

Phylogenetic Analysis of Burkholderia Species by Multilocus Sequence Analysis

  • Paulina Estrada-de los SantosEmail author
  • Pablo Vinuesa
  • Lourdes Martínez-Aguilar
  • Ann M. Hirsch
  • Jesús Caballero-Mellado


Burkholderia comprises more than 60 species of environmental, clinical, and agro-biotechnological relevance. Previous phylogenetic analyses of 16S rRNA, recA, gyrB, rpoB, and acdS gene sequences as well as genome sequence comparisons of different Burkholderia species have revealed two major species clusters. In this study, we undertook a multilocus sequence analysis of 77 type and reference strains of Burkholderia using atpD, gltB, lepA, and recA genes in combination with the 16S rRNA gene sequence and employed maximum likelihood and neighbor-joining criteria to test this further. The phylogenetic analysis revealed, with high supporting values, distinct lineages within the genus Burkholderia. The two large groups were named A and B, whereas the B. rhizoxinica/B. endofungorum, and B. andropogonis groups consisted of two and one species, respectively. The group A encompasses several plant-associated and saprophytic bacterial species. The group B comprises the B. cepacia complex (opportunistic human pathogens), the B. pseudomallei subgroup, which includes both human and animal pathogens, and an assemblage of plant pathogenic species. The distinct lineages present in Burkholderia suggest that each group might represent a different genus. However, it will be necessary to analyze the full set of Burkholderia species and explore whether enough phenotypic features exist among the different clusters to propose that these groups should be considered separate genera.


Burkholderia nifH Gene Acetylene Reduction Activity Melioidosis Burkholderia Species 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



Multilocus sequence analysis


Burkholderia cepacia complex


Maximum likelihood





This work is dedicated to the memory of Dr. Jesus Caballero Mellado (1953–2010), for his many years of fruitful work, support, generosity, and friendship. We are grateful to Jorge Eduardo Buendia Buendia, Isaac Fernando Lopez Moyado, Mariana del Rosario Ruiz Velasco Leyva, Jorge Arturo Zepeda Martinez, and Marie Lisandra Zepeda Mendoza for technical support during training as students from the Undergraduate Program on Genomic Sciences (Centro de Ciencias Genómicas, Universidad Nacional Autónoma de México). We also thank Annette A. Angus (University of California, Los Angeles) for sharing her unpublished data with us. The housekeeping gene sequences were provided from the ongoing sequencing project of B. unamae MTl-641T, B. tuberum STM678T, B. silvatlantica SRMrh-20T, and B. silvatlantica PVA5 from a project, funded in part by the U.S. National Science Foundation (Grant IOB-0537497) to George Weinstock (Washington University, St. Louis, MO) and AMH.

Supplementary material

284_2013_330_MOESM1_ESM.pdf (501 kb)
Supplementary material 1 (PDF 500 kb)


  1. 1.
    Achouak W, Christen R, Barakat M, Martel MH, Heulin T (1999) Burkholderia caribensis sp. nov., an exopolysaccharide producing bacterium isolated from vertisol microaggregates in Martinique. Int J Syst Bacteriol 49:787–794PubMedCrossRefGoogle Scholar
  2. 2.
    Ait-Tayeb L, Lefevre M, Passet V, Diancourt L, Brisse S, Grimont PAD (2008) Comparative phylogenies of Burkholderia, Ralstonia, Comamonas, Brevundimonas and related organism derived from rpoB, gyrB and rrs gene sequences. Res Microbiol 159:169–177CrossRefGoogle Scholar
  3. 3.
    Aizawa T, Bao Ve N, Nakajima M, Sunairi M (2010) Burkholderia heleia sp. nov., a nitrogen-fixing bacterium isolated from an aquatic plant, Eleocharis dulcis, that grows in highly acidic swamps in actual acid sulfate soil areas of Vietnam. Int J Syst Evol Microbiol 60:1152–1157PubMedCrossRefGoogle Scholar
  4. 4.
    Aizawa T, Nguyen BV, Vijarnsorn P, Nakajima M, Sunairi M (2010) Burkholderia acidipaludis sp. nov., aluminum-tolerant bacteria isolated from the Chinese water chestnut, Eleocharis dulcis, that grows in highly acidic swamps in Southeast Asia. Int J Syst Evol Microbiol 60:2036–2041PubMedCrossRefGoogle Scholar
  5. 5.
