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Environmental Science and Pollution Research

, Volume 25, Issue 30, pp 29794–29807 | Cite as

Nonribosomal peptides and polyketides of Burkholderia: new compounds potentially implicated in biocontrol and pharmaceuticals

  • Qassim Esmaeel
  • Maude Pupin
  • Philippe Jacques
  • Valérie Leclère
Chemistry, Activity and Impact of Plant Biocontrol products

Abstract

Bacteria belonging to the genus Burkholderia live in various ecological niches and present a significant role in the environments through the excretion of a wide variety of secondary metabolites including modular nonribosomal peptides (NRPs) and polyketides (PKs). These metabolites represent a widely distributed biomedically and biocontrol important class of natural products including antibiotics, siderophores, and anticancers as well as biopesticides that are considered as a novel source that can be used to defend ecological niche from competitors and to promote plant growth. The aim of this review is to present all NRPs produced or potentially produced by strains of Burkholderia, as NRPs represent a major source of active compounds implicated in biocontrol. The review is a compilation of results from a large screening we have performed on 48 complete sequenced genomes available in NCBI to identify NRPS gene clusters, and data found in the literature mainly because some interesting compounds are produced by strains not yet sequenced. In addition to NRPs, hybrids NRPs/PKs are also included. Specific features about biosynthetic gene clusters and structures of the modular enzymes responsible for the synthesis, the biological activities, and the potential uses in agriculture and pharmaceutical of NRPs and hybrids NRPs/PKs will also be discussed.

