Amphiphilic Lipids, Signaling Molecules, and Quorum Sensing

Reference work entry
Part of the Handbook of Hydrocarbon and Lipid Microbiology book series (HHLM)

Abstract

Many bacteria communicate with each other through the action of diffusible signal molecules, a process that has been termed quorum sensing (QS). QS acts to regulate diverse processes in different bacteria, to include the formation of biofilms, cellular differentiation, synthesis of antibiotics and other secondary metabolites, and the production of virulence factors in pathogens. Many bacteria use amphiphilic lipids of different chemical classes as signal molecules. N-acyl homoserine lactones, cis-2-unsaturated fatty acids, methyl esters of hydroxylated fatty acids, and tridecanone derivatives have been described in different Gram-negative organisms and gamma-butyrolactones in Gram-positive streptomycetes. A diverse range of mechanisms for perception and transduction of these signals has been described. Here we review these different signals, their mode of biosynthesis, and transduction pathways before going on to discuss interference of QS as a strategy for the control of bacterial disease.

References

  1. Amari DT, Marques CNH, Davies DG (2013) The putative enoyl-coenzyme A hydratase DspI is required for production of the Pseudomonas aeruginosa biofilm dispersion autoinducer cis-2-decenoic acid. J Bacteriol 195:4600–4610CrossRefPubMedPubMedCentralGoogle Scholar
  2. An SQ, Allan JH, McCarthy Y, Febrer M, Dow JM, Ryan RP (2014) The PAS domain-containing histidine kinase RpfS is a second sensor for the diffusible signal factor of Xanthomonas campestris. Mol Microbiol 92:586–597CrossRefPubMedPubMedCentralGoogle Scholar
  3. Barber CE, Tang JL, Feng JX, Pan MQ, Wilson TJ, Slater H, Dow JM, Williams P, Daniels MJ (1997) A novel regulatory system required for pathogenicity of Xanthomonas campestris is mediated by a small diffusible signal molecule. Mol Microbiol 24:555–566CrossRefPubMedGoogle Scholar
  4. Beaulieu ED, Ionescu M, Chatterjee S, Yokota K, Trauner D, Lindow S (2013) Characterization of a diffusible signaling factor from Xylella fastidiosa. MBio 4:e00539–e00512CrossRefPubMedPubMedCentralGoogle Scholar
  5. Bi H, Christensen QH, Feng Y, Wang H, Cronan JE (2012) The Burkholderia cenocepacia BDSF quorum sensing fatty acid is synthesized by a bifunctional crotonase homologue having both dehydratase and thioesterase activities. Mol Microbiol 83:840–855CrossRefPubMedPubMedCentralGoogle Scholar
  6. Bi H, Yu Y, Dong H, Wang H, Cronan JE (2014) Xanthomonas campestris RpfB is a fatty acyl-CoA ligase required to counteract the thioesterase activity of the RpfF diffusible signal factor (DSF) synthase. Mol Microbiol 93:262–275CrossRefPubMedPubMedCentralGoogle Scholar
  7. Biarnes-Carrera M, Breitling R, Takano E (2015) Butyrolactone signalling circuits for synthetic biology. Curr Opin Chem Biol 28:91–98CrossRefPubMedGoogle Scholar
  8. Boon C, Deng Y, Wang LH, He Y, Xu JL, Fan Y, Pan SQ, Zhang LH (2008) A novel DSF-like signal from Burkholderia cenocepacia interferes with Candida albicans morphological transition. ISME J 2:27–36CrossRefPubMedGoogle Scholar
  9. Caserta R, Picchi SC, Takita MA, Tomaz JP, Pereira WE, Machado MA, Ionescu M, Lindow S, De Souza AA (2014) Expression of Xylella fastidiosa RpfF in citrus disrupts signaling in Xanthomonas citri subsp. citri and thereby its virulence. Mol Plant-Microbe Interact 27:1241–1252CrossRefPubMedGoogle Scholar
  10. Chowdhary PK, Keshavan N, Nguyen HQ, Peterson JA, González JE, Haines DC (2007) Bacillus megaterium CYP102A1 oxidation of acyl homoserine lactones and acyl homoserines. Biochemistry 46:14429–14437CrossRefPubMedGoogle Scholar
  11. Clough SJ, Lee KE, Schell MA, Denny TP (1997) A two-component system in Ralstonia (Pseudomonas) solanacearum modulates production of PhcA-regulated virulence factors in response to 3-hydroxypalmitic acid methyl ester. J Bacteriol 179:3639–3648CrossRefPubMedPubMedCentralGoogle Scholar
  12. Cooley M, Chhabra SR, Williams P (2008) N-acylhomoserine lactone-mediated quorum sensing: a twist in the tail and a blow for host immunity. Chem Biol 15:1141–1147CrossRefPubMedGoogle Scholar
  13. Curtis MM, Russell R, Moreira CG, Adebesin AM, Wang C, Williams NS, Taussig R, Stewart D, Zimmern P, Lu B, Prasad RN, Zhu C, Rasko DA, Huntley JF, Falck JR, Sperandio V (2014) QseC inhibitors as an antivirulence approach for gram-negative pathogens. MBio 5:e02165CrossRefPubMedPubMedCentralGoogle Scholar
  14. Davies DG, Marques CNH (2009) A fatty acid messenger is responsible for inducing dispersion in microbial biofilms. J Bacteriol 191:1393–1403CrossRefPubMedGoogle Scholar
  15. Deng Y, Wu J, Tao F, Zhang LH (2011) Listening to a new language: DSF-based quorum sensing in gram-negative bacteria. Chem Rev 111:160–173CrossRefPubMedGoogle Scholar
  16. Deng Y, Schmid N, Wang C, Wang J, Pessi G, Wu D, Lee J, Aguilar C, Ahrens CH, Chang C, Song H, Eberl L, Zhang LH (2012) Cis-2-dodecenoic acid receptor RpfR links quorum-sensing signal perception with regulation of virulence through cyclic dimeric guanosine monophosphate turnover. Proc Natl Acad Sci U S A 109:15479–15484CrossRefPubMedPubMedCentralGoogle Scholar
  17. Deng Y, Liu X, Wu J, Lee J, Chen S, Cheng Y, Zhang C, Zhang LH (2015) The host plant metabolite glucose is the precursor of diffusible signal factor (DSF) family signals in Xanthomonas campestris. Appl Environ Microbiol 81:2861–2868CrossRefPubMedPubMedCentralGoogle Scholar
  18. Dong YH, Wang LH, Xu JL, Zhang HB, Zhang XF, Zhang LH (2001) Quenching quorum-sensing-dependent bacterial infection by an N-acyl homoserine lactonase. Nature 411:813–817CrossRefPubMedGoogle Scholar
  19. Fray RG, Throup JP, