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Microbial Ecology

, Volume 63, Issue 2, pp 249–266 | Cite as

Common Features of Environmental and Potentially Beneficial Plant-Associated Burkholderia

  • Zulma Rocío Suárez-Moreno
  • Jesús Caballero-Mellado
  • Bruna G. Coutinho
  • Lucia Mendonça-Previato
  • Euan K. James
  • Vittorio VenturiEmail author
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Abstract

The genus Burkholderia comprises more than 60 species isolated from a wide range of niches. Although they have been shown to be diverse and ubiquitously distributed, most studies have thus far focused on the pathogenic species due to their clinical importance. However, the increasing number of recently described Burkholderia species associated with plants or with the environment has highlighted the division of the genus into two main clusters, as suggested by phylogenetical analyses. The first cluster includes human, animal, and plant pathogens, such as Burkholderia glumae, Burkholderia pseudomallei, and Burkholderia mallei, as well as the 17 defined species of the Burkholderia cepacia complex, while the other, more recently established cluster comprises more than 30 non-pathogenic species, which in most cases have been found to be associated with plants, and thus might be considered to be potentially beneficial. Several species from the latter group share characteristics that are of use when associating with plants, such as a quorum sensing system, the presence of nitrogen fixation and/or nodulation genes, and the ability to degrade aromatic compounds. This review examines the commonalities in this growing subgroup of Burkholderia species and discusses their prospective biotechnological applications.

Keywords

Sugarcane Rhizobium Quorum Sense Burkholderia Quorum Sense System 
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.

Notes

Acknowledgments

ZRSM was financially supported by an ICGEB fellowship. BGC PhD programme is funded by CAPES (Brazil). We thank Paulina Estrada de Los Santos for reading the manuscript and useful suggestions. During the preparation of this review, our dear friend and colleague Jesús Caballero-Mellado unexpectedly passed away; his warm friendship, availability, and important contributions in this research field are very sadly missed. EKJ thanks NERC (UK) for funds, and numerous colleagues and collaborators for participating in the NERC-funded Beta-rhizobia project.

References

  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.
    Aizawa T, Ve NB, 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
  3. 3.
    Aizawa T, Ve NB, 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
  4. 4.
    Aizawa T, Vijarnsorn P, Nakajima M, Sunairi M (2011) Burkholderia bannensis sp. nov., an 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
  5. 5.
    Anandham R, Indira Gandhi P, Kwon SW, Sa TM, Kim YK, Jee HJ (2009) Mixotrophic metabolism in Burkholderia kururiensis subsp. thiooxydans subsp. nov., a facultative chemolithoautotrophic thiosulfate oxidizing bacterium isolated from rhizosphere soil and proposal for classification of the type strain of Burkholderia kururiensis as Burkholderia kururiensis subsp. kururiensis subsp. nov. Arch Microbiol 191:885–894PubMedCrossRefGoogle Scholar
  6. 6.
    Atkinson S, Williams P (2009) Quorum sensing and social networking in the microbial world. J R Soc Interface 6:959–978PubMedCrossRefGoogle Scholar
  7. 7.
    Azevedo JL, Maccheroni W Jr, Pereira JO, Araújo WL (2000) Endophytic microorganisms: a review on insect control and recent advances on tropical plants. Electron J Biotechnol 3:40–65Google Scholar
  8. 8.
    Bacon C, Hinton D (2006) Bacterial endophytes: the endophytic niche, its occupants, and its utility. In: Gnanamanickam S (ed) Plant-associated bacteria, vol. 1. Springer, Dordrecht, pp 155–194CrossRefGoogle Scholar
  9. 9.
    Baldani JI, Caruso L, Baldani VLD, Goi SR, Dobereiner J (1997) Recent advances in BNF with non-legume plants. Soil Biol Biochem 29:911–922CrossRefGoogle Scholar
  10. 10.
    Baldani VL, Oliveira E, Balota E, Baldani JI, Kirchhof G, Döbereiner J (1997) Burkholderia brasilensis sp. nov. uma nova espécie de bactéria diazotrófica endofítica. An Acad Bras Cienc 69:1Google Scholar
  11. 11.
    Ballard RW, Palleroni NJ, Doudoroff M, Stanier RY, Mandel M (1970) Taxonomy of the aerobic pseudomonads: Pseudomonas cepacia, P. marginata, P. alliicola and P. caryophylli. J Gen Microbiol 60:199–214PubMedGoogle Scholar
  12. 12.
    Barka EA, Belarbi A, Hachet C, Nowak J, Audran JC (2000) Enhancement of in vitro growth and resistance to gray mould of Vitis vinifera co-cultured with plant growth-promoting rhizobacteria. FEMS Microbiol Lett 186:91–95PubMedCrossRefGoogle Scholar
  13. 13.
    Barka EA, Gognies S, Nowak J, Audran JC, Belarbi A (2002) Inhibitory effect of endophyte bacteria on Botrytis cinerea and its influence to promote the grapevine growth. Biological Control 24:135–142CrossRefGoogle Scholar
  14. 14.
    Barrett CF, Parker MA (2006) Coexistence of Burkholderia, Cupriavidus, and Rhizobium sp. nodule bacteria on two Mimosa spp. in Costa Rica. Appl Environ Microbiol 72:1198–1206PubMedCrossRefGoogle Scholar
  15. 15.
    Barrett CF, Parker MA (2005) Prevalence of Burkholderia sp. nodule symbionts on four mimosoid legumes from Barro Colorado Island, Panama. Syst Appl Microbiol 28:57–65PubMedCrossRefGoogle Scholar
  16. 16.
