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Secondary metabolites from the Burkholderia pseudomallei complex: structure, ecology, and evolution

  • Environmental Microbiology - Review
  • Published:
Journal of Industrial Microbiology & Biotechnology

Abstract

Bacterial secondary metabolites play important roles in promoting survival, though few have been carefully studied in their natural context. Numerous gene clusters code for secondary metabolites in the genomes of members of the Bptm group, made up of three closely related species with distinctly different lifestyles: the opportunistic pathogen Burkholderia pseudomallei, the non-pathogenic saprophyte Burkholderia thailandensis, and the host-adapted pathogen Burkholderia mallei. Several biosynthetic gene clusters are conserved across two or all three species, and this provides an opportunity to understand how the corresponding secondary metabolites contribute to survival in different contexts in nature. In this review, we discuss three secondary metabolites from the Bptm group: bactobolin, malleilactone (and malleicyprol), and the 4-hydroxy-3-methyl-2-alkylquinolines, providing an overview of each of their biosynthetic pathways and insight into their potential ecological roles. Results of studies on these secondary metabolites provide a window into how secondary metabolites contribute to bacterial survival in different environments, from host infections to polymicrobial soil communities.

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References

  1. Abisado RG, Benomar S, Klaus JR, Dandekar AA, Chandler JR (2018) Bacterial quorum sensing and microbial community interactions. MBio 9:e02331–e2317. https://doi.org/10.1128/mBio.02331-17

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Agarwal A, Kahyaoglu C, Hansen DB (2012) Characterization of HmqF, a protein involved in the biosynthesis of unsaturated quinolones produced by Burkholderia thailandensis. Biochemistry 51:1648–1657. https://doi.org/10.1021/bi201625w

    Article  CAS  PubMed  Google Scholar 

  3. Alice AF, Lopez CS, Lowe CA, Ledesma MA, Crosa JH (2006) Genetic and transcriptional analysis of the siderophore malleobactin biosynthesis and transport genes in the human pathogen Burkholderia pseudomallei K96243. J Bacteriol 188:1551–1566. https://doi.org/10.1128/JB.188.4.1551-1566.2006

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Amunts A, Fiedorczuk K, Truong TT, Chandler J, Peter Greenberg E, Ramakrishnan V (2015) Bactobolin A binds to a site on the 70S ribosome distinct from previously seen antibiotics. J Mol Biol 427:753–755. https://doi.org/10.1016/j.jmb.2014.12.018

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. An D, Danhorn T, Fuqua C, Parsek MR (2006) Quorum sensing and motility mediate interactions between Pseudomonas aeruginosa and Agrobacterium tumefaciens in biofilm cocultures. Proc Natl Acad Sci USA 103:3828–3833. https://doi.org/10.1073/pnas.0511323103

    Article  CAS  PubMed  Google Scholar 

  6. Benomar S, Evans KC, Unckless RL, Chandler JR (2019) Efflux pumps in Chromobacterium species increase antibiotic resistance and promote survival in a co-culture competition model. Appl Environ Microbiol 85:e00908–00919. https://doi.org/10.1128/AEM.00908-19

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Biggins JB, Kang HS, Ternei MA, DeShazer D, Brady SF (2014) The chemical arsenal of Burkholderia pseudomallei is essential for pathogenicity. J Am Chem Soc 136:9484–9490. https://doi.org/10.1021/ja504617n

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. 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. https://doi.org/10.1021/ja1087369

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. 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. https://doi.org/10.1021/ja3052156

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Brady SF, Bauer JD, Clarke-Pearson MF, Daniels R (2007) Natural products from isnA-containing biosynthetic gene clusters recovered from the genomes of cultured and uncultured bacteria. J Am Chem Soc 129:12102–12103. https://doi.org/10.1021/ja075492v

    Article  CAS  PubMed  Google Scholar 

  11. 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. https://doi.org/10.1021/ol200922s

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Challis GL, Hopwood DA (2003) Synergy and contingency as driving forces for the evolution of multiple secondary metabolite production by Streptomyces species. Proc Natl Acad Sci USA 100(2):14555–14561. https://doi.org/10.1073/pnas.1934677100