    Aizawa T, Vijarnosrn P, Nakajima M, Surairi M (2011) Burkholderia bannensis sp. nov., and acidic pH-neutralizing bacterium isolated from torpedo grass (Panicum repens) that grows in highly acidic swamps in Thailand. Int J Syst Evol Microbiol 61:1645–1650PubMedCrossRefGoogle Scholar
  6. 6.
    Anisimova M, Gascuel O (2006) Approximate likelihood-ratio test for branches: a fast, accurate, and powerful alternative. Syst Biol 55:539–552PubMedCrossRefGoogle Scholar
  7. 7.
    Bramer CO, Vandamme P, da Silva LF, Gomez JGC, Steinbuchel A (2001) Burkholderia sacchari sp. nov., a polyhydroxyalkanoate-accumulating bacterium isolated from soil of a sugar-cane plantation in Brazil. Int J Syst Evol Microbiol 51:1709–1713PubMedCrossRefGoogle Scholar
  8. 8.
    Caballero-Mellado J, Martinez-Aguilar L, Paredes-Valdez G, Estrada-de los Santos P (2004) Burkholderia unamae sp. nov., a N2-fixing rhizospheric and endophytic species. Int J Syst Evol Microbiol 54:1165–1172PubMedCrossRefGoogle Scholar
  9. 9.
    Caballero-Mellado J, Onofre-Lemus J, Estrada-de los Santos P, Martínez-Aguilar L (2007) The tomato rhizosphere, an environment rich in nitrogen-fixing Burkholderia species with capabilities of interest for agriculture and bioremediation. Appl Environ Microbiol 73:5308–5319PubMedCrossRefGoogle Scholar
  10. 10.
    Chen WM, Laevens S, Lee TM, Coenye T, De Vos P, Mergeay M, Vandamme P (2001) Ralstonia taiwanensis sp. nov., isolated from root nodules of Mimosa species and sputum of cystic fibrosis patient. Int J Syst Evol Microbiol 51:1729–1735PubMedCrossRefGoogle Scholar
  11. 11.
    Chen WM, Moulin L, Bontemps C, Vandamme P, Bena G, Boivin-Masson C (2003) Legume symbiotic nitrogen fixation by β-proteobacteria is widespread in nature. J Bacteriol 185:7266–7272PubMedCrossRefGoogle Scholar
  12. 12.
    Chen WM, de Faria SM, Straliotto R, Pitard RM, Simoes-Araujo JL, Chou JH, Chou YJ, Barrios E, Prescott AR, Elliot GN, Sprent JI, Young JPW, James EK (2005) Proof that Burkholderia strains from effective symbioses with legumes: a study of novel Mimosa-nodulating strains from South America. Appl Environ Microbiol 71:7461–7471PubMedCrossRefGoogle Scholar
  13. 13.
    Chen WM, James EK, Chou JH, Sheu SY, Yang SZ, Sprent JI (2005) β-rhizobia from Mimosa pigra, a newly discovered invasive plant in Taiwan. New Phytol 168:661–675PubMedCrossRefGoogle Scholar
  14. 14.
    Chen WM, James EK, Coenye T, Chou JH, Barrios E, de Faria SM, Elliott GN, Sheu SY, Sprent JI, Vandamme P (2006) Burkholderia mimosarum sp. nov., isolated from root nodules of Mimosa spp. from Taiwan and South America. Int J Syst Evol Microbiol 56:1847–1851PubMedCrossRefGoogle Scholar
  15. 15.
    Chen WM, de Faria SM, James EK, Elliott GN, Lin KY, Chou JH, Sheu SY, Cnockaert M, Sprent JI, Vandamme P (2007) Burkholderia nodosa sp. nov., isolated from root nodules of the woody Brazilian legumes Mimosa bimucronata and Mimosa scabrella. Int J Syst Evol Microbiol 57:1055–1059PubMedCrossRefGoogle Scholar
  16. 16.
    Chen WM, de Faria SM, Chou JH, James EK, Elliott GN, Sprent JI, Bontemps C, Young JPW, Vandamme P (2008) Burkholderia sabiae sp. nov., isolated from root nodules of Mimosa caesalpiniifolia. Int J Syst Evol Microbiol 58:2174–2179PubMedCrossRefGoogle Scholar
  17. 17.
    Coenye T, Holmes B, Kersters K, Govan JRW, Vandamme P (1999) Burkholderia cocovenenans (van Damme et al. 1960) Gillis et al. 1995 and Burkholderia vandii Urakami et al. 1994 are junior synonyms of Burkholderia gladioli (Severini 1913) Yabuuchi et al. 1993 and Burkholderia plantarii (Azegami et al. 1987) Urakami et al. 1994, respectively. Int J Syst Bacteriol 49:37–42PubMedCrossRefGoogle Scholar
  18. 18.