    Barriuso J, Pereyra MT, Lucas Garcia JA, Megias M, Gutierrez Manero FJ, Ramos B (2005) Screening for putative PGPR to improve establishment of the symbiosis Lactarius deliciosus–Pinus sp. Microb Ecol 50:82–89PubMedCrossRefGoogle Scholar
  17. 17.
    Barriuso J, Ramos Solano B, Fray RG, Camara M, Hartmann A, Gutierrez Manero FJ (2008) Transgenic tomato plants alter quorum sensing in plant growth-promoting rhizobacteria. Plant Biotechnol J 6:442–452PubMedCrossRefGoogle Scholar
  18. 18.
    Bloemberg GV, Lugtenberg BJ (2001) Molecular basis of plant growth promotion and biocontrol by rhizobacteria. Curr Opin Plant Biol 4:343–350PubMedCrossRefGoogle Scholar
  19. 19.
    Bontemps C, Elliott GN, Simon MF, Dos Reis Junior FB, Gross E, Lawton RC, Neto NE, de Fatima LM, De Faria SM, Sprent JI, James EK, Young JP (2010) Burkholderia species are ancient symbionts of legumes. Mol Ecol 19:44–52PubMedCrossRefGoogle Scholar
  20. 20.
    Bopp LH (1986) Degradation of highly chlorinated PCBs by Pseudomonas strain LB400. J Ind Microbiol Biotechnol 1:23–29Google Scholar
  21. 21.
    Bramer CO, Vandamme P, da Silva LF, Gomez JG, Steinbuchel A (2001) Polyhydroxyalkanoate-accumulating bacterium isolated from soil of a sugar-cane plantation in Brazil. Int J Syst Evol Microbiol 51:1709–1713PubMedCrossRefGoogle Scholar
  22. 22.
    Burkholder WH (1950) Sour skin, a bacterial rot of onion bulbs. Phytopathology 40:115–117Google Scholar
  23. 23.
    Burkholder WH (1942) Three bacterial plant pathogens:Phytomonas caryophylli, sp.n., Phytomonas alliicola sp.n., and Phytomonas manihotis (Artaud-Berthet et Bondar) Viegas. Phytopathology 32:141–149Google Scholar
  24. 24.
    Caballero-Mellado J, Martinez-Aguilar L, Paredes-Valdez G, Santos PE (2004) Burkholderia unamae sp. nov., an N2-fixing rhizospheric and endophytic species. Int J Syst Evol Microbiol 54:1165–1172PubMedCrossRefGoogle Scholar
  25. 25.
    Caballero-Mellado J, Onofre-Lemus J, Estrada-de Los Santos P, Martinez-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
  26. 26.
    Chain PS, Denef VJ, Konstantinidis KT, Vergez LM, Agullo L, Reyes VL, Hauser L, Cordova M, Gomez L, Gonzalez M, Land M, Lao V, Larimer F, LiPuma JJ, Mahenthiralingam E, Malfatti SA, Marx CJ, Parnell JJ, Ramette A, Richardson P, Seeger M, Smith D, Spilker T, Sul WJ, Tsoi TV, Ulrich LE, Zhulin IB, Tiedje JM (2006) Burkholderia xenovorans LB400 harbors a multi-replicon, 9.73-Mbp genome shaped for versatility. Proc Natl Acad Sci USA 103:15280–15287PubMedCrossRefGoogle Scholar
  27. 27.
    Chen W-M, de Faria SM, Chou J-H, 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
  28. 28.
    Chen W-M, de Faria SM, James EK, Elliott GN, Lin K-Y, Chou J-H, Sheu S-Y, 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
  29. 29.
    Chen W-M, James EK, Coenye T, Chou J-H, Barrios E, de Faria SM, Elliott GN, Sheu S-Y, 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
  30. 30.
    Chen WM, de Faria SM, Straliotto R, Pitard RM, Simoes-Araujo JL, Chou JH, Chou YJ, Barrios E, Prescott AR, Elliott GN, Sprent JI, Young JP, James EK (2005) Proof that Burkholderia strains form effective symbioses with legumes: a study of novel Mimosa-nodulating strains from South America. Appl Environ Microbiol 71:7461–7471PubMedCrossRefGoogle Scholar
  31. 31.
    Chen WM, James EK, Chou JH, Sheu SY, Yang SZ, Sprent JI (2005) Beta-rhizobia from Mimosa pigra, a newly discovered invasive plant in Taiwan. New Phytol 168:661–675PubMedCrossRefGoogle Scholar
  32. 32.
    Chen WM, James EK, Prescott AR, Kierans M, Sprent JI (2003) Nodulation of Mimosa spp. by the beta-proteobacterium Ralstonia taiwanensis. Mol Plant Microbe Interact 16:1051–1061PubMedCrossRefGoogle Scholar
  33. 33.
    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 a cystic fibrosis patient. Int J Syst Evol Microbiol 51:1729–1735PubMedCrossRefGoogle Scholar
  34. 34.
    Chen WM, Moulin L, Bontemps C, Vandamme P, Bena G, Boivin-Masson C (2003) Legume symbiotic nitrogen fixation by beta-proteobacteria is widespread in nature. J Bacteriol 185:7266–7272PubMedCrossRefGoogle Scholar
  35. 35.
    Coenye T (2010) Social interactions in the Burkholderia cepacia complex: biofilms and quorum sensing. Future Microbiol 5:1087–1099PubMedCrossRefGoogle Scholar
  36. 36.
    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
  37. 37.