    Article  CAS  PubMed  Google Scholar 

  13. Chandler JR, Heilmann S, Mittler JE, Greenberg EP (2012) Acyl-homoserine lactone-dependent eavesdropping promotes competition in a laboratory co-culture model. ISME J 6:2219–2228. https://doi.org/10.1038/ismej.2012.69

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Chandler JR, Truong TT, Silva PM, Seyedsayamdost MR, Carr G, Radey M, Jacobs MA, Sims EH, Clardy J, Greenberg EP (2012) Bactobolin resistance is conferred by mutations in the L2 ribosomal protein. MBio 3:e00499–e412. https://doi.org/10.1128/mBio.00499-12

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Chapalain A, Groleau M-C, Le Guillouzer S, Miomandre A, Vial L, Milot S, Déziel E (2017) Interplay between 4-Hydroxy-3-Methyl-2-Alkylquinoline and N-Acyl-Homoserine Lactone Signaling in a Burkholderia cepacia Complex Clinical Strain. Front Microbiol. https://doi.org/10.3389/fmicb.2017.01021

    Article  PubMed  PubMed Central  Google Scholar 

  16. Chapalain A, Groleau MC, Le Guillouzer S, Miomandre A, Vial L, Milot S, Déziel E (2017) Interplay between 4-Hydroxy-3-Methyl-2-Alkylquinoline and N-Acyl-Homoserine lactone signaling in a Burkholderia cepacia complex clinical strain. Front Microbiol 8:1021. https://doi.org/10.3389/fmicb.2017.01021

    Article  PubMed  PubMed Central  Google Scholar 

  17. Coulon PML, Groleau MC, Déziel E (2019) Potential of the Burkholderia cepacia complex to produce 4-hydroxy-3-methyl-2-alkyquinolines. Front Cell Infect Microbiol 9:33. https://doi.org/10.3389/fcimb.2019.00033

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Déziel E, Gopalan S, Tampakaki AP, Lépine F, Padfield KE, Saucier M, Xiao G, Rahme LG (2005) The contribution of MvfR to Pseudomonas aeruginosa pathogenesis and quorum sensing circuitry regulation: multiple quorum sensing-regulated genes are modulated without affecting lasRI, rhlRI or the production of N-acyl-L-homoserine lactones. Mol Microbiol 55:998–1014. https://doi.org/10.1111/j.1365-2958.2004.04448.x

    Article  CAS  PubMed  Google Scholar 

  19. Déziel E, Lépine F, Milot S, He J, Mindrinos MN, Tompkins RG, Rahme LG (2004) Analysis of Pseudomonas aeruginosa 4-hydroxy-2-alkylquinolines (HAQs) reveals a role for 4-hydroxy-2-heptylquinoline in cell-to-cell communication. Proc Natl Acad Sci USA 101:1339–1344. https://doi.org/10.1073/pnas.0307694100

    Article  CAS  PubMed  Google Scholar 

  20. Diggle SP, Lumjiaktase P, Dipilato F, Winzer K, Kunakorn M, Barrett DA, Chhabra SR, Camara M, Williams P (2006) Functional genetic analysis reveals a 2-alkyl-4-quinolone signaling system in the human pathogen Burkholderia pseudomallei and related bacteria. Chem Biol 13:701–710. https://doi.org/10.1016/j.chembiol.2006.05.006

    Article  CAS  PubMed  Google Scholar 

  21. Diggle SP, Matthijs S, Wright VJ, Fletcher MP, Chhabra SR, Lamont IL, Kong X, Hider RC, Cornelis P, Camara M, Williams P (2007) The Pseudomonas aeruginosa 4-quinolone signal molecules HHQ and PQS play multifunctional roles in quorum sensing and iron entrapment. Chem Biol 14:87–96. https://doi.org/10.1016/j.chembiol.2006.11.014

    Article  CAS  PubMed  Google Scholar 

  22. Diggle SP, Winzer K, Chhabra SR, Worrall KE, Camara M, Williams P (2003) The Pseudomonas aeruginosa quinolone signal molecule overcomes the cell density-dependency of the quorum sensing hierarchy, regulates rhl-dependent genes at the onset of stationary phase and can be produced in the absence of LasR. Mol Microbiol 50:29–43

    Article  CAS  Google Scholar 

  23. Drees SL, Ernst S, Belviso BD, Jagmann N, Hennecke U, Fetzner S (2018) PqsL uses reduced flavin to produce 2-hydroxylaminobenzoylacetate, a preferred PqsBC substrate in alkyl quinolone biosynthesis in Pseudomonas aeruginosa. J Biol Chem 293:9345–9357. https://doi.org/10.1074/jbc.RA117.000789

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. 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. https://doi.org/10.1128/JB.00200-09

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Dulcey CE, Dekimpe V, Fauvelle DA, Milot S, Groleau MC, Doucet N, Rahme LG, Lépine F, Déziel E (2013) The end of an old hypothesis: the Pseudomonas signaling molecules 4-hydroxy-2-alkylquinolines derive from fatty acids, not 3-ketofatty acids. Chem Biol 20:1481–1491. https://doi.org/10.1016/j.chembiol.2013.09.021

    Article  CAS  PubMed  Google Scholar 

  26. Farrow JM 3rd, Pesci EC (2007) Two distinct pathways supply anthranilate as a precursor of the Pseudomonas quinolone signal. J Bacteriol 189:3425–3433. https://doi.org/10.1128/JB.00209-07

    Article  CAS  PubMed  PubMed Central  Google 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 51:11611–11615. https://doi.org/10.1002/anie.201205566

    Article  CAS  Google 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 52:8271–8275. https://doi.org/10.1002/anie.201303196

    Article  CAS  Google Scholar 

  29. Greenberg EP, Chandler JR, Seyedsayamdost MR (2020) The Chemistry and Biology of Bactobolin: A 10-Year Collaboration with Natural Product Chemist Extraordinaire Jon Clardy. J Nat Prod 83:738–743. https://doi.org/10.1021/acs.jnatprod.9b01237

    Article  CAS  PubMed  Google Scholar 

  30. Grove A (2010) Urate-responsive MarR homologs from Burkholderia. Mol Biosyst 6:2133–2142. https://doi.org/10.1039/c0mb00086h

    Article  CAS  PubMed  Google Scholar 

  31. Gupta A, Bedre R, Thapa SS, Sabrin A, Wang G, Dassanayake M, Grove A (2017) Global Awakening of Cryptic Biosynthetic Gene Clusters in Burkholderia thailandensis. ACS Chem Biol 12:3012–3021. https://doi.org/10.1021/acschembio.7b00681

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Gupta A, Grove A (2014) Ligand-binding pocket bridges DNA-binding and dimerization domains of the urate-responsive MarR homologue MftR from Burkholderia thailandensis. Biochemistry 53:4368–4380. https://doi.org/10.1021/bi500219t

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Gutierrez MG, Yoder-Himes DR, Warawa JM (2015) Comprehensive identification of virulence factors required for respiratory melioidosis using Tn-seq mutagenesis. Front Cell Infect Microbiol 5:78. https://doi.org/10.3389/fcimb.2015.00078

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Hacker B, Barquera B, Crofts AR, Gennis RB (1993) Characterization of mutations in the cytochrome b subunit of the bc1 complex of Rhodobacter sphaeroides that affect the quinone reductase site (Qc). Biochemistry 32:4403–4410. https://doi.org/10.1021/bi00067a033

    Article  CAS  PubMed  Google Scholar 

  35. Hazan R, Que YA, Maura D, Strobel B, Majcherczyk PA, Hopper LR, Wilbur DJ, Hreha TN, Barquera B, Rahme LG (2016) Auto poisoning of the respiratory chain by a quorum-sensing-regulated molecule favors biofilm formation and antibiotic tolerance. Curr Biol 26:195–206. https://doi.org/10.1016/j.cub.2015.11.056