    Coenye T, Laevens S, Willems A, Ohlen M, Hannant W, Govan JRW, Gillis M, Falsen E, Vandamme P (2001) Burkholderia fungorum sp. nov. and Burkholderia caledonica sp. nov., two new species isolated from the environment, animals and human clinical samples. Int J Syst Evol Microbiol 51:1099–1107PubMedCrossRefGoogle Scholar
  19. 19.
    Coenye T, Mahenthiralingam E, Henry D, LiPuma JJ, Laevens S, Gillis M, Speert DP, Vandamme P (2001) Burkholderia ambifaria sp. nov., a novel member of the Burkholderia cepacia complex including biocontrol and cystic fibrosis-related isolates. Int J Syst Evol Microbiol 51:1481–1490PubMedCrossRefGoogle Scholar
  20. 20.
    Coenye T, Goris J, De Vos P, Vandamme P, LiPuma JJ (2003) Classification of Ralstonia pickettii-like isolates from the environment and clinical samples as Ralstonia insidiosa sp. nov. Int J Syst Evol Microbiol 53:1075–1080PubMedCrossRefGoogle Scholar
  21. 21.
    Coenye T, Henry D, Speert DP, Vandamme P (2004) Burkholderia phenoliruptrix sp. nov., to accommodate the 2,4,5-trichlorophenoxyacetic acid and halophenol-degrading strain AC1100. Syst Appl Microbiol 27:623–627PubMedCrossRefGoogle Scholar
  22. 22.
    Compant S, Nowak J, Coenye T, Clement C, Barka EA (2008) Diversity and occurrence of Burkholderia spp. in the natural environment. FEMS Microbiol Rev 32:607–626PubMedCrossRefGoogle Scholar
  23. 23.
    De Baere T, Steyaert S, Wauters G, De Vos P, Goris J, Coenye T, Suyama T, Verschraegen G, Vaneechoutte M (2001) Classification of Ralstonia pickettii biovar 3/‘thomasii’ strains (Pickett 1994) and of new isolates related to nosocomial recurrent meningitis as Ralstonia mannitolytica sp. nov. Int J Syst Evol Microbiol 51:547–558PubMedGoogle Scholar
  24. 24.
    Deris ZZ, Van Rostenberghe H, Habsah H, Noraida R, Tan GC, Chan YY, Rosliza RN, Ravichandran M (2010) First isolation of Burkholderia tropica from neonatal patient successfully treated with imipenem. Int J Infect Dis 14:e73–e74PubMedCrossRefGoogle Scholar
  25. 25.
    Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797PubMedCrossRefGoogle Scholar
  26. 26.
    Elliot GN, Chen WM, Chou JH, Wang HC, Sheu SY, Perin L, Reis VM, Moulin L, Simon MF, Bontemps C, Sutherland JM, Bessi R, de Faria SM, Trinick MJ, Prescott AR, Sprent JI, James EK (2007) Burkholderia phymatum is a highly effective nitrogen-fixing symbiont of Mimosa spp. and fixes nitrogen ex planta. New Phytol 173:168–180CrossRefGoogle Scholar
  27. 27.
    Elliot GN, Chen WM, Bontemps C, Chou JH, Young JP, Sprent JI, James EK (2007) Nodulation of Cyclopia spp. (Leguminosae, Papilionoidae) by Burkholderia tuberum. Ann Bot 100:1403–1411CrossRefGoogle Scholar
  28. 28.
    Estrada-de los Santos P, Bustillos-Cristales R, Caballero-Mellado J (2001) Burkholderia, a genus rich in plant-associated nitrogen fixers with wide environmental and geographic distribution. Appl Environ Microbiol 67:2790–2798PubMedCrossRefGoogle Scholar
  29. 29.
    Estrada-de los Santos P, Martínez-Aguilar L, López-Lara IM, Caballero-Mellado J (2012) Cupriavidus alkaliphilus sp. nov., a new species associated with agricultural plants that grow in alkaline soils. Syst Appl Microbiol 35:310–314PubMedCrossRefGoogle Scholar
  30. 30.
    Ferreira PAA, Bomfeti CA, Soares BL, Moreira FMS (2012) Efficient nitrogen-fixing Rhizobium strains isolated from Amazonian soils are highly tolerant to acidity and aluminum. World J Microbiol Biotechnol 28:1947–1959CrossRefGoogle Scholar
  31. 31.