    Coenye T, Laevens S, Willems A, Ohlen M, Hannant W, Govan JR, 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
  38. 38.
    Compant S, Clement C, Sessitsch A (2010) Plant growth-promoting bacteria in the rhizo- and endosphere of plants: their role, colonization, mechanisms involved and prospects for utilization. Soil Biol Biochem 42:669–678CrossRefGoogle Scholar
  39. 39.
    Compant S, Nowak J, Coenye T, Clement C, Ait Barka E (2008) Diversity and occurrence of Burkholderia spp. in the natural environment. FEMS Microbiol Rev 32:607–626PubMedCrossRefGoogle Scholar
  40. 40.
    Compant S, Reiter B, Sessitsch A, Nowak J, Clement C, Ait Barka E (2005) Endophytic colonization of Vitis vinifera L. by plant growth-promoting bacterium Burkholderia sp. strain PsJN. Appl Environ Microbiol 71:1685–1693PubMedCrossRefGoogle Scholar
  41. 41.
    Cunha MV, Sousa SA, Leitao JH, Moreira LM, Videira PA, Sa-Correia I (2004) Studies on the involvement of the exopolysaccharide produced by cystic fibrosis-associated isolates of the Burkholderia cepacia complex in biofilm formation and in persistence of respiratory infections. J Clin Microbiol 42:3052–3058PubMedCrossRefGoogle Scholar
  42. 42.
    Dos Reis FB Jr, Simon MF, Gross E, Boddey RM, Elliott GN, Neto NE, de Loureiro MF, de Queiroz LP, Scotti MR, Chen WM, Noren A, Rubio MC, de Faria SM, Bontemps C, Goi SR, Young JP, Sprent JI, James EK (2010) Nodulation and nitrogen fixation by Mimosa spp. in the Cerrado and Caatinga biomes of Brazil. New Phytol 186:934–946PubMedCrossRefGoogle Scholar
  43. 43.
    Duerkop BA, Ulrich RL, Greenberg EP (2007) Octanoyl-homoserine lactone is the cognate signal for Burkholderia mallei BmaR1-BmaI1 quorum sensing. J Bacteriol 189:5034–5040PubMedCrossRefGoogle Scholar
  44. 44.
    Duerkop BA, Varga J, Chandler JR, Peterson SB, Herman JP, Churchill ME, Parsek MR, Nierman WC, Greenberg EP (2009) Quorum-sensing control of antibiotic synthesis in Burkholderia thailandensis. J Bacteriol 191:3909–3918PubMedCrossRefGoogle Scholar
  45. 45.
    Eberl L (2006) Quorum sensing in the genus Burkholderia. Int J Med Microbiol 296:103–110PubMedCrossRefGoogle Scholar
  46. 46.
    Egland KA, Greenberg EP (1999) Quorum sensing in Vibrio fischeri: elements of the luxl promoter. Mol Microbiol 31:1197–1204PubMedCrossRefGoogle Scholar
  47. 47.
    Elliott GN, Chen WM, Bontemps C, Chou JH, Young JP, Sprent JI, James EK (2007) Nodulation of Cyclopia spp. (Leguminosae, Papilionoideae) by Burkholderia tuberum. Ann Bot (Lond) 100:1403–1411CrossRefGoogle Scholar
  48. 48.
    Elliott 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 173:168–180PubMedCrossRefGoogle Scholar
  49. 49.
    Elliott GN, Chou JH, Chen WM, Bloemberg GV, Bontemps C, Martinez-Romero E, Velazquez E, Young JP, Sprent JI, James EK (2009) Burkholderia spp. are the most competitive symbionts of Mimosa, particularly under N-limited conditions. Environ Microbiol 11:762–778PubMedCrossRefGoogle Scholar
  50. 50.
    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
  51. 51.
    Ferreira AS, Leitao JH, Silva IN, Pinheiro PF, Sousa SA, Ramos CG, Moreira LM (2010) Distribution of cepacian biosynthesis genes among environmental and clinical Burkholderia strains and role of cepacian exopolysaccharide in resistance to stress conditions. Appl Environ Microbiol 76:441–450PubMedCrossRefGoogle Scholar
  52. 52.
    Frommel MI, Nowak J, Lazarovits G (1991) Growth enhancement and developmental modifications of in vitro grown potato (Solanum tuberosum spp. tuberosum) as affected by a nonfluorescent Pseudomonas sp. Plant Physiol 96:928–936PubMedCrossRefGoogle Scholar
  53. 53.
    Garau G, Yates R, Deiana P, Howieson JG (2009) Novel strains of nodulating Burkholdeira have a role in nitrogen fixation with papilionoid herbaceous legumes adapted to acid, infertile soil. Soil Biol Biochem 41:125–134CrossRefGoogle Scholar
  54. 54.
    Gilad J (2007) Burkholderia mallei and Burkholderia pseudomallei: the causative micro-organisms of glanders and melioidosis. Recent Pat Antiinfect Drug Discov 2:233–241PubMedCrossRefGoogle Scholar
  55. 55.
    Gillis M, Van Van T, Bardin R, Goor M, Herbar 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
  56. 56.
    Glick BR (1995) The enhancement of plant growth by free-living bacteria. Can J Microbiol 41:109–117CrossRefGoogle Scholar
  57. 57.
    Godoy D, Randle G, Simpson AJ, Aanensen DM, Pitt TL, Kinoshita R, Spratt BG (2003) Multilocus sequence typing and evolutionary relationships among the causative agents of melioidosis and glanders, Burkholderia pseudomallei and Burkholderia mallei. J Clin Microbiol 41:2068–2079PubMedCrossRefGoogle Scholar
  58. 58.