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Heilmann S, Krishna S, Kerr B (2015) Why do bacteria regulate public goods by quorum sensing?-How the shapes of cost and benefit functions determine the form of optimal regulation. Front Microbiol 6:767. https://doi.org/10.3389/fmicb.2015.00767

    Article  PubMed  PubMed Central  Google Scholar 

  37. Hibbing ME, Fuqua C, Parsek MR, Peterson SB (2010) Bacterial competition: surviving and thriving in the microbial jungle. Nat Rev Microbiol 8:15–25. https://doi.org/10.1038/nrmicro2259

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Kilani-Feki O, Culioli G, Ortalo-Magne A, Zouari N, Blache Y, Jaoua S (2011) Environmental Burkholderia cepacia strain Cs5 acting by two analogous alkyl-quinolones and a didecyl-phthalate against a broad spectrum of phytopathogens fungi. Curr Microbiol 62:1490–1495. https://doi.org/10.1007/s00284-011-9892-6

    Article  CAS  PubMed  Google Scholar 

  39. Kilani-Feki O, Zouari I, Culioli G, Ortalo-Magne A, Zouari N, Blache Y, Jaoua S (2012) Correlation between synthesis variation of 2-alkylquinolones and the antifungal activity of a Burkholderia cepacia strain collection. World J Microbiol Biotechnol 28:275–281. https://doi.org/10.1007/s11274-011-0817-0

    Article  CAS  PubMed  Google Scholar 

  40. Klaus JR, Deay J, Neuenswander B, Hursh W, Gao Z, Bouddhara T, Williams TD, Douglas J, Monize K, Martins P, Majerczyk C, Seyedsayamdost MR, Peterson BR, Rivera M, Chandler JR (2018) Malleilactone Is a Burkholderia pseudomallei virulence factor regulated by antibiotics and quorum sensing. J Bacteriol 200:e00008–00018. https://doi.org/10.1128/JB.00008-18

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Klaus JR, Majerczyk C, Eppler NA, Ball P, Groleau M-C, Asfahl KL, Smalley NE, Hayden H, Piochon M, Dandekar AA, Gauthier C, Déziel E, Chandler JR (2020) Burkholderia thailandensis methylated hydroxy-alkylquinolines: biosynthesis and antimicrobial activity in co-culture experiments. Appl Environ Microbiol 86:e01452–20. https://doi.org/10.1128/AEM.01452-20

    Article  Google Scholar 

  42. Kondo S, Horiuchi Y, Hamada M, Takeuchi T, Umezawa H (1979) A new antitumor antibiotic, bactobolin produced by Pseudomonas. J Antibiot (Tokyo) 32:1069–1071. https://doi.org/10.7164/antibiotics.32.1069

    Article  CAS  Google Scholar 

  43. Kunakom S, Eustaquio AS (2019) Burkholderia as a source of natural products. J Nat Prod 82:2018–2037. https://doi.org/10.1021/acs.jnatprod.8b01068

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Kunakom S, Eustáquio AS (2019) Burkholderia as a Source of Natural Products. J Nat Prod 82:2018–2037. https://doi.org/10.1021/acs.jnatprod.8b01068

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Le Guillouzer S, Groleau MC, Déziel E (2017) The complex quorum sensing circuitry of Burkholderia thailandensis is both hierarchically and homeostatically organized. mBio 8:e01861–01817. doi:https://doi.org/10.1128/mBio.01861-17

  46. Le Guillouzer S, Groleau MC, Mauffrey F, Déziel E (2020) ScmR, a global regulator of gene expression, quorum sensing, pH homeostasis, and virulence in Burkholderia thailandensis. J Bacteriol 202:e00776–e1719. https://doi.org/10.1128/JB.00776-19

    Article  PubMed  Google Scholar 

  47. Lépine F, Milot S, Déziel E, He J, Rahme LG (2004) Electrospray/mass spectrometric identification and analysis of 4-hydroxy-2-alkylquinolines (HAQs) produced by Pseudomonas aeruginosa. J Am Soc Mass Spectrom 15:862–869. https://doi.org/10.1016/j.jasms.2004.02.012