    Gillis M, Van Van T, Bardin R, Goor M, Hebbar P, Willems A, Segers P, Kersters K, Heulin T, Fernandez MP (1995) Polyphasic taxonomy in the genus Burkholderia leading to an emended description of the genus and proposition of Burkholderia vietnamiensis sp. nov. for N2-fixing isolates from rice in Vietnam. Int J Syst Bacteriol 45:274–289CrossRefGoogle Scholar
  32. 32.
    Glass MB, Steigerwalt AG, Jordan JG, Wilkins PP, Gee JE (2006) Burkholderia oklahomensis sp. nov., a Burkholderia pseudomallei-like species formerly known as the Oklahoma strain of Pseudomonas pseudomallei. Int J Syst Evol Microbiol 56:2171–2176PubMedCrossRefGoogle Scholar
  33. 33.
    Goris J, De Vos P, Coenye T, Hoste B, Janssens D, Brim H, Diels L, Mergeay M, Kersters K, Vandamme P (2001) Classification of metal-resistant bacteria from industrial biotopes as Ralstonia campinensis sp. nov., Ralstonia metallidurans sp. nov. and Ralstonia basilensis Steinle et al. 1998 emend. Int J Syst Evol Microbiol 51:1773–1782PubMedCrossRefGoogle Scholar
  34. 34.
    Goris J, Dejonghe W, Falsen E, De Clerck E, Geeraerts B, Willems A, Top EM, Vandamme P, De Vos P (2002) Diversity of transconjugants that acquired plasmid pJP4 or pEMT1 after inoculation of a donor strain in the A- and B-horizon of an agricultural soil and description of Burkholderia hospita sp. nov. and Burkholderia terricola sp. nov. Syst Appl Microbiol 25:340–352PubMedCrossRefGoogle Scholar
  35. 35.
    Goris J, De Vos P, Caballero-Mellado J, Park JH, Falsen E, Quensen JF III, Tiedje JM, Vandamme P (2004) Classification of the PCB- and biphenyl-degrading strain LB400 and relatives as Burkholderia xenovorans sp. nov. Int J Syst Evol Microbiol 54:1677–1681PubMedCrossRefGoogle Scholar
  36. 36.
    Guindon S, Delsuc F, Dufayard JF, Gascuel O (2009) Estimating maximum likelihood phylogenies with PhyML. Methods Mol Biol 537:113–137PubMedCrossRefGoogle Scholar
  37. 37.
    Gyaneshwar P, Hirsch AM, Chen WM, Elliott GN, Bontemps C, Gross E, dos Reis Junior FB, Sprent JI, Young JPW, James EK (2011) Legume nodulating β-proteobacteria: diversity, host range and future prospects. Mol Plant Microbe Interact 24:1276–1288PubMedCrossRefGoogle Scholar
  38. 38.
    Hauser AR, Jain M, Bar-Meir M, McColley SA (2011) Clinical significance of microbial infection and adaptation in cystic fibrosis. Clin Microbiol Rev 24:29–70PubMedCrossRefGoogle Scholar
  39. 39.
    Hee-Chan Y, Wan-Taek I, Kwang KK, Dong-Shan A, Sung-Taik L (2006) Burkholderia terrae sp. nov., isolated from a forest soil. Int J Syst Evol Microbiol 56:453–457CrossRefGoogle Scholar
  40. 40.
    Ho-Bin K, Min-Ju P, Hee-Chan Y, Dong-Shan A, Hai-Zhu J, Deok-Chun Y (2006) Burkholderia ginsengisoli sp. nov. a β-glucosidase-producing bacterium isolated from soil of a ginseng field. Int J Syst Evol Microbiol 56:2529–2533CrossRefGoogle Scholar
  41. 41.
    Jiao Z, Kawamura Y, Mishima N, Yang R, Li N, Liu X, Ezaki T (2003) Need to differentiate lethal toxin-producing strains of Burkholderia gladioli, which cause severe food poisoning: description of B. gladioli pathovar cocovenenans and emended description of B. gladioli. Microbiol Immunol 47:915–925PubMedGoogle Scholar
  42. 42.
    Lackner G, Moebius N, Partida-Martinez L, Hertweck C (2011) Complete genome sequence of Burkholderia rhizoxinica, an endosymbiont of Rhizopus microsporus. J Bacteriol 193:783–784PubMedCrossRefGoogle Scholar
  43. 43.