Keywords

Burkholderia NRPS Hybrid NRPS/PKS Biocontrol Lipopeptides Siderophores 

Notes

Acknowledgements

This work was supported by the University of Lille 1, the INTERREG IVa program France-Wallonie-Vlaanderen (Phytobio project), the INTERREGVa program (SmartBioControle/BioScreen project), and the bioinformatics platform bilille.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. Abe M, Nakazawa T (1994) Characterization of hemolytic and antifungal substance, cepalycin, from Pseudomonas cepacia. Microbiol Immunol 38:1–9. doi: 10.1111/j.1348-0421.1994.tb01737.x CrossRefGoogle Scholar
  2. Adler C, Corbalán NS, Seyedsayamdost MR, Pomares MF, de Cristóbal RE, Clardy J, Kolter R, Vincent PA (2012) Catecholate Siderophores protect Bacteria from Pyochelin toxicity. PLoS One 7:e46754. doi: 10.1371/journal.pone.0046754 CrossRefGoogle Scholar
  3. Andrews SC, Robinson AK, Rodríguez-Quiñones F (2003) Bacterial iron homeostasis. FEMS Microbiol Rev 27:215–237. doi: 10.1016/s0168-6445(03)00055-x CrossRefGoogle Scholar
  4. Bais HP, Fall R, Vivanco JM (2004) Biocontrol of Bacillus subtilis against infection of Arabidopsis roots by Pseudomonas syringae is facilitated by biofilm formation and surfactin production. Plant Physiol 134:307–319. doi: 10.1104/pp.103.028712 CrossRefGoogle Scholar
  5. Balibar CJ, Vaillancourt FH, Walsh CT (2005) Generation of D amino acid residues in assembly of Arthrofactin by dual condensation/epimerization domains. Chem Biol 12:1189–1200. doi: 10.1016/j.chembiol.2005.08.010 CrossRefGoogle Scholar
  6. Barelmann I, Meyer J-M, Taraz K, Budzikiewicz H (1996) Cepaciachelin, a new Catecholate Siderophore from Burkholderia (Pseudomonas) Cepacia. Z Naturforsch 51C:627–630CrossRefGoogle Scholar
  7. Bibb MJ (2005) Regulation of secondary metabolism in Streptomycetes. Curr Opin Microbiol 8:208–215. doi: 10.1016/j.mib.2005.02.016 CrossRefGoogle Scholar
  8. Biggins JB, Gleber CD, Brady SF (2011a) Acyldepsipeptide HDAC inhibitor production induced in Burkholderia thailandensis. Org Lett 13:1536–1539. doi: 10.1021/ol200225v CrossRefGoogle Scholar
  9. Biggins JB, Liu X, Feng Z, Brady SF (2011b) 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 CrossRefGoogle Scholar
  10. 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 CrossRefGoogle Scholar
  11. Biggins JB, Kang H-S, Ternei MA, DeShazer D, Brady SF (2014) The chemical arsenal of Burkholderia pseudomallei is essential for pathogenicity. J Am Chem Soc 136:9484–9490. doi: 10.1021/ja504617n CrossRefGoogle Scholar
  12. Bisacchi GS, Hockstein DR, Koster WH, Parker WL, Rathnum ML, Unger SE (1987) Xylocandin: a new complex of antifungal peptides. II. Structural studies and chemical modifications. J Antibiot 40:1520–1529. doi: 10.7164/antibiotics.40.1520 CrossRefGoogle Scholar
  13. 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 73:5308–5319. doi: 10.1128/AEM.00324-07 CrossRefGoogle Scholar
  14. Caradec T, Pupin M, Vanvlassenbroeck A, Devignes M-D, Smaïl-Tabbone M, Jacques P, Leclère V (2014) Prediction of monomer isomery in Florine: a workflow dedicated to nonribosomal peptide discovery. PLoS One 9:e85667. doi: 10.1371/journal.pone.0085667 CrossRefGoogle Scholar
  15. Carr G, Seyedsayamdost MR, Chandler JR, Greenberg EP, Clardy J (2011) Sources of diversity in Bactobolin Biosynthesis by Burkholderia thailandensis E264. Org Lett 13:3048–3051. doi: 10.1021/ol200922s CrossRefGoogle Scholar
  16. Chain PS, Denef VJ, Konstantinidis KT, Vergez LM, Agulló L, Reyes VL, Hauser L, Córdova M, Gómez L, González M (2006) Burkholderia xenovorans LB400 harbors a multi-replicon, 9.73-Mbp genome shaped for versatility. Proc Natl Acad Sci U S A 103:15280–15287. doi: 10.1073/pnas.0606924103 CrossRefGoogle Scholar
  17. 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 56:1847–1851. doi: 10.1099/ijs.0.64325-0 CrossRefGoogle Scholar
  18. 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 57:1055–1059. doi: 10.1099/ijs.0.64873-0 CrossRefGoogle Scholar
