Advertisement

Applied Microbiology and Biotechnology

, Volume 100, Issue 12, pp 5215–5229 | Cite as

Burkholderia: an update on taxonomy and biotechnological potential as antibiotic producers

  • Eliza Depoorter
  • Matt J. Bull
  • Charlotte Peeters
  • Tom Coenye
  • Peter VandammeEmail author
  • Eshwar MahenthiralingamEmail author
Mini-Review

Abstract

Burkholderia is an incredibly diverse and versatile Gram-negative genus, within which over 80 species have been formally named and multiple other genotypic groups likely represent new species. Phylogenetic analysis based on the 16S rRNA gene sequence and core genome ribosomal multilocus sequence typing analysis indicates the presence of at least three major clades within the genus. Biotechnologically, Burkholderia are well-known for their bioremediation and biopesticidal properties. Within this review, we explore the ability of Burkholderia to synthesise a wide range of antimicrobial compounds ranging from historically characterised antifungals to recently described antibacterial antibiotics with activity against multiresistant clinical pathogens. The production of multiple Burkholderia antibiotics is controlled by quorum sensing and examples of quorum sensing pathways found across the genus are discussed. The capacity for antibiotic biosynthesis and secondary metabolism encoded within Burkholderia genomes is also evaluated. Overall, Burkholderia demonstrate significant biotechnological potential as a source of novel antibiotics and bioactive secondary metabolites.

Keywords

Burkholderia Taxonomy Phylogeny Genomics Antibiotic biosynthesis Secondary metabolism 

Notes

Acknowledgments

MB acknowledges funding from the Cardiff University Synthetic Biology initiative. CP is indebted to the Special Research Council of Ghent University. TC acknowledges funding from the Fund for Scientific Research-Flanders and the Interuniversity Attraction Poles Programme initiated by the Belgian Science Policy Office. EM is a recipient of funding from the Biotechnology and Biological Sciences Research Council (Grant BB/L021692/1). PV and TC acknowledge funding from the Industrial Research Fund of Ghent University (Grant F2015/IOF-ConcepTT/142).

Compliance with ethical standards

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. Agnoli K, Schwager S, Uehlinger S, Vergunst A, Viteri DF, Nguyen DT, Sokol PA, Carlier A, Eberl L (2012) Exposing the third chromosome of Burkholderia cepacia complex strains as a virulence plasmid. Mol Microbiol 83:362–378. doi: 10.1111/j.1365-2958.2011.07937.x PubMedCrossRefGoogle Scholar
  2. Angus AA, Agapakis CM, Fong S, Yerrapragada S, Estrada-de los Santos P, Yang P, Song N, Kano S, Caballero-Mellado J, de Faria SM, Dakora FD, Weinstock G, Hirsch AM (2014) Plant-associated symbiotic Burkholderia species lack hallmark strategies required in mammalian pathogenesis. PLoS One 9:e83779. doi: 10.1371/journal.pone.0083779 PubMedPubMedCentralCrossRefGoogle Scholar
  3. Azegami K, Nishiyama K, Watanabe Y, Kadota I, Ohuchi A, Fukazawa C (1987) Pseudomonas plantarii sp. nov., the causal agent of rice seedling blight. Int J Syst Bacteriol 37:144–152. doi: 10.1099/00207713-37-2-144 CrossRefGoogle Scholar
  4. 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 60:199–214. doi: 10.1099/00221287-60-2-199 PubMedCrossRefGoogle Scholar
  5. Bharti P, Anand V, Chander J, Singh IP, Singh TV, Tewari R (2012) Heat stable antimicrobial activity of Burkholderia gladioli OR1 against clinical drug resistant isolates. Indian J Med Res 135:666–671PubMedPubMedCentralGoogle Scholar
  6. Biggins JB, Liu X, Feng Z, Brady SF (2011) Metabolites from the induced expression of cryptic single operons found in the genome of Burkholderia pseudomallei. J Am Chem Soc 133:1638–1641. doi: 10.1021/ja1087369 PubMedCrossRefGoogle Scholar
  7. Biggins JB, Ternei MA, Brady SF (2012) Malleilactone, a polyketide synthase-derived virulence factor encoded by the cryptic secondary metabolome of Burkholderia pseudomallei group pathogens. J Am Chem Soc 134:13192–13195. doi: 10.1021/ja3052156 PubMedPubMedCentralCrossRefGoogle Scholar
  8. Blin K, Medema MH, Kazempour D, Fischbach MA, Breitling R, Takano E, Weber T (2013) antiSMASH 2.0—a versatile platform for genome mining of secondary metabolite producers. Nucleic Acids Res 41:W204–W212. doi: 10.1093/nar/gkt449 PubMedPubMedCentralCrossRefGoogle Scholar
  9. Boon C, Deng Y, Wang L-H, He Y, Xu J-L, Fan Y, Pan SQ, Zhang L-H (2008) A novel DSF-like signal from Burkholderia cenocepacia interferes with Candida albicans morphological transition. ISME J 2:27–36. doi: 10.1038/ismej.2007.76 PubMedCrossRefGoogle Scholar
  10. Bowers JH, Parke JL (1993) Epidemiology of Pythium damping-off and Aphanomyces root rot of peas after seed treatment with bacterial agents for biological control. Phytopathology 83:1466. doi: 10.1094/Phyto-83-1466 CrossRefGoogle Scholar
  11. Burkhead KD, Schisler DA, Slininger PJ (1994) Pyrrolnitrin production by biological control agent Pseudomonas cepacia B37w in culture and in colonized wounds of potatoes. Appl Environ Microbiol 60:2031–2039PubMedPubMedCentralGoogle Scholar
  12. Carlier AL, Eberl L (2012) The eroded genome of a Psychotria leaf symbiont: hypotheses about lifestyle and interactions with its plant host. Environ Microbiol 14:2757–2769. doi: 10.1111/j.1462-2920.2012.02763.x PubMedCrossRefGoogle Scholar
  13. Cartwright DK, Chilton WS, Benson DM (1995) Pyrrolnitrin and phenazine production by Pseudomonas cepacia, strain 5.5B, a biocontrol agent of Rhizoctonia solani. Appl Microbiol Biotechnol 43:211–216. doi: 10.1007/BF00172814 CrossRefGoogle Scholar
  14. Chapalain A, Vial L, Laprade N, Dekimpe V, Perreault J, Déziel E (2013) Identification of quorum sensing-controlled genes in Burkholderia ambifaria. Microbiologyopen 2:226–242. doi: 10.1002/mbo3.67 PubMedPubMedCentralCrossRefGoogle Scholar
  15. Chen R, Barphagha IK, Karki HS, Ham JH (2012) Dissection of quorum-sensing genes in Burkholderia glumae reveals non-canonical regulation and the new regulatory gene tofM for toxoflavin production. PLoS One 7:e52150. doi: 10.1371/journal.pone.0052150 PubMedPubMedCentralCrossRefGoogle Scholar
  16. Cimermancic P, Medema MH, Claesen J, Kurita K, Wieland Brown LC, Mavrommatis K, Pati A, Godfrey PA, Koehrsen M, Clardy J, Birren BW, Takano E, Sali A, Linington RG, Fischbach MA (2014) Insights into secondary metabolism from a global analysis of prokaryotic biosynthetic gene clusters. Cell 158:412–421. doi: 10.1016/j.cell.2014.06.034 PubMedPubMedCentralCrossRefGoogle Scholar
  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 49:37–42. doi: 10.1099/00207713-49-1-37
  18. Coenye T, Falsen E, Hoste B, Ohlen M, Goris J, Govan J, Gillis M, Vandamme P (2000) Description of Pandoraea gen. nov. with Pandoraea apista sp. nov., Pandoraea pulmonicola sp. nov., Pandoraea pnomenusa sp. nov., Pandoraea sputorum sp. nov. and Pandoraea norimbergensis comb. nov. Int J Syst Evol Microbiol 50:887–899. doi: 10.1099/00207713-50-2-887 PubMedCrossRefGoogle Scholar
  19. Coenye T, Laevens S, Gillis M, Vandamme P (2001a) Genotypic and chemotaxonomic evidence for the reclassification of Pseudomonas woodsii (Smith 1911) Stevens 1925 as Burkholderia andropogonis (Smith 1911) Gillis et al. 1995. Int J Syst Evol Microbiol 51:183–185. doi: 10.1099/00207713-51-1-183 PubMedCrossRefGoogle Scholar
  20. Coenye T, Laevens S, Willems A, Ohlen M, Hannant W, Govan J, Gillis M, Falsen E, Vandamme P (2001b) 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 51:1099–1107. doi: 10.1099/00207713-51-3-1099 PubMedCrossRefGoogle Scholar
  21. Coenye T, Goris J, Spilker T, Lipuma JJ, Vandamme P (2002) Characterization of unusual bacteria isolated from respiratory secretions of cystic fibrosis patients and description of Inquilinus limosus gen. nov., sp. nov. J Clin Microbiol 40:2062–2069. doi: 10.1128/JCM.40.6.2062 PubMedPubMedCentralCrossRefGoogle Scholar
  22. Conway B-A, Greenberg EP (2002) Quorum-sensing signals and quorum-sensing genes in Burkholderia vietnamiensis. J Bacteriol 184:1187–1191. doi: 10.1128/jb.184.4.1187-1191.2002 PubMedPubMedCentralCrossRefGoogle Scholar
  23. Coutinho BG, Mitter B, Talbi C, Sessitsch A, Bedmar EJ, Halliday N, James EK, Camara M, Venturi V (2013) Regulon studies and in planta role of the BraI/R quorum-sensing system in the plant-beneficial Burkholderia cluster. Appl Environ Microbiol 79:4421–4432. doi: 10.1128/AEM.00635-13 PubMedPubMedCentralCrossRefGoogle Scholar
  24. Currie B (2015) Melioidosis: evolving concepts in epidemiology, pathogenesis, and treatment. Semin Respir Crit Care Med 36:111–125. doi: 10.1055/s-0034-1398389 PubMedCrossRefGoogle Scholar
  25. Deng Y, Wu J, Eberl L, Zhang L-H (2010) Structural and functional characterization of diffusible signal factor family quorum-sensing signals produced by members of the Burkholderia cepacia complex. Appl Environ Microbiol 76:4675–4683. doi: 10.1128/AEM.00480-10 PubMedPubMedCentralCrossRefGoogle Scholar
  26. Deris ZZ, Van Rostenberghe H, Habsah H, Noraida R, Tan GC, Chan YY, Rosliza AR, Ravichandran M (2010) First isolation of Burkholderia tropica from a neonatal patient successfully treated with imipenem. Int J Infect Dis 14:e73–e74. doi: 10.1016/j.ijid.2009.03.005 PubMedCrossRefGoogle Scholar
  27. 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 191:3909–3918. doi: 10.1128/JB.00200-09 PubMedPubMedCentralCrossRefGoogle Scholar
  28. El-Banna N, Winkelmann G (1998) Pyrrolnitrin from Burkholderia cepacia: antibiotic activity against fungi and novel activities against streptomycetes. J Appl Microbiol 85:69–78. doi: 10.1046/j.1365-2672.1998.00473.x PubMedCrossRefGoogle Scholar
  29. Estrada-de los Santos P, Vinuesa P, Martínez-Aguilar L, Hirsch AM, Caballero-Mellado J (2013) Phylogenetic analysis of Burkholderia species by multilocus sequence analysis. Curr Microbiol 67:51–60. doi: 10.1007/s00284-013-0330-9 PubMedCrossRefGoogle Scholar
  30. Estrada-de los Santos P, Rojas-Rojas FU, Tapia-García EY, Vásquez-Murrieta MS, Hirsch AM (2015) To split or not to split: an opinion on dividing the genus Burkholderia. Ann Microbiol. doi: 10.1007/s13213-015-1183-1 Google Scholar
  31. Franke J, Ishida K, Hertweck C (2012) Genomics-driven discovery of burkholderic acid, a noncanonical, cryptic polyketide from human pathogenic Burkholderia species. Angew Chemie - Int Ed 51:11611–11615. doi: 10.1002/anie.201205566 CrossRefGoogle Scholar
  32. Garrity GM, Oren A (2015) List of new names and new combinations previously effectively, but not validly, published. Int J Syst Evol Microbiol 65:2017–2025. doi: 10.1099/ijs.0.000317 CrossRefGoogle Scholar
  33. Gerrits GP, Klaassen C, Coenye T, Vandamme P, Meis JF (2005) Burkholderia fungorum septicemia. Emerg Infect Dis 11:1115–1117. doi: 10.3201/eid1107.041290 PubMedPubMedCentralCrossRefGoogle Scholar
  34. Groenhagen U, Baumgartner R, Bailly A, Gardiner A, Eberl L, Schulz S, Weisskopf L (2013) Production of bioactive volatiles by different Burkholderia ambifaria strains. J Chem Ecol 39:892–906. doi: 10.1007/s10886-013-0315-y PubMedCrossRefGoogle Scholar
  35. Groll M, Schellenberg B, Bachmann AS, Archer CR, Huber R, Powell TK, Lindow S, Kaiser M, Dudler R (2008) A plant pathogen virulence factor inhibits the eukaryotic proteasome by a novel mechanism. Nature 452:755–758. doi: 10.1038/nature06782 PubMedCrossRefGoogle Scholar
  36. Gyaneshwar P, Hirsch AM, Moulin L, Chen W-M, Elliott GN, Bontemps C, Estrada-de los Santos P, Gross E, dos Reis FB, Sprent JI, Young JPW, James EK (2011) Legume-nodulating Betaproteobacteria: diversity, host range, and future prospects. Mol Plant-Microbe Interact 24:1276–1288. doi: 10.1094/MPMI-06-11-0172 PubMedCrossRefGoogle Scholar
  37. Heungens K, Parke JL (2000) Zoospore homing and infection events: effects of the biocontrol bacterium Burkholderia cepacia AMMDR1 on two oomycete pathogens of pea (Pisum sativum L.). Appl Environ Microbiol 66:5192–5200. doi: 10.1128/AEM.66.12.5192-5200.2000 PubMedPubMedCentralCrossRefGoogle Scholar
  38. Heungens K, Parke JL (2001) Postinfection biological control of oomycete pathogens of pea by Burkholderia cepacia AMMDR1. Phytopathology 91:383–391. doi: 10.1094/PHYTO.2001.91.4.383 PubMedCrossRefGoogle Scholar
  39. Ho Y-N, Huang C-C (2015) Draft genome sequence of Burkholderia cenocepacia strain 869T2, a plant-beneficial endophytic bacterium. Genome Announc 3:e01327–15. doi: 10.1128/genomeA.01327-15 PubMedCrossRefGoogle Scholar
  40. Hwang J, Chilton W, Benson D (2002) Pyrrolnitrin production by Burkholderia cepacia and biocontrol of Rhizoctonia stem rot of poinsettia. Biol Control 25:56–63. doi: 10.1016/S1049-9644(02)00044-0 CrossRefGoogle Scholar
  41. Ishida K, Lincke T, Behnken S, Hertweck C (2010) Induced biosynthesis of cryptic polyketide metabolites in a Burkholderia thailandensis quorum sensing mutant. J Am Chem Soc 132:13966–13968. doi: 10.1021/ja105003g PubMedCrossRefGoogle Scholar
  42. Jeong Y, Kim J, Kim S, Kang Y, Nagamatsu T, Hwang I (2003) Toxoflavin produced by Burkholderia glumae causing rice grain rot is responsible for inducing bacterial wilt in many field crops. Plant Dis 87:890–895. doi: 10.1094/PDIS.2003.87.8.890 CrossRefGoogle Scholar
  43. Jiao Y, Yoshihara T, Ishikuri S, Uchino H, Ichihara A (1996) Structural identification of cepaciamide A, a novel fungitoxic compound from Pseudomonas cepacia D-202. Tetrahedron Lett 37:1039–1042. doi: 10.1016/0040-4039(95)02342-9 CrossRefGoogle Scholar
  44. Jolley KA, Maiden MC (2010) BIGSdb: scalable analysis of bacterial genome variation at the population level. BMC Bioinformatics 11:595. doi: 10.1186/1471-2105-11-595 PubMedPubMedCentralCrossRefGoogle Scholar
  45. Jolley KA, Bliss CM, Bennett JS, Bratcher HB, Brehony C, Colles FM, Wimalarathna H, Harrison OB, Sheppard SK, Cody AJ, Maiden MCJ (2012) Ribosomal multilocus sequence typing: universal characterization of bacteria from domain to strain. Microbiology 158:1005–1015. doi: 10.1099/mic.0.055459-0 PubMedPubMedCentralCrossRefGoogle Scholar
  46. Keum YS (2009) Effects of nutrients on quorum signals and secondary metabolite productions of Burkholderia sp. O33. J Microbiol Biotechnol. doi: 10.4014/jmb.0901.465 PubMedGoogle Scholar
  47. Kikuchi Y, Hosokawa T, Fukatsu T (2011) An ancient but promiscuous host–symbiont association between Burkholderia gut symbionts and their heteropteran hosts. ISME J 5:446–460. doi: 10.1038/ismej.2010.150 PubMedPubMedCentralCrossRefGoogle Scholar
  48. Kim J, Kim JG, Kang Y, Jang JY, Jog GJ, Lim JY, Kim S, Suga H, Nagamatsu T, Hwang I (2004) Quorum sensing and the LysR-type transcriptional activator ToxR regulate toxoflavin biosynthesis and transport in Burkholderia glumae. Mol Microbiol 54:921–934. doi: 10.1111/j.1365-2958.2004.04338.x PubMedCrossRefGoogle Scholar
  49. Kirinuki T, Ichiba T, Katayama K (1984) General survey of action site of altericidins on metabolism of Alternaria kikuchiana and Ustilago maydis. J Pestic Sci 9:601–610. doi: 10.1584/jpestics.9.601 CrossRefGoogle Scholar
  50. Knappe TA, Linne U, Zirah S, Rebuffat S, Xie X, Marahiel MA (2008) Isolation and structural characterization of capistruin, a lasso peptide predicted from the genome sequence of Burkholderia thailandensis E264. J Am Chem Soc 130:11446–11454. doi: 10.1021/ja802966g PubMedCrossRefGoogle Scholar
  51. Lemaire B, Robbrecht E, van Wyk B, Van Oevelen S, Verstraete B, Prinsen E, Smets E, Dessein S (2011) Identification, origin, and evolution of leaf nodulating symbionts of Sericanthe (Rubiaceae). J Microbiol 49:935–941. doi: 10.1007/s12275-011-1163-5 PubMedCrossRefGoogle Scholar
  52. Lemaire B, van Oevelen S, de Block P, Verstraete B, Smets E, Prinsen E, Dessein S (2012) Identification of the bacterial endosymbionts in leaf nodules of Pavetta (Rubiaceae). Int J Syst Evol Microbiol 62:202–209. doi: 10.1099/ijs.0.028019-0 PubMedCrossRefGoogle Scholar
  53. Lewenza S, Conway B, Greenberg EP, Sokol PA (1999) Quorum sensing in Burkholderia cepacia: identification of the LuxRI homologs CepRI. J Bacteriol 181:748–756PubMedPubMedCentralGoogle Scholar
  54. 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 53:1631–1636. doi: 10.1099/ijs.0.02456-0 PubMedCrossRefGoogle Scholar
  55. Lipuma JJ (2010) The changing microbial epidemiology in cystic fibrosis. Clin Microbiol Rev 23:299–323. doi: 10.1128/CMR.00068-09 PubMedPubMedCentralCrossRefGoogle Scholar
  56. Liu X, Cheng Y-QQ (2014) Genome-guided discovery of diverse natural products from Burkholderia sp. J Ind Microbiol Biotechnol 41:275–284. doi: 10.1007/s10295-013-1376-1 PubMedPubMedCentralCrossRefGoogle Scholar
  57. Liu X-Y, Li C-X, Luo X-J, Lai Q-L, Xu J-H (2014) Burkholderia jiangsuensis sp. nov., a methyl parathion degrading bacterium, isolated from methyl parathion contaminated soil. Int J Syst Evol Microbiol 64:3247–3253. doi: 10.1099/ijs.0.064444-0 PubMedCrossRefGoogle Scholar
  58. Lu S-E, Novak J, Austin FW, Gu G, Ellis D, Kirk M, Wilson-Stanford S, Tonelli M, Smith L (2009) Occidiofungin, a unique antifungal glycopeptide produced by a strain of Burkholderia contaminans. Biochemistry 48:8312–8321. doi: 10.1021/bi900814c PubMedPubMedCentralCrossRefGoogle Scholar
  59. Lu P, Zheng L-Q, Sun J-J, Liu H-M, Li S-P, Hong Q, Li W-J (2012) Burkholderia zhejiangensis sp. nov., a methyl-parathion-degrading bacterium isolated from a wastewater-treatment system. Int J Syst Evol Microbiol 62:1337–1341. doi: 10.1099/ijs.0.035428-0 PubMedCrossRefGoogle Scholar
  60. Mahenthiralingam E, Song L, Sass A, White J, Wilmot C, Marchbank A, Boaisha O, Paine J, Knight D, Challis GL (2011) Enacyloxins are products of an unusual hybrid modular polyketide synthase encoded by a cryptic Burkholderia ambifaria genomic island. Chem Biol 18:665–677. doi: 10.1016/j.chembiol.2011.01.020 PubMedCrossRefGoogle Scholar
  61. Majerczyk CD, Brittnacher MJ, Jacobs MA, Armour CD, Radey MC, Bunt R, Hayden HS, Bydalek R, Greenberg EP (2014) Cross-species comparison of the Burkholderia pseudomallei, Burkholderia thailandensis, and Burkholderia mallei quorum-sensing regulons. J Bacteriol 196:3862–3871. doi: 10.1128/JB.01974-14 PubMedPubMedCentralCrossRefGoogle Scholar
  62. Malott RJ, Baldwin A, Mahenthiralingam E, Sokol PA (2005) Characterization of the cciIR quorum-sensing system in Burkholderia cenocepacia. Infect Immun 73:4982–4992. doi: 10.1128/IAI.73.8.4982 PubMedPubMedCentralCrossRefGoogle Scholar
  63. Meyers E, Bisacchi GS, Dean L, Liu WC, Minassian B, Slusarchyk DS, Sykes RB, Tanaka SK, Trejo W (1987) Xylocandin: a new complex of antifungal peptides. I. Taxonomy, isolation and biological activity. J Antibiot (Tokyo) 40:1515–1519. doi: 10.7164/antibiotics.40.1515 CrossRefGoogle Scholar
  64. Mitchell RE, Greenwood DR, Sarojini V (2008) An antibacterial pyrazole derivative from Burkholderia glumae, a bacterial pathogen of rice. Phytochemistry 69:2704–2707. doi: 10.1016/j.phytochem.2008.08.013 PubMedCrossRefGoogle Scholar
  65. Moebius N, Ross C, Scherlach K, Rohm B, Roth M, Hertweck C (2012) Biosynthesis of the respiratory toxin bongkrekic acid in the pathogenic bacterium Burkholderia gladioli. Chem Biol 19:1164–1174. doi: 10.1016/j.chembiol.2012.07.022 PubMedCrossRefGoogle Scholar
  66. Moon SS, Kang PM, Park KS, Kim CH (1996) Plant growth promoting and fungicidal 4-quinolinones from Pseudomonas cepacia. Phytochemistry 42:365–368. doi: 10.1016/0031-9422(95)00897-7 CrossRefGoogle Scholar
  67. Nguyen T, Ishida K, Jenke-Kodama H, Dittmann E, Gurgui C, Hochmuth T, Taudien S, Platzer M, Hertweck C, Piel J (2008) Exploiting the mosaic structure of trans-acyltransferase polyketide synthases for natural product discovery and pathway dissection. Nat Biotechnol 26:225–233. doi: 10.1038/nbt1379 PubMedCrossRefGoogle Scholar
  68. Parke JL (1990) Population dynamics of Pseudomonas cepacia in the pea spermosphere in relation to biocontrol of Pythium. Phytopathology 80:1307. doi: 10.1094/Phyto-80-1307 CrossRefGoogle Scholar
  69. Parke JL, Gurian-sherman D (2001) Diversity of the Burkholderia cepacia complex and implications for risk assessment of biological control strains. Annu Rev Phytopathol 39:225–258. doi: 10.1146/annurev.phyto.39.1.225 PubMedCrossRefGoogle Scholar
  70. Parker WL, Rathnum ML, Seiner V, Trejo WH, Principe PA, Sykes RB (1984) Cepacin A and cepacin B, two new antibiotics produced by Pseudomonas cepacia. J Antibiot (Tokyo) 37:431–440CrossRefGoogle Scholar
  71. Parte AC (2014) LPSN—list of prokaryotic names with standing in nomenclature. Nucleic Acids Res 42:D613–D616. doi: 10.1093/nar/gkt1111 PubMedPubMedCentralCrossRefGoogle Scholar
  72. Partida-Martinez LP, Hertweck C (2005) Pathogenic fungus harbours endosymbiotic bacteria for toxin production. Nature 437:884–888. doi: 10.1038/nature03997 PubMedCrossRefGoogle Scholar