    Goris J, De Vos P, Caballero-Mellado J, Park J, Falsen E, Quensen JF 3rd, Tiedje JM, Vandamme P (2004) Classification of the biphenyl- and polychlorinated biphenyl-degrading strain LB400 and relatives as Burkholderia xenovorans sp. nov. Int J Syst Evol Microbiol 54:1677–1681PubMedCrossRefGoogle Scholar
  59. 59.
    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
  60. 60.
    Govindarajan M, Balandreau J, Kwon S-W, Weon H-Y, Lakshminarasimhan C (2008) Effects of the inoculation of Burkholderia vietnamensis and related endophytic diazotrophic bacteria on grain yield of rice. Microb Ecol 55:21–37PubMedCrossRefGoogle Scholar
  61. 61.
    Graham PH (2008) Ecology of the root-nodule bacteria of legumes. In: Dilworth M, James EK, Sprent JI, Newton WE (eds) Nitrogen-fixing legume symbioses. Springer, DordrechtGoogle Scholar
  62. 62.
    Gyaneshwar P, Hirsch AM, Moulin I, Chen WM, Elliott GN, Bontemps C, Estrada de Los Santos P, Gross E, Dos Reis Junior FB, Sprent JI, Young JP, James EK (2011) Legume-nodulating betaproteobacteria: diversity, host range and future prospects. Mol Plant Microbe Interact (in press)Google Scholar
  63. 63.
    Gyaneshwar P, James EK, Mathan N, Reddy PM, Reinhold-Hurek B, Ladha JK (2001) Endophytic colonization of rice by a diazotrophic strain of Serratia marcescens. J Bacteriol 183:2634–2645PubMedCrossRefGoogle Scholar
  64. 64.
    Gyaneshwar P, James EK, Reddy PM, Ladha JK (2002) Herbaspirillum colonization increases growth and nitrogen accumulation in aluminium tolerant rice varieties. New Phytol 154:131–146CrossRefGoogle Scholar
  65. 65.
    Hallack LF, Passos DS, Mattos KA, Agrellos OA, Jones C, Mendonca-Previato L, Previato JO, Todeschini AR (2009) Structural elucidation of the repeat unit in highly branched acidic exopolysaccharides produced by nitrogen fixing Burkholderia. Glycobiology 20:338–347PubMedCrossRefGoogle Scholar
  66. 66.
    Hallmann J (1997) Bacterial endophytes in agricultural crops. Can J Microbiol 43:895–914CrossRefGoogle Scholar
  67. 67.
    Huber B, Riedel K, Hentzer M, Heydorn A, Gotschlich A, Givskov M, Molin S, Eberl L (2001) The cep quorum-sensing system of Burkholderia cepacia H111 controls biofilm formation and swarming motility. Microbiology 147:2517–2528PubMedGoogle Scholar
  68. 68.
    Hurek T, Reinhold-Hurek B, Turner GL, Bergersen FJ (1994) Augmented rates of respiration and efficient nitrogen fixation at nanomolar concentrations of dissolved O2 in hyperinduced Azoarcus sp. strain BH72. J Bacteriol 176:4726–4733PubMedGoogle Scholar
  69. 69.
    Isles A, Maclusky I, Corey M, Gold R, Prober C, Fleming P, Levison H (1984) Pseudomonas cepacia infection in cystic fibrosis: an emerging problem. J Pediatr 104:206–210PubMedCrossRefGoogle Scholar
  70. 70.
    Izumi H, Cairney JW, Killham K, Moore E, Alexander I, Anderson I (2010) Bacteria associated with ectomycorrhizas of slash pine (Pinus elliotti) in south-eastern Queensland, Australia. FEMS Microbiol Lett 282:196–204CrossRefGoogle Scholar
  71. 71.
    James EK (2000) Nitrogen fixation in endophytici and associative symbiosis. Field Crop Res 65:197–209CrossRefGoogle Scholar
  72. 72.
    James EK, Gyaneshwar P, Mathan N, Barraquio WL, Reddy PM, Iannetta PP, Olivares FL, Ladha JK (2002) Infection and colonization of rice seedlings by the plant growth-promoting bacterium Herbaspirillum seropedicae Z67. Mol Plant Microbe Interact 15:894–906PubMedCrossRefGoogle Scholar
  73. 73.
    Jonsson V (1970) Proposal of a new species Pseudomonas kingii. Int J Syst Bacteriol 20:255–257CrossRefGoogle Scholar
  74. 74.
    Kellogg ST, Chatterjee DK, Chakrabarty AM (1981) Plasmid-assisted molecular breeding: new technique for enhanced biodegradation of persistent toxic chemicals. Science 214:1133–1135PubMedCrossRefGoogle Scholar
  75. 75.
    Kilbane JJ, Chatterjee DK, Karns JS, Kellogg ST, Chakrabarty AM (1982) Biodegradation of 2,4,5-trichlorophenoxyacetic acid by a pure culture of Pseudomonas cepacia. Appl Environ Microbiol 44:72–78PubMedGoogle Scholar
  76. 76.
    Kim H-B, Park M-J, Yang H-C, An D-S, Jin H-Z, Yang D-C (2006) Burkholderia ginsengisoli sp. nov., a beta-glucosidase-producing bacterium isolated from soil of a ginseng field. Int J Syst Evol Microbiol 56:2529–2533PubMedCrossRefGoogle Scholar
  77. 77.
    Kiratisin P, Sanmee S (2008) Roles and interactions of Burkholderia pseudomallei BpsIR quorum-sensing system determinants. J Bacteriol 190:7291–7297PubMedCrossRefGoogle Scholar
  78. 78.
    Leigh J, Coplin D (1992) Exopolysaccharides in plant–bacterial interactions. Annu Rev Microbiol 46:307–346PubMedCrossRefGoogle Scholar
  79. 79.
    Leitao JH, Sousa SA, Ferreira AS, Ramos CG, Silva IN, Moreira LM (2010) Pathogenicity, virulence factors, and strategies to fight against Burkholderia cepacia complex pathogens and related species. Appl Microbiol Biotechnol 87:31–40PubMedCrossRefGoogle Scholar
  80. 80.
    Lerat E, Moran NA (2004) The evolutionary history of quorum-sensing systems in bacteria. Mol Biol Evol 21:903–913PubMedCrossRefGoogle Scholar
  81. 81.
    Lim JH, Baek SH, Lee ST (2008) Burkholderia sediminicola sp. nov., isolated from freshwater sediment. Int J Syst Evol Microbiol 58:565–569PubMedCrossRefGoogle Scholar
  82. 82.
    Liu XY, Wu W, Wang ET, Zhang B, Macdermott J, Chen WX (2011) Phylogenetic relationships and diversity of beta-rhizobia associated with Mimosa spp. grown in Sishuangbanna, China. Int J Syst Evol Microbiol 61:334–342PubMedCrossRefGoogle Scholar
  83. 83.
    Lugtenberg B, Kamilova F (2009) Plant-growth-promoting rhizobacteria. Annu Rev Microbiol 63:541–556PubMedCrossRefGoogle Scholar
  84. 84.
    Luvizzotto D, Marcon J, Andreote FD, Dini-Andreote F, Neves AC, Araujo WL, Pizzirani-Kleiner AA (2010) Genetic diversity and plant-growth related features of Burkholderia spp. from sugarcane roots. World J Microbiol Biotechnol 25:175–180Google Scholar
  85. 85.
    Mahenthiralingam E, Baldwin A, Dowson CG (2008) Burkholderia cepacia complex bacteria: opportunistic pathogens with important natural biology. JAppl Microbiol 104:1539–1551CrossRefGoogle Scholar
  86. 86.
    Mahenthiralingam E, Urban TA, Goldberg JB (2005) The multifarious, multireplicon Burkholderia cepacia complex. Nat Rev Microbiol 3:144–156PubMedCrossRefGoogle Scholar
  87. 87.
    Malott RJ, Baldwin A, Mahenthiralingam E, Sokol PA (2005) Characterization of the cciIR quorum-sensing system in Burkholderia cenocepacia. Infect Immun 73:4982–4992PubMedCrossRefGoogle Scholar
  88. 88.
    Malott RJ, Sokol PA (2007) Expression of the bviIR and cepIR quorum-sensing systems of Burkholderia vietnamiensis. J Bacteriol 189:3006–3016PubMedCrossRefGoogle Scholar
  89. 89.
    Marin VA, Teixeira KR, Baldani JI (2003) Characterization of amplified polymerase chain reaction glnB and nifH gene fragments of nitrogen-fixing Burkholderia species. Lett Appl Microbiol 36:77–82PubMedCrossRefGoogle Scholar
  90. 90.
    Martinez-Aguilar L, Diaz R, Pena-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
  91. 91.
    Masson-Boivin C, Giraud E, Perret X, Batut J (2009) Establishing nitrogen-fixing symbiosis with legumes: how many rhizobium recipes? Trends Microbiol 17:458–466PubMedCrossRefGoogle Scholar
  92. 92.
    Mattos KA, Jones C, Heise N, Previato JO, Mendonca-Previato L (2001) Structure of an acidic exopolysaccharide produced by the diazotrophic endophytic bacterium Burkholderia brasiliensis. Eur J Biochem 268:3174–3179PubMedCrossRefGoogle Scholar
  93. 93.
    Mattos KA, Padua VL, Romeiro A, Hallack LF, Neves BC, Ulisses TM, Barros CF, Todeschini AR, Previato JO, Mendonca-Previato L (2008) Endophytic colonization of rice (Oryza sativa L.) by the diazotrophic bacterium Burkholderia kururiensis and its ability to enhance plant growth. An Acad Bras Cienc 80:477–493PubMedCrossRefGoogle Scholar
  94. 94.
    Mattos KA, Todeschini AR, Heise N, Jones C, Previato JO, Mendonca-Previato L (2005) Nitrogen-fixing bacterium Burkholderia brasiliensis produces a novel yersiniose A-containing O-polysaccharide. Glycobiology 15:313–321PubMedCrossRefGoogle Scholar
  95. 95.
    Menard A, Monnez C, de Los E, Santos P, Segonds C, Caballero-Mellado J, Lipuma JJ, Chabanon G, Cournoyer B (2007) Selection of nitrogen-fixing deficient Burkholderia vietnamiensis strains by cystic fibrosis patients: involvement of nif gene deletions and auxotrophic mutations. Environ Microbiol 9:1176–1185PubMedCrossRefGoogle Scholar
  96. 96.
    Mendes R, Pizzirani-Kleiner AA, Araujo WL, Raaijmakers JM (2007) Diversity of cultivated endophytic bacteria from sugarcane: genetic and biochemical characterization of Burkholderia cepacia complex isolates. Appl Environ Microbiol 73:7259–7267PubMedCrossRefGoogle Scholar
  97. 97.
    Morris MB, Roberts JB (1959) A Group of Pseudomonads able to synthesize poly-[beta]-hydroxybutyric acid. Nature 183:1538–1539PubMedCrossRefGoogle Scholar
  98. 98.
    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
  99. 99.
    Mukhopadhyay K, Garrison NK, Hinton DM, Bacon CW, Khush GS, Peck HD, Datta N (1996) Identification and characterization of bacterial endophytes of rice. Mycopathologia 134:151–159PubMedCrossRefGoogle Scholar
  100. 100.
    Muresu R, Polone E, Sulas L, Baldan B, Tondello A, Delogu G, Cappuccinelli P, Alberghini S, Benhizia Y, Benhizia H, Benguedouar A, Mori B, Calamassi R, Dazzo FB, Squartini A (2008) Coexistence of predominantly nonculturable rhizobia with diverse, endophytic bacterial taxa within nodules of wild legumes. FEMS Microbiol Ecol 63:383–400PubMedCrossRefGoogle Scholar
  101. 101.
    Ng WL, Bassler BL (2009) Bacterial quorum-sensing network architectures. Annu Rev Genet 43:197–222PubMedCrossRefGoogle Scholar
  102. 102.
    Nowak J, Asiedu SK, Lazarovits G (1995) Enhancement of in vitro growth and transplant stress tolerance of potato and vegetable plants co-cultured with a plant growth promoting rhizobacterium. In: Chagvardieff CP (ed) Ecophysiology and photosynthetic in vitro cultures, vol. 173-180. CEA, Aix-en-ProvenceGoogle Scholar
  103. 103.
    Nowak J, Shulaev V (2003) Priming for transplant stress resistance in in vitro propagation. In Vitro Cell Dev Biol Plant 39:107–124Google Scholar
  104. 104.
    Omarjee J, Balandreau J, Spaull VW, Cadet P (2008) Relationships between Burkholderia populations and platn parasitic nematodes in sugarcane. Appl Soil Ecol 39:1CrossRefGoogle Scholar
  105. 105.
    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
  106. 106.
    Otsuka Y, Muramatsu Y, Nakagawa Y, Matsuda M, Nakamura M, Murata H (2011) Burkholderia oxyphila sp. nov., a bacterium isolated from acidic forest soil that catabolizes (+)-catechin and its putative aromatic derivatives. Int J Syst Evol Microbiol 61:249–254PubMedCrossRefGoogle Scholar
  107. 107.
    Palleroni NJ (2005) The genus Burkholderia. In: Brenner DJ, Krieg NR, Garrity GM, Staley JT (eds) Bergey’s manual of systematic bacteriology: the Proteobacteria; the Alpha-, Beta-, Delta-, and Epsilonproteobacteria, vol 2. Springer, East Lansing, pp 575–600CrossRefGoogle Scholar
  108. 108.
    Palleroni NJ, Kunisawa R, Contopoulou R, Doudoroff M (1973) Nucleic acid homologies in the genus Pseudomonas. Int J Syst Bacteriol 23:333–339CrossRefGoogle Scholar
  109. 109.
    Parke JL, Gurian-Sherman D (2001) Diversity of the Burkholderia cepacia complex and implications for risk assessment of biological control strains. Annu Rev Phytopathol 39:225–258PubMedCrossRefGoogle Scholar
  110. 110.
    Payne GW, Ramette A, Rose HL, Weightman AJ, Jones TH, Tiedje JM, Mahenthiralingam E (2006) Application of a recA gene-based identification approach to the maize rhizosphere reveals novel diversity in Burkholderia species. FEMS Microbiol Lett 259:126–132PubMedCrossRefGoogle Scholar
  111. 111.
    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
  112. 112.
    Pellock BJ, Cheng HP, Walker GC (2000) Alfalfa root nodule invasion efficiency is dependent on Sinorhizobium meliloti polysaccharides. J Bacteriol 182:4310–4318PubMedCrossRefGoogle Scholar
  113. 113.
    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. Appl Environ Microbiol 72:3103–3110PubMedCrossRefGoogle Scholar
  114. 114.
    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 sugar cane and maize. Int J Syst Evol Microbiol 56:1931–1937PubMedCrossRefGoogle Scholar
  115. 115.
    Pillay VK, Nowak J (1997) Inoculum density, temperature, and genotype effects on in vitro growth promotion and epiphytic and endophytic colonization of tomato (Lycopersicon esculentum L.) seedlings inoculated with a pseudomonad bacterium. Can J Microbiol 43:354–361CrossRefGoogle Scholar
  116. 116.
    Pol-Fachin L, Serrato RV, Verli H (2010) Solution conformation and dynamics of exopolysaccharides from Burkholderia species. Carbohydr Res 345:1922–1931PubMedCrossRefGoogle Scholar
  117. 117.
    Rasolomampianina R, Bailly R, Fetiarison R, Rabevohitra R, Bena G, Ramaroson M, Raherimandimby R, Moulin I, De Lajudie P, Dreyfus B, Avarre JC (2005) Nitrogen-fixing nodules from rose wood legume trees Dalbergia spp. endemic to Madagascar host seven different genera belonging to B-Proteobacteria. Mol Ecol 14:4135–4146PubMedCrossRefGoogle Scholar
  118. 118.
    Redfearn MS, Palleroni NJ, Stanier RY (1966) A comparative study of Pseudomonas pseudomallei and Bacillus mallei. J Gen Microbiol 43:293–313PubMedGoogle Scholar
  119. 119.
    Reis VM, Estrada-de los Santos P, Tenorio-Salgado S, Vogel J, Stoffels M, Guyon S, Mavingui P, Baldani VL, 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
  120. 120.