  19. Cornelis P (2010) Iron uptake and metabolism in Pseudomonads. Appl Microbiol Biotechnol 86:1637–1645. doi: 10.1007/s00253-010-2550-2 CrossRefGoogle Scholar
  20. Cox CD, Graham R (1979) Isolation of an iron-binding compound from Pseudomonas aeruginosa. J Bacteriol 137:357–364Google Scholar
  21. Crosa JH (1989) Genetics and molecular biology of siderophore-mediated iron transport in bacteria. Microbiol Rev 53:517–530Google Scholar
  22. Czárán TL, Hoekstra RF, Pagie L (2002) Chemical warfare between microbes promotes biodiversity. Proc Natl Acad Sci 99:786–790. doi: 10.1073/pnas.012399899 CrossRefGoogle Scholar
  23. Darling P, Chan M, Cox AD, Sokol PA (1998) Siderophore production by cystic fibrosis isolates of Burkholderia cepacia. Infect Immun 66:874–877Google Scholar
  24. Du L, Sánchez C, Shen B (2001) Hybrid peptide–polyketide natural products: biosynthesis and prospects toward engineering novel molecules. Metab Eng 3:78–95. doi: 10.1006/mben.2000.0171 CrossRefGoogle Scholar
  25. Ellis D, Gosai J, Emrick C, Heintz R, Romans L, Gordon D, Lu S-E, Austin F, Smith L (2012) Occidiofungin’s chemical stability and in vitro potency against Candida species. Antimicrob Agents Chemother 56:765–769. doi: 10.1128/aac.05231-11 CrossRefGoogle Scholar
  26. Esmaeel Q, Pupin M, Kieu NP, Chataigné G, Béchet M, Deravel J, Krier F, Höfte M, Jacques P, Leclère V (2016) Burkholderia genome mining for nonribosomal peptide synthetases reveals a great potential for novel siderophores and lipopeptides synthesis. MicrobiologyOpen 5(3):512–526. doi: 10.1002/mbo3.347 CrossRefGoogle Scholar
  27. Franke J, Ishida K, Hertweck C (2012) Genomics-driven discovery of Burkholderic acid, a Noncanonical, cryptic polyketide from human pathogenic Burkholderia species. Angew Chem Int Ed 51:11611–11615. doi: 10.1002/anie.201205566 CrossRefGoogle Scholar
  28. Franke J, Ishida K, Ishida-Ito M, Hertweck C (2013) Nitro versus hydroxamate in siderophores of pathogenic bacteria: effect of missing hydroxylamine protection in malleobactin biosynthesis. Angew Chem Int Ed 52:8271–8275. doi: 10.1002/anie.201303196 CrossRefGoogle Scholar
  29. Franke J, Ishida K, Hertweck C (2014) Evolution of Siderophore pathways in human pathogenic Bacteria. J Am Chem Soc 136:5599–5602. doi: 10.1021/ja501597w CrossRefGoogle Scholar
  30. Gu G, Smith L, Wang N, Wang H, Lu S-E (2009) Biosynthesis of an antifungal oligopeptide in Burkholderia contaminans strain MS14. Biochem Biophys Res Commun 380:328–332. doi: 10.1016/j.bbrc.2009.01.073 CrossRefGoogle Scholar
  31. Gu G, Smith L, Liu A, Lu S-E (2011) Genetic and biochemical map for the Biosynthesis of Occidiofungin, an antifungal produced by Burkholderia contaminans strain MS14. Appl Environ Microbiol 77:6189–6198. doi: 10.1128/aem.00377-11 CrossRefGoogle Scholar
  32. Hertweck C (2009) The biosynthetic logic of polyketide diversity. Angew Chem Int Ed 48:4688–4716. doi: 10.1002/anie.200806121 CrossRefGoogle Scholar
  33. Hider RC, Kong X (2010) Chemistry and biology of siderophores. Nat Prod Rep 27:637–657. doi: 10.1039/B906679A CrossRefGoogle Scholar
  34. 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 147:2517–2528. doi: 10.1099/00221287-147-9-2517 CrossRefGoogle Scholar
  35. 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 CrossRefGoogle Scholar
  36. Jain A, Liu X, Wordinger RJ, Yorio T, Cheng Y-Q, Clark AF (2013) Effects of thailanstatins on glucocorticoid response in trabecular meshwork and steroid-induced glaucoma. Invest Ophthalmol Vis Sci 54:3137CrossRefGoogle Scholar
  37. Kang Y, Carlson R, Tharpe W, Schell MA (1998) Characterization of genes involved in Biosynthesis of a novel antibiotic from Burkholderia cepacia BC11 and their role in Biological control of Rhizoctonia solani. Appl Environ Microbiol 64:3939–3947Google Scholar
  38. Kearns DB, Losick R (2003) Swarming motility in undomesticated Bacillus subtilis. Mol Microbiol 49:581–590. doi: 10.1046/j.1365-2958.2003.03584.x CrossRefGoogle Scholar