  73. Partida-Martinez LP, Groth I, Schmitt I, Richter W, Roth M, Hertweck C (2007) Burkholderia rhizoxinica sp. nov. and Burkholderia endofungorum sp. nov., bacterial endosymbionts of the plant-pathogenic fungus Rhizopus microsporus. Int J Syst Evol Microbiol 57:2583–2590. doi: 10.1099/ijs.0.64660-0 PubMedCrossRefGoogle Scholar
  74. Peeters C, Zlosnik JEA, Spilker T, Hird TJ, LiPuma JJ, Vandamme P (2013) Burkholderia pseudomultivorans sp. nov., a novel Burkholderia cepacia complex species from human respiratory samples and the rhizosphere. Syst Appl Microbiol 36:483–489. doi: 10.1016/j.syapm.2013.06.003 PubMedCrossRefGoogle Scholar
  75. Pérez-Pantoja D, Donoso R, Agulló L, Córdova M, Seeger M, Pieper DH, González B (2012) Genomic analysis of the potential for aromatic compounds biodegradation in Burkholderiales. Environ Microbiol 14:1091–1117. doi: 10.1111/j.1462-2920.2011.02613.x PubMedCrossRefGoogle Scholar
  76. Price MN, Dehal PS, Arkin AP (2010) FastTree 2—approximately maximum-likelihood trees for large alignments. PLoS One 5:e9490. doi: 10.1371/journal.pone.0009490 PubMedPubMedCentralCrossRefGoogle Scholar
  77. Pruesse E, Peplies J, Glockner FO (2012) SINA: accurate high-throughput multiple sequence alignment of ribosomal RNA genes. Bioinformatics 28:1823–1829. doi: 10.1093/bioinformatics/bts252 PubMedPubMedCentralCrossRefGoogle Scholar
  78. Ross C, Opel V, Scherlach K, Hertweck C (2014) Biosynthesis of antifungal and antibacterial polyketides by Burkholderia gladioli in coculture with Rhizopus microsporus. Mycoses 57:48–55. doi: 10.1111/myc.12246 PubMedCrossRefGoogle Scholar
  79. Ryan RP, McCarthy Y, Watt SA, Niehaus K, Dow JM (2009) Intraspecies signaling involving the diffusible signal factor BDSF (cis-2-dodecenoic acid) influences virulence in Burkholderia cenocepacia. J Bacteriol 191:5013–5019. doi: 10.1128/JB.00473-09 PubMedPubMedCentralCrossRefGoogle Scholar
  80. Sawana A, Adeolu M, Gupta RS (2014) Molecular signatures and phylogenomic analysis of the genus Burkholderia: proposal for division of this genus into the emended genus Burkholderia containing pathogenic organisms and a new genus Paraburkholderia gen. nov. harboring environmental species. Front Genet 5:1–22. doi: 10.3389/fgene.2014.00429
  81. Schellenberg B, Bigler L, Dudler R (2007) Identification of genes involved in the biosynthesis of the cytotoxic compound glidobactin from a soil bacterium. Environ Microbiol 9:1640–1650. doi: 10.1111/j.1462-2920.2007.01278.x PubMedCrossRefGoogle Scholar
  82. Scherlach K, Busch B, Lackner G, Paszkowski U, Hertweck C (2012) Symbiotic cooperation in the biosynthesis of a phytotoxin. Angew Chemie Int Ed 51:9615–9618. doi: 10.1002/anie.201204540 CrossRefGoogle Scholar
  83. Schmidt S, Blom JF, Pernthaler J, Berg G, Baldwin A, Mahenthiralingam E, Eberl L (2009) Production of the antifungal compound pyrrolnitrin is quorum sensing-regulated in members of the Burkholderia cepacia complex. Environ Microbiol 11:1422–1437. doi: 10.1111/j.1462-2920.2009.01870.x PubMedCrossRefGoogle Scholar
  84. Seyedsayamdost MR, Chandler JR, Blodgett JAV, Lima PS, Duerkop BA, Oinuma K-I, Greenberg EP, Clardy J (2010) Quorum-sensing-regulated bactobolin production by Burkholderia thailandensis E264. Org Lett 12:716–719. doi: 10.1021/ol902751x PubMedPubMedCentralCrossRefGoogle Scholar
  85. Sheu S-Y, Chou J-H, Bontemps C, Elliott GN, Gross E, James EK, Sprent JI, Young JPW, Chen W-M (2012) Burkholderia symbiotica sp. nov., isolated from root nodules of Mimosa spp. native to north-east Brazil. Int J Syst Evol Microbiol 62:2272–2278. doi: 10.1099/ijs.0.037408-0 PubMedCrossRefGoogle Scholar
  86. Shibata TF, Maeda T, Nikoh N, Yamaguchi K, Oshima K, Hattori M, Nishiyama T, Hasebe M, Fukatsu T, Kikuchi Y, Shigenobu S (2013) Complete genome sequence of Burkholderia sp. strain RPE64, bacterial symbiont of the bean bug Riptortus pedestris. Genome Announc 1:e00441–13. doi: 10.1128/genomeA.00441-13 PubMedPubMedCentralCrossRefGoogle Scholar
  87. Sokol PA, Malott RJ, Riedel K, Eberl L (2007) Communication systems in the genus Burkholderia: global regulators and targets for novel antipathogenic drugs. Future Microbiol 2:555–563. doi: 10.2217/17460913.2.5.555 PubMedCrossRefGoogle Scholar