    Article  CAS  PubMed  Google Scholar 

  48. Li A, Mao D, Yoshimura A, Rosen PC, Martin WL, Gallant E, Wuhr M, Seyedsayamdost MR (2020) Multi-omic analyses provide links between low-dose antibiotic treatment and induction of secondary metabolism in Burkholderia thailandensis. mBio 11:e03210–03219. doi:https://doi.org/10.1128/mBio.03210-19

  49. Li D, Oku N, Hasada A, Shimizu M, Igarashi Y (2018) Two new 2-alkylquinolones, inhibitory to the fish skin ulcer pathogen Tenacibaculum maritimum, produced by a rhizobacterium of the genus Burkholderia sp. Beilstein J Org Chem 14:1446–1451. https://doi.org/10.3762/bjoc.14.122

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Lipscomb L, Schell MA (2011) Elucidation of the regulon and cis-acting regulatory element of HrpB, the AraC-type regulator of a plant pathogen-like type III secretion system in Burkholderia pseudomallei. J Bacteriol 193:1991–2001. https://doi.org/10.1128/JB.01379-10

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Liu X, Cheng YQ (2014) Genome-guided discovery of diverse natural products from Burkholderia sp. J Ind Microbiol Biotechnol 41:275–284. https://doi.org/10.1007/s10295-013-1376-1

    Article  CAS  PubMed  Google Scholar 

  52. 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. https://doi.org/10.1016/j.chembiol.2011.01.020

    Article  CAS  PubMed  Google Scholar 

  53. Majerczyk C, Brittnacher M, Jacobs M, Armour CD, Radey M, Schneider E, Phattarasokul S, Bunt R, Greenberg EP (2014) Global analysis of the Burkholderia thailandensis quorum sensing-controlled regulon. J Bacteriol 196:1412–1424. https://doi.org/10.1128/JB.01405-13

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. 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. https://doi.org/10.1128/JB.01974-14

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Mao D, Bushin LB, Moon K, Wu Y, Seyedsayamdost MR (2017) Discovery of scmR as a global regulator of secondary metabolism and virulence in Burkholderia thailandensis E264. Proc Natl Acad Sci USA 114:E2920–E2928. https://doi.org/10.1073/pnas.1619529114

    Article  CAS  PubMed  Google Scholar 

  56. Marenda M, Brito B, Callard D, Genin S, Barberis P, Boucher C, Arlat M (1998) PrhA controls a novel regulatory pathway required for the specific induction of Ralstonia solanacearum hrp genes in the presence of plant cells. Mol Microbiol 27:437–453

    Article  CAS  Google Scholar 

  57. Martin HM, Hancock JT, Salisbury V, Harrison R (2004) Role of xanthine oxidoreductase as an antimicrobial agent. Infect Immun 72:4933–4939. https://doi.org/10.1128/IAI.72.9.4933-4939.2004

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Mazzola M, Cook RJ, Thomashow LS, Weller DM, Pierson LS 3rd (1992) Contribution of phenazine antibiotic biosynthesis to the ecological competence of fluorescent pseudomonads in soil habitats. Appl Environ Microbiol 58:2616–2624

    Article  CAS  Google Scholar 

  59. Moons P, Van Houdt R, Aertsen A, Vanoirbeek K, Engelborghs Y, Michiels CW (2006) Role of quorum sensing and antimicrobial component production by Serratia plymuthica in formation of biofilms, including mixed biofilms with Escherichia coli. Appl Environ Microbiol 72:7294–7300. https://doi.org/10.1128/AEM.01708-06

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Moons P, Van Houdt R, Aertsen A, Vanoirbeek K, Michiels CW (2005) Quorum sensing dependent production of antimicrobial component influences establishment of E. coli in dual species biofilms with Serratia plymuthica. Commun Agric Appl Biol Sci 70:195–198