    Ribeiro GX, Fernandes ME, De Aquino AM, Zilli JE, Rumjanek NG (2010) The structural and functional biodiversity of soil: an interdisciplinary vision of conservation agriculture in Brazil. In: Dion P (ed) Soil biology and agriculture in the tropics, vol. 1. Springer, Quebec, pp 65–80Google Scholar
  121. 121.
    Rosenblueth M, Martinez-Romero E (2006) Bacterial endophytes and their interactions with hosts. Mol Plant Microbe Interact 19:827–837PubMedCrossRefGoogle Scholar
  122. 122.
    Ruff J, Denger K, Cook AM (2003) Sulphoacetaldehyde acetyltransferase yields acetyl phosphate: purification from Alcaligenes defragrans and gene clusters in taurine degradation. Biochem J 369:275–285PubMedCrossRefGoogle Scholar
  123. 123.
    Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425PubMedGoogle Scholar
  124. 124.
    Salles JF, van Elsas JD, van Veen JA (2006) Effect of agricultural management regime on Burkholderia community structure in soil. Microb Ecol 52:267–279PubMedCrossRefGoogle Scholar
  125. 125.
    Seeger M, Gonzalez M, Camara B, Munoz L, Ponce E, Mejias L, Mascayano C, Vasquez Y, Sepulveda-Boza S (2003) Biotransformation of natural and synthetic isoflavonoids by two recombinant microbial enzymes. Appl Environ Microbiol 69:5045–5050PubMedCrossRefGoogle Scholar
  126. 126.
    Serrato RV, Sassaki GL, Cruz LM, Pedrosa FO, Gorin PAJ, Iacomini M (2006) Culture conditions for the production of an acidic exopolysaccharide by the nitrogen-fixing bacterium Burkholderia tropica. Can J Microbiol 52:489–493PubMedCrossRefGoogle Scholar
  127. 127.
    Sessitsch A, Coenye T, Sturz AV, Vandamme P, Barka EA, Salles JF, Van Elsas JD, Faure D, Reiter B, Glick BR, Wang-Pruski G, Nowak J (2005) Burkholderia phytofirmans sp. nov., a novel plant-associated bacterium with plant-beneficial properties. Int J Syst Evol Microbiol 55:1187–1192PubMedCrossRefGoogle Scholar
  128. 128.
    Siciliano SD, Fortin N, Mihoc A, Wisse G, Labelle S, Beaumier D, Ouellette D, Roy R, Whyte LG, Banks MK, Schwab P, Lee K, Greer CW (2001) Selection of specific endophytic bacterial genotypes by plants in response to soil contamination. Appl Environ Microbiol 67:2469–2475PubMedCrossRefGoogle Scholar
  129. 129.
    Silipo A, Ierano T, Lanzetta R, Molinaro A, Parrilli M (2008) The structure of the O-chain polysaccharide from the Gram-negative endophytic bacterium Burkholderia phytofirmans strain PsJN. Eur J Organic Chem 2008:2303–2308CrossRefGoogle Scholar
  130. 130.
    Smith DJ, Martin VJ, Mohn WW (2004) A cytochrome P450 involved in the metabolism of abietane diterpenoids by Pseudomonas abietaniphila BKME-9. J Bacteriol 186:3631–3639PubMedCrossRefGoogle Scholar
  131. 131.
    Smith DJ, Park J, Tiedje JM, Mohn WW (2007) A large gene cluster in Burkholderia xenovorans encoding abietane diterpenoid catabolism. J Bacteriol 189:6195–6204PubMedCrossRefGoogle Scholar
  132. 132.
    Smith DJ, Patrauchan MA, Florizone C, Eltis LD, Mohn WW (2008) Distinct roles for two CYP226 family cytochromes P450 in abietane diterpenoid catabolism by Burkholderia xenovorans LB400. J Bacteriol 190:1575–1583PubMedCrossRefGoogle Scholar
  133. 133.
    Spilker T, Baldwin A, Bumford A, Dowson CG, Mahenthiralingam E, Lipuma JJ (2009) Expanded multilocus sequence typing for Burkholderia species. J Clin Microbiol 47:2607–2610PubMedCrossRefGoogle Scholar
  134. 134.
    Sprent JI (2009) Legume nodulation: A global perspective. Wiley, ChichesterGoogle Scholar
  135. 135.
    Stanier RY, Palleroni NJ, Doudoroff M (1966) The aerobic pseudomonads: a taxonomic study. J Gen Microbiol 43:159–271PubMedGoogle Scholar
  136. 136.
    Suarez Moreno ZR, Devescovi G, Myers M, Hallack L, Mendonca-Previato L, Caballero-Mellado J, Venturi V (2010) Commonalities and differences in N-acyl homoserine lactone quorum sensing regulation in the species cluster of beneficial plant associated Burkholderia. Appl Environ Microbiol 76:4302–4317PubMedCrossRefGoogle Scholar
  137. 137.
    Suarez-Moreno ZR, Caballero-Mellado J, Venturi V (2008) The new group of non-pathogenic plant-associated nitrogen-fixing Burkholderia spp. shares a conserved quorum-sensing system, which is tightly regulated by the RsaL repressor. Microbiology 154:2048–2059PubMedCrossRefGoogle Scholar
  138. 138.
    Sun Y, Cheng Z, Glick BR (2009) The presence of a 1-aminocyclopropane-1-carboxylate (ACC) deaminase deletion mutation alters the physiology of the endophytic plant growth-promoting bacterium Burkholderia phytofirmans PsJN. FEMS Microbiol Lett 296:131–136PubMedCrossRefGoogle Scholar
  139. 139.