  88. Solis R, Bertani I, Degrassi G, Devescovi G, Venturi V (2006) Involvement of quorum sensing and RpoS in rice seedling blight caused by Burkholderia plantarii. FEMS Microbiol Lett 259:106–112. doi: 10.1111/j.1574-6968.2006.00254.x PubMedCrossRefGoogle Scholar
  89. 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 154:2048–2059. doi: 10.1099/mic.0.2008/017780-0
  90. Suarez-Moreno ZR, Caballero-Mellado J, Coutinho BG, Mendonça-Previato L, James EK, Venturi V (2012) Common features of environmental and potentially beneficial plant-associated Burkholderia. Microb Ecol 63:249–266. doi: 10.1007/s00248-011-9929-1 PubMedCrossRefGoogle Scholar
  91. Talavera G, Castresana J (2007) Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Syst Biol 56:564–577. doi: 10.1080/10635150701472164 PubMedCrossRefGoogle Scholar
  92. Tamura K, Nei M (1993) Estimation of the number of base nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol Biol Evol 10:512–526PubMedGoogle Scholar
  93. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729. doi: 10.1093/molbev/mst197 PubMedPubMedCentralCrossRefGoogle Scholar
  94. Tawfik KA, Jeffs P, Bray B, Dubay G, Falkinham JO, Mesbah M, Youssef D, Khalifa S, Schmidt EW (2010) Burkholdines 1097 and 1229, potent antifungal peptides from Burkholderia ambifaria 2.2N. Org Lett 12:664–666. doi: 10.1021/ol9029269 PubMedCrossRefGoogle Scholar
  95. Thomson ELS, Dennis JJ (2012) A Burkholderia cepacia complex non-ribosomal peptide-synthesized toxin is hemolytic and required for full virulence. Virulence 3:286–298. doi: 10.4161/viru.19355 PubMedPubMedCentralCrossRefGoogle Scholar
  96. Tian Y, Kong BH, Liu SL, Li CL, Yu R, Liu L, Li YH (2013) Burkholderia grimmiae sp. nov., isolated from a xerophilous moss (Grimmia montana). Int J Syst Evol Microbiol 63:2108–3113. doi: 10.1099/ijs.0.045492-0 PubMedCrossRefGoogle Scholar
  97. Torbeck L, Raccasi D, Guilfoyle DE, Friedman RL, Hussong D (2011) Burkholderia cepacia: this decision is overdue. PDA J Pharm Sci Technol 65:535–543. doi: 10.5731/pdajpst.2011.00793 PubMedCrossRefGoogle Scholar
  98. Tran Van V, Berge O, Ngo Ke S, 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 of Vietnam. Plant Soil 218(2):273–284. doi: 10.1023/A:1014986916913 CrossRefGoogle Scholar
  99. Truong TT, Seyedsayamdost M, Greenberg EP, Chandler JR (2015) A Burkholderia thailandensis acyl-homoserine lactone-independent orphan LuxR homolog that activates production of the cytotoxin malleilactone. J Bacteriol 197:3456–3462. doi: 10.1128/JB.00425-15 PubMedPubMedCentralCrossRefGoogle Scholar
  100. van Oevelen S, de Wachter R, Vandamme P, Robbrecht E, Prinsen E (2004) “Candidatus Burkholderia calva” and “Candidatus Burkholderia nigropunctata” as leaf gall endosymbionts of African Psychotria. Int J Syst Evol Microbiol 54:2237–2239. doi: 10.1099/ijs.0.63188-0 PubMedCrossRefGoogle Scholar
  101. Vandamme P, Peeters C (2014) Time to revisit polyphasic taxonomy. Antonie Van Leeuwenhoek 106:57–65. doi: 10.1007/s10482-014-0148-x PubMedCrossRefGoogle Scholar
  102. Vandamme P, De Brandt E, Houf K, Salles JF, Dirk van Elsas J, Spilker T, LiPuma JJ (2013) Burkholderia humi sp. nov., Burkholderia choica sp. nov., Burkholderia telluris sp. nov., Burkholderia terrestris sp. nov. and Burkholderia udeis sp. nov.: Burkholderia glathei-like bacteria from soil and rhizosphere soil. Int J Syst Evol Microbiol 63:4707–4718. doi: 10.1099/ijs.0.048900-0
  103. 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 59:102–111. doi: 10.1099/ijs.0.001123-0 PubMedCrossRefGoogle Scholar
  104. Verstraete B, Van Elst D, Steyn H, Van Wyk B, Lemaire B, Smets E, Dessein S (2011) Endophytic bacteria in toxic south African plants: identification, phylogeny and possible involvement in gousiekte. PLoS One 6:e19265. doi: 10.1371/journal.pone.0019265 PubMedPubMedCentralCrossRefGoogle Scholar
  105. Verstraete B, Janssens S, Smets E, Dessein S (2013) Symbiotic ß-proteobacteria beyond legumes: Burkholderia in Rubiaceae. PLoS One 8:e55260. doi: 10.1371/journal.pone.0055260 PubMedPubMedCentralCrossRefGoogle Scholar
  106. Vial L, Groleau M-C, Dekimpe V, Déziel E (2007) Burkholderia diversity and versatility: an inventory of the extracellular products. J Microbiol Biotechnol 17:1407–1429PubMedGoogle Scholar