    CAS  PubMed  Google Scholar 

  61. Mori T, Yamashita T, Furihata K, Nagai K, Suzuki K, Hayakawa Y, Shin-Ya K (2007) Burkholone, a new cytotoxic antibiotic against IGF-I dependent cells from Burkholderia sp. J Antibiot (Tokyo) 60:713–716. https://doi.org/10.1038/ja.2007.92

    Article  CAS  Google Scholar 

  62. Moule MG, Spink N, Willcocks S, Lim J, Guerra-Assuncao JA, Cia F, Champion OL, Senior NJ, Atkins HS, Clark T, Bancroft GJ, Cuccui J, Wren BW (2015) Characterization of new virulence factors involved in the intracellular growth and survival of Burkholderia pseudomallei. Infect Immun 84:701–710. https://doi.org/10.1128/IAI.01102-15

    Article  CAS  PubMed  Google Scholar 

  63. Nickzad A, Déziel E (2016) Adaptive significance of quorum sensing-dependent regulation of rhamnolipids by integration of growth rate in Burkholderia glumae: A trade-off between survival and efficiency. Front Microbiol 7:1215. https://doi.org/10.3389/fmicb.2016.01215

    Article  PubMed  PubMed Central  Google Scholar 

  64. Okada BK, Wu Y, Mao D, Bushin LB, Seyedsayamdost MR (2016) Mapping the Trimethoprim-Induced Secondary Metabolome of Burkholderia thailandensis. ACS Chem Biol 11:2124–2130. https://doi.org/10.1021/acschembio.6b00447

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Park JD, Moon K, Miller C, Rose J, Xu F, Ebmeier CC, Jacobsen JR, Mao D, Old WM, DeShazer D, Seyedsayamdost MR (2020) Thailandenes, cryptic polyene natural products isolated from Burkholderia thailandensis using phenotype-guided transposon mutagenesis. ACS Chem Biol. doi:https://doi.org/10.1021/acschembio.9b00883

  66. Piochon M, Coulon PML, Caulet A, Groleau M-C, Déziel E, Gauthier C (2020) Synthesis and antimicrobial activity of Burkholderia-related 4-hydroxy-3-methyl-2-alkenylquinolones (HMAQs) and their N-oxide counterparts. J Nat Prod 83:2145–2154. https://doi.org/10.1021/acs.jnatprod.0c00171

    Article  CAS  PubMed  Google Scholar 

  67. Reen FJ, McGlacken GP, O'Gara F (2018) The expanding horizon of alkyl quinolone signalling and communication in polycellular interactomes. FEMS Microbiol Lett. https://doi.org/10.1093/femsle/fny076

    Article  PubMed  Google Scholar 

  68. Seyedsayamdost MR (2014) High-throughput platform for the discovery of elicitors of silent bacterial gene clusters. Proc Natl Acad Sci USA 111:7266–7271. https://doi.org/10.1073/pnas.1400019111

    Article  CAS  PubMed  Google Scholar 

  69. Seyedsayamdost MR, Chandler JR, Blodgett JA, Lima PS, Duerkop BA, Oinuma K, Greenberg EP, Clardy J (2010) Quorum-sensing-regulated bactobolin production by Burkholderia thailandensis E264. Org Lett 12:716–719. https://doi.org/10.1021/ol902751x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. Smalley NE, An D, Parsek MR, Chandler JR, Dandekar AA (2015) Quorum sensing protects Pseudomonas aeruginosa against cheating by other species in a laboratory coculture model. J Bacteriol 197:3154–3159. https://doi.org/10.1128/JB.00482-15

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Thapa SS, Grove A (2019) Do global regulators hold the key to production of bacterial secondary metabolites? Antibiotics (Basel). https://doi.org/10.3390/antibiotics8040160

    Article  Google Scholar 

  72. Trottmann F, Franke J, Richter I, Ishida K, Cyrulies M, Dahse HM, Regestein L, Hertweck C (2019) Cyclopropanol warhead in malleicyprol confers virulence of human- and animal-pathogenic Burkholderia species. Angew Chem 58:14129–14133. https://doi.org/10.1002/anie.201907324