    Lestin F, Kraak R, Podbielski A (2008) Two cases of keratitis and corneal ulcers caused by Burkholderia gladioli. J Clin Microbiol 46:2445–2449PubMedCrossRefGoogle Scholar
  44. 44.
    Lim YW, Baik KS, Han SK, Kim SB, Bae KS (2003) Burkholderia sordidicola sp. nov., isolated from the white-rot fungus Phanerochaete sordida. Int J Syst Evol Microbiol 53:1631–1636PubMedCrossRefGoogle Scholar
  45. 45.
    Lim JH, Baek SH, Lee ST (2008) Burkholderia sediminicola sp. nov., isolated from freshwater sediment. Int J Syst Evol Microbiol 58:565–569PubMedCrossRefGoogle Scholar
  46. 46.
    Lu P, Zheng LQ, Sun JJ, Liu HM, Li SP, Li WJ, Hong Q (2012) Burkholderia zhejiangensis sp. nov., a novel methyl parathion-degrading bacterium isolated from a wastewater-treating system. Int J Syst Evol Microbiol 62:1337–1341PubMedCrossRefGoogle Scholar
  47. 47.
    Martínez-Aguilar L, Diaz R, Peña-Cabriales JJ, Estrada-de los Santos P, Dunn MF, Caballero-Mellado J (2008) Multichromosomal genome structure and confirmation of diazotrophy in novel plant-associated Burkholderia species. Appl Environ Microbiol 74:4574–4579PubMedCrossRefGoogle Scholar
  48. 48.
    Moulin L, Munive A, Dreyfus B, Boivin-Masson C (2001) Nodulation of legumes by members of the beta-subclass of Proteobacteria. Nature 411:948–950PubMedCrossRefGoogle Scholar
  49. 49.
    Onofre-Lemus J, Hernandez-Lucas I, Girard L, Caballero-Mellado J (2009) ACC (1-aminocyclopropane-1-carboxylate) deaminase activity, a widespread trait in Burkholderia species, and its growth-promoting effect on tomato plants. Appl Environ Microbiol 75:6581–6590PubMedCrossRefGoogle Scholar
  50. 50.
    Otsuka Y, Muramatsu Y, Nakagawa Y, Matsuda M, Nakamura M, Murata H (2010) Burkholderia oxyphila sp. nov., isolated from acidic forest soil that catabolizes (+)-catechin and its putative aromatic derivatives. Int J Syst Evol Microbiol 61:249–254PubMedCrossRefGoogle Scholar
  51. 51.
    Palleroni NJ, Kunisawa R, Contopoulou R, Doudoroff M (1973) Nucleic acid homologies in the genus Pseudomonas. Int J Syst Bacteriol 23:333–339CrossRefGoogle Scholar
  52. 52.
    Payne GW, Vandamme P, Morgan SH, LiPuma JJ, Coenye T, Weightman AJ, Jones TH, Mahenthiralingam E (2005) Development of a recA gene-based identification approach for the entire Burkholderia genus. Appl Environ Microbiol 71:3917–3927PubMedCrossRefGoogle Scholar
  53. 53.
    Perin L, Martinez-Aguilar L, Castro-Gonzalez R, Estrada-de los Santos P, Cabellos-Avelar T, Guedes HV, Reis VM, Caballero-Mellado J (2006) Diazotrophic Burkholderia species associated with field-grown maize and sugarcane. Int J Syst Evol Microbiol 72:3103–3110Google Scholar
  54. 54.
    Perin L, Martinez-Aguilar L, Paredes-Valdez G, Baldani JI, Estrada-de los Santos P, Reis VM, Caballero-Mellado J (2006) Burkholderia silvatlantica sp. nov., a diazotrophic bacterium associated with sugarcane and maize. Int J Syst Evol Microbiol 56:1931–1937PubMedCrossRefGoogle Scholar
  55. 55.
    Poly F, Monrozier LJ, Bally R (2001) Improvement in the RFLP procedure for studying the diversity of nifH genes in communities of nitrogen fixers in soil. Res Microbiol 152:95–103PubMedCrossRefGoogle Scholar
  56. 56.
    Posada D, Crandall KA (1998) MODELTEST: testing the model of DNA substitution. Bioinformatics 14:817–818PubMedCrossRefGoogle Scholar
  57. 57.
    Posada D, Buckley TR (2004) Model selection and model averaging in phylogenetics: advantages of Akaike information criterion and bayesian approaches over likelihood ratio tests. Syst Biol 53:793–808PubMedCrossRefGoogle Scholar
  58. 58.