  107. Vial L, Chapalain A, Groleau MC, Déziel E (2011) The various lifestyles of the Burkholderia cepacia complex species: a tribute to adaptation. Environ Microbiol 13:1–12. doi: 10.1111/j.1462-2920.2010.02343.x PubMedCrossRefGoogle Scholar
  108. Vidal-Quist JC, O’Sullivan LA, Desert A, Fivian-Hughes AS, Millet C, Jones TH, Weightman AJ, Rogers HJ, Berry C, Mahenthiralingam E (2014) Arabidopsis thaliana and Pisum sativum models demonstrate that root colonization is an intrinsic trait of Burkholderia cepacia complex bacteria. Microbiology 160:373–384. doi: 10.1099/mic.0.074351-0 PubMedCrossRefGoogle Scholar
  109. Wang Z, Wu M (2013) A phylum-level bacterial phylogenetic marker database. Mol Biol Evol 30:1258–1262. doi: 10.1093/molbev/mst059 PubMedCrossRefGoogle Scholar
  110. Wang C, Henkes LM, Doughty LB, He M, Wang D, Meyer-Almes F-J, Cheng Y-Q (2011) Thailandepsins: bacterial products with potent histone deacetylase inhibitory activities and broad-spectrum antiproliferative activities. J Nat Prod 74:2031–2038. doi: 10.1021/np200324x PubMedPubMedCentralCrossRefGoogle Scholar
  111. Wang M, Hashimoto M, Hashidoko Y (2013) Repression of tropolone production and induction of a Burkholderia plantarii pseudo-biofilm by carot-4-en-9,10-diol, a cell-to-cell signaling disrupter produced by Trichoderma virens. PLoS One 8:e78024. doi: 10.1371/journal.pone.0078024 PubMedPubMedCentralCrossRefGoogle Scholar
  112. Weber T, Blin K, Duddela S, Krug D, Kim HU, Bruccoleri R, Lee SY, Fischbach MA, Muller R, Wohlleben W, Breitling R, Takano E, Medema MH (2015) antiSMASH 3.0—a comprehensive resource for the genome mining of biosynthetic gene clusters. Nucleic Acids Res 1–7. doi:  10.1093/nar/gkv437
  113. Whitehead NA, Barnard AML, Slater H, Simpson NJL, Salmond GPC (2001) Quorum-sensing in Gram-negative bacteria. FEMS Microbiol Rev 25:365–404. doi: 10.1111/j.1574-6976.2001.tb00583.x PubMedCrossRefGoogle Scholar
  114. Wilson MS, Herrick JB, Jeon CO, Hinman DE, Madsen EL (2003) Horizontal transfer of phnAc dioxygenase genes within one of two phenotypically and genotypically distinctive naphthalene-degrading guilds from adjacent soil environments. Appl Environ Microbiol 69:2172–2181. doi: 10.1128/AEM.69.4.2172-2181.2003 PubMedPubMedCentralCrossRefGoogle Scholar
  115. 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 36:1251–1275. doi: 10.1111/j.1348-0421.1992.tb02129.x PubMedCrossRefGoogle Scholar
  116. Yabuuchi E, Kosako Y, Yano I, Hotta H, Nishiuchi Y (1995) Transfer 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 39:897–904. doi: 10.1111/j.1348-0421.1995.tb03275.x
  117. Yoo S-H, Kim B-Y, Weon H-Y, Kwon S-W, Go S-J, Stackebrandt E (2007) Burkholderia soli sp. nov., isolated from soil cultivated with Korean ginseng. Int J Syst Evol Microbiol 57:122–125. doi: 10.1099/ijs.0.64471-0 PubMedCrossRefGoogle Scholar
  118. Yutin N, Puigbò P, Koonin EV, Wolf YI (2012) Phylogenomics of prokaryotic ribosomal proteins. PLoS One 7:e36972. doi: 10.1371/journal.pone.0036972 PubMedPubMedCentralCrossRefGoogle Scholar
  119. Zerikly M, Challis GL (2009) Strategies for the discovery of new natural products by genome mining. ChemBioChem 10:625–633. doi: 10.1002/cbic.200800389 PubMedCrossRefGoogle Scholar
  120. Zhou H, Yao F, Roberts DP, Lessie TG (2003) AHL-deficient mutants of Burkholderia ambifaria BC-F have decreased antifungal activity. Curr Microbiol 47:174–179. doi: 10.1007/s00284-002-3926-z PubMedCrossRefGoogle Scholar
  121. Zolg W, Ottow JCG (1975) Pseudomonas glathei sp. nov., a new nitrogen-scavenging rod isolated from acid lateritic relicts in Germany. Z Allg Mikrobiol 15:287–299. doi: 10.1002/jobm.19750150410 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Eliza Depoorter
    • 1
    • 2
  • Matt J. Bull
    • 3
  • Charlotte Peeters
    • 1
  • Tom Coenye
    • 2
  • Peter Vandamme
    • 1
    Email author
  • Eshwar Mahenthiralingam
    • 3
    Email author
  1. 1.Laboratory of MicrobiologyGhent UniversityGhentBelgium
  2. 2.Laboratory of Pharmaceutical MicrobiologyGhent UniversityGhentBelgium
  3. 3.Organisms and Environment Division, Cardiff School of BiosciencesCardiff UniversityCardiffUK

Personalised recommendations