    Article  CAS  Google Scholar 

  73. Trottmann F, Ishida K, Franke J, Stanisic A, Ishida-Ito M, Kries H, Pohnert G, Hertweck C (2020) Sulfonium acids loaded onto an unusual thiotemplate assembly line construct the cyclopropanol warhead of a Burkholderia virulence factor. Angew Chem. https://doi.org/10.1002/anie.202003958

    Article  Google Scholar 

  74. 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. https://doi.org/10.1128/JB.00425-15

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Tuanyok A, Kim HS, Nierman WC, Yu Y, Dunbar J, Moore RA, Baker P, Tom M, Ling JM, Woods DE (2005) Genome-wide expression analysis of iron regulation in Burkholderia pseudomallei and Burkholderia mallei using DNA microarrays. FEMS Microbiol Lett 252:327–335. https://doi.org/10.1016/j.femsle.2005.09.043

    Article  CAS  PubMed  Google Scholar 

  76. Van Ark G, Berden JA (1977) Binding of HQNO to beef-heart sub-mitochondrial particles. Biochem Biophys Acta 459:119–127. https://doi.org/10.1016/0005-2728(77)90014-7

    Article  PubMed  Google Scholar 

  77. Vial L, Lépine F, Milot S, Groleau MC, Dekimpe V, Woods DE, Déziel E (2008) Burkholderia pseudomallei, B. thailandensis, and B. ambifaria produce 4-hydroxy-2-alkylquinoline analogues with a methyl group at the 3 position that is required for quorum-sensing regulation. J Bacteriol 190:5339–5352. https://doi.org/10.1128/JB.00400-08

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  78. Waters CM, Bassler BL (2005) Quorum sensing: cell-to-cell communication in bacteria. Annu Rev Cell Dev Biol 21:319–346. https://doi.org/10.1146/annurev.cellbio.21.012704.131001

    Article  CAS  Google Scholar 

  79. Wu Y, Seyedsayamdost MR (2017) Synergy and target promiscuity drive structural divergence in bacterial alkylquinolone biosynthesis. Cell Chem Biol 24(1437–1444):e1433. https://doi.org/10.1016/j.chembiol.2017.08.024

    Article  CAS  Google Scholar 

  80. Xavier JB, Kim W, Foster KR (2011) A molecular mechanism that stabilizes cooperative secretions in Pseudomonas aeruginosa. Mol Microbiol 79:166–179. https://doi.org/10.1111/j.1365-2958.2010.07436.x

    Article  CAS  PubMed  Google Scholar 

  81. Xiao G, Déziel E, He J, Lépine F, Lesic B, Castonguay MH, Milot S, Tampakaki AP, Stachel SE, Rahme LG (2006) MvfR, a key Pseudomonas aeruginosa pathogenicity LTTR-class regulatory protein, has dual ligands. Mol Microbiol 62:1689–1699. https://doi.org/10.1111/j.1365-2958.2006.05462.x

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

This work was supported by the NIH through grant R35GM133572 and a pilot award from the COBRE Chemical Biology of Infectious Disease Program (P20 GM113117) to J.R.C. and grant DP2-AI-124786 to M.R.S. Support for E.D. was from the Canadian Institutes of Health Research (CIHR) under award number MOP-142466.

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  1. Department of Molecular Biosciences, University of Kansas, 1200 Sunnyside Ave, Lawrence, KS, 66045, USA

    Jennifer R. Klaus, Pratik Koirala & Josephine R. Chandler

  2. Centre Armand-Frappier Santé Biotechnologie, Institut National de la Recherche Scientifique (INRS), Laval, Québec, H7V 1B7, Canada

    Pauline M. L. Coulon & Eric Déziel

  3. Department of Chemistry, Princeton University, Princeton, NJ, 08544, USA

    Mohammad R. Seyedsayamdost

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Klaus, J.R., Coulon, P.M.L., Koirala, P. et al. Secondary metabolites from the Burkholderia pseudomallei complex: structure, ecology, and evolution. J Ind Microbiol Biotechnol 47, 877–887 (2020). https://doi.org/10.1007/s10295-020-02317-0

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