    Reis VM, Estrada-de los Santos P, Tenorio-Salgado S, Vogel J, Stoffels M, Guyon S, Mavingui P, Baldani VLD, Schmid M, Baldani JI, Balandreau J, Hartmann A, Caballero-Mellado J (2004) Burkholderia tropica sp. nov., a novel nitrogen-fixing, plant-associated bacterium. Int J Syst Evol Microbiol 54:2155–2162PubMedCrossRefGoogle Scholar
  59. 59.
    Sato Y, Nishihara H, Yoshida M, Watanabe M, Rondal JD, Concepcion RN, Ohta H (2006) Cupriavidus pinatubonensis sp. nov. and Cupriavidus laharis sp. nov., novel hydrogen oxidizing, facultatively chemolithotrophic bacteria isolated from volcanic mudflow deposits from Mt. Pinatubo in the Philippines. Int J Syst Evol Microbiol 56:973–978PubMedCrossRefGoogle Scholar
  60. 60.
    Segonds C, Clavel-Batut P, Thouverez M, Grenet D, Le Coustumier L, Plesiat P, Chabanon G (2009) Microbiological and epidemiological features of clinical respiratory isolates of Burkholderia gladioli. J Clin Microbiol 47:1510–1516PubMedCrossRefGoogle Scholar
  61. 61.
    Sheu SY, Chou JH, Bontemps C, Elliott GN, Gross E, James EK, Sprent JI, Young JPW, Chen WM (2012) Burkholderia symbiotica sp. nov., isolated from root nodules of Mimosa spp. native to north east Brazil. Int J Syst Evol Microbiol 62:2272–2278PubMedCrossRefGoogle Scholar
  62. 62.
    Sheu SY, Chou JH, Bontemps C, Elliott GN, Gross E, dos Reis FB Jr., Melkonian R, Moulin L, James EK, Sprent JI, Young JPW, Chen WM (2012) Burkholderia diazotrophica sp. nov., isolated from root nodules of Mimosa spp. Int J Syst Evol Microbiol. doi: 10.1099/ijs.0.039859-0
  63. 63.
    Spilker T, Baldwin A, Bumford A, Dowson CG, Mahenthiralingam E, LiPuma J (2009) Expanded multilocus sequence typing for Burkholderia species. J Clin Microbiol 47:2607–2610PubMedCrossRefGoogle Scholar
  64. 64.
    Storms V, Van Den Vraken N, Coenye T, Mahenthiralingam E, LiPuma JJ, Gillis M, Vandamme P (2004) Polyphasic characterisation of Burkholderia cepacia-like isolates leading to the emended description of Burkholderia pyrrocinia. Syst Appl Microbiol 27:517–526PubMedCrossRefGoogle Scholar
  65. 65.
    Talbi C, Delgado MJ, Girard L, Ramírez-Trujillo A, Caballero-Mellado J, Bedmar EJ (2008) Burkholderia phymatum strains capable of nodulating Phaseolus vulgaris are present in Moroccan soils. Appl Environ Microbiol 76:4587–4591CrossRefGoogle Scholar
  66. 66.
    Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distances, and maximum parsimony methods. Mol Biol Evol 28:2731–2739PubMedCrossRefGoogle Scholar
  67. 67.
    Tindall BJ, Rossello-Mora R, Busse HJ, Ludwig W, Kampfer P (2010) Notes on the characterization of prokaryote strains for taxonomic purposes. Int J Syst Evol Microbiol 60:249–266PubMedCrossRefGoogle Scholar
  68. 68.
    Urakami T, Ito-Yoshida C, Araki H, Kijima T, Suzuki KI, Komagata K (1994) Transfer of Pseudomonas plantarii and Pseudomonas glumae to Burkholderia as Burkholderia spp. and description of Burkholderia vandii sp. nov. Int J Syst Bacteriol 44:235–245CrossRefGoogle Scholar
  69. 69.
    Ussery DW, Kiil K, Lagesen K, Sicheritz-Ponten T, Bohlin J, Wassenaar TM (2009) The genus Burkholderia: analysis of 56 genomic sequences. Genome Dyn 6:140–157PubMedCrossRefGoogle Scholar
  70. 70.
    Valdes M, Perez NO, Estrada-de los Santos P, Caballero-Mellado J, Peña-Cabriales JJ, Normand P, Hirsch AM (2005) Non-Frankia actinomycetes isolated from surface-sterilized roots of Casuarina equisetifolia fix nitrogen. Appl Environ Microbiol 71:460–466PubMedCrossRefGoogle Scholar
  71. 71.