    Talbi C, Delgado MJ, Girard L, Ramirez-Trujillo A, Caballero-Mellado J, Bedmar EJ (2010) Burkholderia phymatum strains capable of nodulating Phaseolus vulgaris are present in Moroccan soils. Appl Environ Microbiol 76:4587–4591PubMedCrossRefGoogle Scholar
  140. 140.
    Tayeb LA, Lefevre M, Passet V, Diancourt L, Brisse S, Grimont PA (2008) Comparative phylogenies of Burkholderia, Ralstonia, Comamonas, Brevundimonas and related organisms derived from rpoB, gyrB and rrs gene sequences. Res Microbiol 159:169–177PubMedCrossRefGoogle Scholar
  141. 141.
    Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680PubMedCrossRefGoogle Scholar
  142. 142.
    Van Tran V, Berger O, Ngo K, Balandreau J, Heulin T (2000) Repeated beneficial effects of rice inoculation with a strain of Burkholderia vietnamiensis on early and late yield components in low fertility sulphate acid soils. Plant Soil 218:273–284CrossRefGoogle Scholar
  143. 143.
    Trognitz F, Scherwinski K, Fekete A, Schmidt S, Eberl L, Rodewald J, Schmid M, Compant S, Hartmann A, Schmitt-Kopplin P, Trognitz B, Sessitsch A (2009) Interaction between potato and the endophyte Burkholderia phytofirmans. Tag Vereinig Pflanzenzücht Saatgutkaufl Österr 59:63–66Google Scholar
  144. 144.
    Ulrich RL, Deshazer D, Brueggemann EE, Hines HB, Oyston PC, Jeddeloh JA (2004) Role of quorum sensing in the pathogenicity of Burkholderia pseudomallei. J Med Microbiol 53:1053–1064PubMedCrossRefGoogle Scholar
  145. 145.
    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
  146. 146.
    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
  147. 147.
    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
  148. 148.
    Vandamme P, Holmes B, Vancanneyt M, Coenye T, Hoste B, Coopman R, Revets H, Lauwers S, Gillis M, Kersters K, Govan JR (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
  149. 149.
    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
  150. 150.
    Vanhaverbeke C, Heyraud A, Mazeau K (2003) Conformational analysis of the exopolysaccharide from Burkholderia caribensis strain MWAP71: impact on the interaction with soils. Biopolymers 69:480–497PubMedCrossRefGoogle Scholar
  151. 151.
    Vanlaere E, Baldwin A, Gevers D, Henry D, De Brandt E, LiPuma JJ, Mahenthiralingam E, Speert DP, Dowson C, Vandamme P (2009) Taxon K, 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
  152. 152.
    Vanlaere E, Sergeant K, Dawyndt P, Kallow W, Erhard M, Sutton H, Dare D, Devreese B, Samyn B, Vandamme P (2008) Matrix-assisted laser desorption ionisation-time-of of-flight mass spectrometry of intact cells allows rapid identification of Burkholderia cepacia complex. J Microbiol Methods 75:279–286PubMedCrossRefGoogle Scholar
  153. 153.
    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
  154. 154.
    Venturi V, Friscina A, Bertani I, Devescovi G, Aguilar C (2004) Quorum sensing in the Burkholderia cepacia complex. Res Microbiol 155:238–244PubMedCrossRefGoogle Scholar
  155. 155.
    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 48:549–563PubMedGoogle Scholar
  156. 156.
    Warmink JA, Nazir R, Corten B, van Elsas JD (2011) Hitchhikers on the fungal highway: the helper effect for bacterial migration via fungal hyphae. Soil Biol Biochem 43:760–765CrossRefGoogle Scholar
  157. 157.
    Warmink JA, van Elsas JD (2009) Migratory response of soil bacteria to Lyophyllum sp. strain Karsten in soil microcosms. Appl Environ Microbiol 75:2820–2830PubMedCrossRefGoogle Scholar
  158. 158.
    Warmink JA, van Elsas JD (2008) Selection of bacterial populations in the mycosphere of Laccaria proxima: is type III secretion involved? ISME J 2:887–900PubMedCrossRefGoogle Scholar
  159. 159.
    Weilharter A, Mitter B, Shin MV, Chain PS, Nowak J, Sessitsch A (2011) Complete genome sequence of the plant growth-promoting endophyte Burkholderia phytofirmans strain PsJN. J Bacteriol 193:3383–3384PubMedCrossRefGoogle Scholar
  160. 160.
    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
  161. 161.
    Yabuuchi E, Kosako Y, 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
  162. 162.
    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, LLC 2011

Authors and Affiliations

  • Zulma Rocío Suárez-Moreno
    • 1
    • 2
  • Jesús Caballero-Mellado
    • 3
  • Bruna G. Coutinho
    • 1
    • 6
  • Lucia Mendonça-Previato
    • 4
  • Euan K. James
    • 5
  • Vittorio Venturi
    • 1
    Email author
  1. 1.Bacteriology GroupInternational Centre for Genetic Engineering & BiotechnologyTriesteItaly
  2. 2.University of Medicine and Dentistry of New JerseyNewarkUSA
  3. 3.Centro de Ciencias GenómicasUniversidad Nacional Autónoma de MéxicoCuernavacaMéxico
  4. 4.Instituto de Biofísica Carlos Chagas Filho, Centro de Ciências da SaúdeUniversidade Federal do Rio de JaneiroRio de JaneiroBrazil
  5. 5.EPI DivisionThe James Hutton InstituteDundeeUK
  6. 6.The Capes FoundationMinistry of Education of BrazilBrasiliaBrazil

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