  39. Lackner G, Moebius N, Partida-Martinez LP, Boland S, Hertweck C (2011) Evolution of an endofungal lifestyle: deductions from the Burkholderia rhizoxinica genome. BMC Genomics 12:1–13. doi: 10.1186/1471-2164-12-210 CrossRefGoogle Scholar
  40. Lafontaine JA, Provencal DP, Gardelli C, Leahy JW (2003) Enantioselective total synthesis of the antitumor macrolide rhizoxin D. J Org Chem 68:4215–4234. doi: 10.1021/jo034011x CrossRefGoogle Scholar
  41. Leclère V, Marti R, Béchet M, Fickers P, Jacques P (2006) The lipopeptides mycosubtilin and surfactin enhance spreading of Bacillus subtilis strains by their surface-active properties. Arch Microbiol 186:475–483. doi: 10.1007/s00203-006-0163-z CrossRefGoogle Scholar
  42. Lee CH, Kim S, Hyun B, Suh JW, Yon C, Kim C, Lim Y, Kim C (1994) Cepacidine a, a novel antifungal antibiotic produced by Pseudomonas cepacia. I. Taxonomy, production, isolation and biological activity. J Antibiot 47:1402–1405. doi: 10.7164/antibiotics.47.1402 CrossRefGoogle Scholar
  43. Lee CH, Suh JW, Cho YH (1999) Immunosuppressive activity of cepacidine a, a novel antifungal antibiotic produced by Pseudomonas cepacia. J Microbiol Biotechnol 9:672–674Google Scholar
  44. Lee CH, Kempf HJ, Lim Y, Cho YH (2000) Biocontrol activity of Pseudomonas cepacia AF2001 and anthelmintic activity of its novel metabolite, cepacidine A. J Microbiol Biotechnol 10:568–571Google Scholar
  45. Lewenza S, Conway B, Greenberg E, Sokol PA (1999) Quorum sensing in Burkholderia cepacia: identification of the LuxRI homologs CepRI. J Bacteriol 181:748–756Google Scholar
  46. Lim Y, J-w S, Kim S, Hyun B, Kim C, Lee C-h (1994) Cepacidine A, a novel antifungal antibiotic produced by Pseudomonas cepacia. II Physico-chemical properties and structure elucidation. J Antibiot 47:1406–1416. doi: 10.7164/antibiotics.47.1406 CrossRefGoogle Scholar
  47. Lin Z, Falkinham JO III, Tawfik KA, Jeffs P, Bray B, Dubay G, Cox JE, Schmidt EW (2012) Burkholdines from Burkholderia ambifaria: antifungal agents and possible virulence factors. J Nat Prod 75:1518–1523. doi: 10.1021/np300108u CrossRefGoogle Scholar
  48. Liu X, Biswas S, Berg MG, Antapli CM, Xie F, Wang Q, Tang M-C, Tang G-L, Zhang L, Dreyfuss G (2013) Genomics-guided discovery of thailanstatins A, B, and C as pre-mRNA splicing inhibitors and antiproliferative agents from Burkholderia thailandensis MSMB43. J Nat Prod 76:685–693. doi: 10.1021/np300913h CrossRefGoogle Scholar
  49. Loper JE, Henkels MD, Shaffer BT, Valeriote FA, Gross H (2008) Isolation and identification of rhizoxin analogs from Pseudomonas fluorescens Pf-5 by using a genomic mining strategy. Appl Environ Microbiol 74. doi: 10.1128/aem.02848-07 CrossRefGoogle Scholar
  50. Lu SE, 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. Biochemist 48:8312–8321. doi: 10.1021/bi900814c CrossRefGoogle Scholar
  51. Mahenthiralingam E, Urban TA, Goldberg JB (2005) The multifarious, multireplicon Burkholderia cepacia complex. Nat Rev Microbiol 3:144–156. doi: 10.1038/nrmicro1085 CrossRefGoogle Scholar
  52. Mahenthiralingam E, Baldwin A, Dowson CG (2008) Burkholderia cepacia complex bacteria: opportunistic pathogens with important natural biology. J Appl Microbiol 104:1539–1551. doi: 10.1111/j.1365-2672.2007.03706.x CrossRefGoogle Scholar
  53. Marahiel MA (2009) Working outside the protein-synthesis rules: insights into non-ribosomal peptide synthesis. J Pept Sci 15:799–807. doi: 10.1002/psc.1183 CrossRefGoogle Scholar
  54. Meyers E, Bisacchi G, Dean L, Liu W, Minassian B, Slusarchyk D, Sykes R, Tanaka S, Trejo W (1987) Xylocandin: a new complex of antifungal peptides. I. Taxonomy, isolation and biological activity. J Antibiot 40:1515–1519. doi: 10.7164/antibiotics.40.1515 CrossRefGoogle Scholar
  55. Miotto-Vilanova L, Jacquard C, Courteaux B, Wortham L, Michel J, Clément C, Barka EA, Sanchez L (2016) Burkholderia phytofirmans PsJN Confers Grapevine Resistance against Botrytis cinerea via a Direct Antimicrobial Effect Combined with a Better Resource Mobilization. Front Plant Sci 7. doi: 10.3389/fpls.2016.01236