    Valverde A, Delvasto P, Peix A, Velazquez E, Santa-Regina I, Ballester A, Rodriguez-Barrueco C, Garcia-Balboa C, Igual JM (2006) Burkholderia ferrariae sp. nov., isolated from an iron ore in Brazil. Int J Syst Evol Microbiol 56:2421–2425PubMedCrossRefGoogle Scholar
  72. 72.
    Vandamme P, Holmes B, Vancanneyt M, Coenye T, Hoste B, Coopman R, Revets H, Lauwers S, Gillis M, Kersters K, Govan JRW (1997) Occurrence of multiple genomovars of Burkholderia cepacia in cystic fibrosis patients and proposal of Burkholderia multivorans sp. nov. Int J Syst Bacteriol 47:1188–1200PubMedCrossRefGoogle Scholar
  73. 73.
    Vandamme P, Mahenthiralingam E, Holmes B, Coenye T, Hoste B, De Vos P, Henry D, Speert DP (2000) Identification and population structure of Burkholderia stabilis sp. nov. (formerly Burkholderia cepacia genomovar IV). J Clin Microbiol 38:1042–1047PubMedGoogle Scholar
  74. 74.
    Vandamme P, Goris J, Chen WM, de Vos P, Willems A (2002) Burkholderia tuberum sp. nov. and Burkholderia phymatum sp. nov. nodulate the roots of tropical legumes. Syst Appl Microbiol 25:507–512PubMedCrossRefGoogle Scholar
  75. 75.
    Vandamme P, Henry D, Coenye T, Nzula S, Vancanneyt M, LiPuma JJ, Speert DP, Govan JRW, Mahenthiralingam E (2002) Burkholderia anthina sp. nov. and Burkholderia pyrrocinia, two additional Burkholderia cepacia complex bacteria, may confound results of new molecular diagnostics tools. FEMS Immunol Med Microbiol 33:143–149PubMedCrossRefGoogle Scholar
  76. 76.
    Vandamme P, Holmes B, Coenye T, Goris J, Mahenthiralingam E, LiPuma J, Govan JRW (2003) Burkholderia cenocepacia sp. nov., a new twist to an old story. Res Microbiol 154:91–96PubMedCrossRefGoogle Scholar
  77. 77.
    Vandamme P, Govan J, LiPuma J (2007) Diversity and role of Burkholderia spp. In: Coenye T, Vandamme P (eds) Burkholderia molecular microbiology and genomics. Horizon Bioscience, Norfolk, pp 1–28Google Scholar
  78. 78.
    Vandamme P, Opelt K, Knochel N, Berg C, Schonmann S, De Brandt E, Eberl L, Falsen E, Berg G (2007) Burkholderia bryophila sp. nov. and Burkholderia megapolitana sp. nov., moss associated species with antifungal and plant-growth-promoting properties. Int J Syst Evol Microbiol 57:2228–2235PubMedCrossRefGoogle Scholar
  79. 79.
    Vandamme P, Dawyndt P (2011) Classification and identification of the Burkholderia cepacia complex: past, present and future. Syst Appl Microbiol 34:87–95PubMedCrossRefGoogle Scholar
  80. 80.
    Vanlaere E, LiPuma JJ, Baldwin A, Henry D, De Brandt E, Speert D, Mahenthiralingam E, Dowson C, Vandamme P (2008) Burkholderia latens sp. nov., Burkholderia diffusa sp. nov., Burkholderia arboris sp. nov., Burkholderia seminalis sp. nov. and Burkholderia metallica sp. nov., novel species within the Burkholderia cepacia complex. Int J Syst Evol Microbiol 58:1580–1590PubMedCrossRefGoogle Scholar
  81. 81.
    Vanlaere E, van der Meer JR, Falsen E, Salles JF, de Brandt E, Vandamme P (2008) Burkholderia sartisoli sp. nov., isolated from a polycyclic aromatic hydrocarbon-contaminated soil. Int J Syst Evol Microbiol 58:420–423PubMedCrossRefGoogle Scholar
  82. 82.
    Vanlaere E, Baldwin A, Gevers D, Henry D, De Brandt E, LiPuma JJ, Mahenthiralingam E, Speert DP, Dowson C, Vandamme P, Taxon K (2009) a complex within the Burkholderia cepacia complex, comprises at least two novel species, Burkholderia contaminans sp. nov. and Burkholderia lata sp. nov. Int J Syst Evol Microbiol 59:102–111PubMedCrossRefGoogle Scholar
  83. 83.
    Vermis K, Coenye T, LiPuma JJ, Mahenthiralingam E, Nelis HJ, Vandamme P (2004) Proposal to accommodate Burkholderia cepacia genomovars VI as Burkholderia dolosa sp. nov. Int J Syst Evol Microbiol 54:689–691PubMedCrossRefGoogle Scholar
  84. 84.
    Viallard V, Poirier I, Cournoyer B, Haurat J, Wiebkin S, Ophel-Keller K, Balandreau J (1998) Burkholderia graminis sp. nov., a rhizospheric Burkholderia species, and reassessment of [Pseudomonas] phenazinium, [Pseudomonas] pyrrocinia and [Pseudomonas] glathei as Burkholderia. Int J Syst Bacteriol 48:549–563PubMedCrossRefGoogle Scholar
  85. 85.
    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., and acidic-tolerant endosymbiont that nodulates endemic genistoid legumes (Papilionoideae: Genisteae) from the Canary Islands, along with Bradyrhizobium japonicum bv. genistearum, Bradyrhizobium geno-species alpha and Bradyrhizobium genospecies beta. Int J Syst Evol Microbiol 55:569–575PubMedCrossRefGoogle Scholar
  86. 86.
    Weinberg JB, Alexander BD, Majure JM, Williams LW, Kim JY, Vandamme P, LiPuma JJ (2008) Burkholderia glumae infection in an infant with chronic granulomatous disease. J Clin Microbiol 45:662–665CrossRefGoogle Scholar
  87. 87.
    Whitlock GC, Estes DM, Torres AG (2007) Glanders: off to the races with Burkholderia mallei. FEMS Microbiol Lett 277:115–122PubMedCrossRefGoogle Scholar
  88. 88.
    Wong-Villarreal A, Caballero-Mellado J (2010) Rapid identification of nitrogen-fixing and legume-nodulating Burkholderia species based on PCR 16S rRNA species-specific oligonucleotides. Syst Appl Microbiol 33:35–43PubMedCrossRefGoogle Scholar
  89. 89.
    Yabuuchi E, Yoshimasa K, Oyaizu H, Yano I, Hotta H, Hashimoto Y, Ezaki T, Arakawa M (1992) Proposal of Burkholderia gen. nov. and transfer of seven species of the genus Pseudomonas homology group II to the new genus, with the type species Burkholderia cepacia (Palleroni and Holmes 1981) comb. nov. Microbiol Immunol 36:1251–1275PubMedGoogle Scholar
  90. 90.
    Yabuuchi E, Kosako Y, Yano I, Hotta H, Nishiuchi Y (1995) Transfers of two Burkholderia and an Alcaligenes species to Ralstonia gen. nov.: proposal of Ralstonia pickettii (Ralston, Palleroni and Doudoroff 1973) comb. nov., Ralstonia solanacearum (Smith 1896) comb. nov. and Ralstonia eutropha (Davis 1969) comb. nov. Microbiol Immunol 39:897–904PubMedGoogle Scholar
  91. 91.
    Yang Z (1996) Among-site rate variation and its impact on phylogenetic analyses. Trends Ecol Evol 11:367–372PubMedCrossRefGoogle Scholar
  92. 92.
    Yoo SH, Kim BY, Weon HY, Kwon SW, Go SJ, Stackebrandt E (2007) Burkholderia soli sp. nov., isolated from soil cultivated with Korean ginseng. Int J Syst Evol Microbiol 57:122–125PubMedCrossRefGoogle Scholar
  93. 93.
    Zhang H, Hanada S, Shigematsu T, Shibuya K, Kamagata Y, Kanagawa T, Kurane R (2000) Burkholderia kururiensis sp. nov., a trichloroethylene (TCE)-degrading bacterium isolated from an aquifer polluted with TCE. Int J Syst Evol Microbiol 50:743–749PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2013

Authors and Affiliations

  • Paulina Estrada-de los Santos
    • 1
    • 2
    Email author
  • Pablo Vinuesa
    • 1
  • Lourdes Martínez-Aguilar
    • 1
  • Ann M. Hirsch
    • 3
  • Jesús Caballero-Mellado
    • 1
  1. 1.Centro de Ciencias GenómicasUniversidad Nacional Autónoma de MéxicoCuernavacaMexico
  2. 2.Departamento de MicrobiologíaEscuela Nacional de Ciencias Biológicas, I.P.N.MexicoMexico
  3. 3.Department of Molecular, Cell and Developmental Biology, Molecular Biology InstituteUniversity of California, Los AngelesLos AngelesUSA

Personalised recommendations