  56. Nakajima H, Hori Y, Terano H, Okuhara M, Manda T, Matsumoto S, Shimomura K (1996) New antitumor substances, FR901463, FR901464 and FR901465. II. Activities against experimental tumors in mice and mechanism of action. J Antibiot 49:1204–1211CrossRefGoogle Scholar
  57. Nakajima H, Takase S, Terano H, Tanaka H (1997) New antitumor substances, FR901463, FR901464 and FR901465. III. Structures of FR901463, FR901464 and FR901465. J Antibiot 50:96–99. doi: 10.7164/antibiotics.50.96 CrossRefGoogle Scholar
  58. Oka M, Nishiyama Y, Ohta S, Kamei H, Konishi M, Miyaki T, Oki T, Kawaguchi H (1988) Glidobactins a, B and C, new antitumor antibiotics. I. Production, isolation, chemical properties and biological activity. J Antibiot 41:1331–1337. doi: 10.7164/antibiotics.41.1331 CrossRefGoogle Scholar
  59. Ongena M, Jacques P (2008) Bacillus lipopeptides: versatile weapons for plant disease biocontrol. Trends Microbiol 16:115–125. doi: 10.1016/j.tim.2007.12.009 CrossRefGoogle Scholar
  60. Partida-Martinez LP, Hertweck C (2005) Pathogenic fungus harbours endosymbiotic bacteria for toxin production. Nature 437:884–888. doi: 10.1038/nature03997 CrossRefGoogle Scholar
  61. Partida-Martinez LP, Hertweck C (2007) A gene cluster encoding rhizoxin biosynthesis in “Burkholderia rhizoxina”, the bacterial endosymbiont of the fungus Rhizopus microsporus. Chembiochem 8:41–45. doi: 10.1002/cbic.200600393 CrossRefGoogle Scholar
  62. Partida-Martinez LP, de Looß CF, Ishida K, Ishida M, Roth M, Buder K, Hertweck C (2007) Rhizonin, the first mycotoxin isolated from the zygomycota, is not a fungal metabolite but is produced by bacterial endosymbionts. Appl Environ Microbiol 73:793–797. doi: 10.1128/AEM.01784-06 CrossRefGoogle Scholar
  63. Pupin M, Esmaeel Q, Flissi A, Dufresne Y, Jacques P, Leclère V (2015) Norine: a powerful resource for novel nonribosomal peptide discovery. Synth Syst Biotechnol. doi: 10.1016/j.synbio.2015.11.001 CrossRefGoogle Scholar
  64. Reading NC, Sperandio V (2006) Quorum sensing: the many languages of bacteria. FEMS Microbiol Lett 254:1–11. doi: 10.1111/j.1574-6968.2005.00001.x CrossRefGoogle Scholar
  65. Rodrigues L, Banat IM, Teixeira J, Oliveira R (2006) Biosurfactants: potential applications in medicine. J Antimicrob Chemother 57:609–618. doi: 10.1093/jac/dkl024 CrossRefGoogle Scholar
  66. Royer M, Koebnik R, Marguerettaz M, Barbe V, Robin G, Brin C, Carrere S, Gomez C, Hugelland M, Voller G, Noell J, Pieretti I, Rausch S, Verdier V, Poussier S, Rott P, Sussmuth R, Cociancich S (2013) Genome mining reveals the genus Xanthomonas to be a promising reservoir for new bioactive non-ribosomally synthesized peptides. BMC Genomics 14:658. doi: 10.1186/1471-2164-14-658 CrossRefGoogle Scholar
  67. 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 CrossRefGoogle Scholar
  68. Schett G, Sloan VS, Stevens RM, Schafer P (2010) Apremilast: a novel PDE4 inhibitor in the treatment of autoimmune and inflammatory diseases. Ther Adv Musculoskelet Dis 2:271–278. doi: 10.1177/1759720x10381432 CrossRefGoogle Scholar
  69. Schlegel K, Taraz K, Budzikiewicz H (2004) The stereoisomers of pyochelin, a siderophore of Pseudomonas aeruginosa. Biometals 17:409–414CrossRefGoogle Scholar
  70. 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 CrossRefGoogle Scholar
  71. Sharma A, Johri B (2003) Growth promoting influence of siderophore-producing Pseudomonas strains GRP3A and PRS 9 in maize (Zea mays L.) under iron limiting conditions. Microbiol Res 158:243–248. doi: 10.1078/0944-5013-00197 CrossRefGoogle Scholar
  72. Shoji J, Hinoo H, Kato T, Hattori T, Hirooka K, Tawara K, Shiratori O, Terui Y (1990) Isolation of cepafungins I, II and III from Pseudomonas species. J Antibiot 43:783–787. doi: 10.7164/antibiotics.43.783 CrossRefGoogle Scholar
  73. Sokol PA, Darling P, Woods DE, Mahenthiralingam E, Kooi C (1999) Role of Ornibactin Biosynthesis in the virulence of Burkholderia cepacia: characterization of pvdA, the Gene encoding l-ornithine N(5)-oxygenase. Infect Immun 67:4443–4455Google Scholar
  74. Staunton J, Weissman KJ (2001) Polyketide biosynthesis: a millennium review. Nat Prod Rep 18:380–416. doi: 10.1039/a909079g CrossRefGoogle Scholar
  75. Tawfik KA, Jeffs P, Bray B, Dubay G, Falkinham JO III, Mesbah M, Youssef D, Khalifa S, Schmidt EW (2010) Burkholdines 1097 and 1229, potent antifungal peptides from Burkholderia ambifaria 2.2 N. Org Lett 12:664–666. doi: 10.1021/ol9029269 CrossRefGoogle Scholar
  76. Thomas MS (2007) Iron acquisition mechanisms of the Burkholderia cepacia complex. Biometals 20:431–452. doi: 10.1007/s10534-007-9100-0 CrossRefGoogle Scholar
  77. 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 CrossRefGoogle Scholar
  78. Tseng C-F, Burger A, Mislin GL, Schalk IJ, Yu SS-F, Chan SI, Abdallah MA (2006) Bacterial siderophores: the solution stoichiometry and coordination of the Fe (III) complexes of pyochelin and related compounds. JBIC, J Biol Inorg Chem 11:419–432. doi: 10.1007/s00775-006-0088-7 CrossRefGoogle Scholar
  79. Van Lanen SG, Shen B (2006) Microbial genomics for the improvement of natural product discovery. Curr Opin Microbiol 9:252–260. doi: 10.1016/j.mib.2006.04.002 CrossRefGoogle Scholar
  80. Van Vliet AH, Wooldridge KG, Ketley JM (1998) Iron-responsive gene regulation in a Campylobacter jejuni fur mutant. J Bacteriol 180:5291–5298Google Scholar
  81. VanderMolen KM, McCulloch W, Pearce CJ, Oberlies NH (2011) Romidepsin (Istodax, NSC 630176, FR901228, FK228, depsipeptide): a natural product recently approved for cutaneous T-cell lymphoma. J Antibiot 64:525–531CrossRefGoogle Scholar
  82. Vial L, Groleau M-C, Dekimpe V, Déziel É (2007) Burkholderia diversity and versatility: an inventory of the extracellular products. J Microbiol Biotechnol 17:1407–1429Google Scholar
  83. Visser M, Majumdar S, Hani E, Sokol P (2004) Importance of the ornibactin and pyochelin siderophore transport systems in Burkholderia cenocepacia lung infections. Infect Immun 72:2850–2857. doi: 10.1128/IAI.72.5.2850-2857.2004 CrossRefGoogle Scholar
  84. Walsh CT (2008) The chemical versatility of natural-product assembly lines. Acc Chem Res 41:4–10. doi: 10.1021/ar7000414 CrossRefGoogle Scholar
  85. 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 CrossRefGoogle Scholar
  86. Weber T, Blin K, Duddela S, Krug D, Kim HU, Bruccoleri R, Lee SY, Fischbach MA, Müller R, Wohlleben W, Breitling R, Takano E, Medema MH (2015) antiSMASH 3.0—a comprehensive resource for the genome mining of biosynthetic gene clusters. Nucl Acids Res. doi: 10.1093/nar/gkv437 CrossRefGoogle Scholar
  87. 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 CrossRefGoogle Scholar
  88. Zhou H, Yao F, Roberts DP, Lessie TG (2003) AHL-deficient mutants of Burkholderia ambifaria BC-F have decreased antifungal activity. Curr Microbiol 47:0174–0179. doi: 10.1007/s00284-002-3926-z CrossRefGoogle Scholar
  89. Ziemert N, Podell S, Penn K, Badger JH, Allen E, Jensen PR (2012) The natural product domain seeker NaPDoS: a phylogeny based Bioinformatic tool to classify secondary metabolite Gene diversity. PLoS One 7:e34064. doi: 10.1371/journal.pone.0034064 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2017

Authors and Affiliations

  • Qassim Esmaeel
    • 1
    • 2
  • Maude Pupin
    • 3
    • 4
  • Philippe Jacques
    • 1
    • 5
  • Valérie Leclère
    • 1
    • 3
    • 4
  1. 1.University Lille, INRA, ISA, University Artois, University Littoral Côte d’Opale, EA 7394-ICV- Institut Charles ViolletteLilleFrance
  2. 2.Laboratoire de Stress, Défenses et Reproduction des Plantes URVVC-EA 4707, UFR Sciences Exactes et NaturellesUniversity of Reims-Champagne-ArdenneReimsFrance
  3. 3.University Lille, CNRS, Centrale Lille, UMR 9189- CRIStAL- Centre de Recherche en Informatique Signal et Automatique de LilleLilleFrance
  4. 4.Inria-Lille Nord Europe, Bonsai teamVilleneuve d’Ascq CedexFrance
  5. 5.TERRA Research Centre, Microbial Processes and Interactions (MiPI)Gembloux Agro-Bio Tech University of LiegeGemblouxBelgium

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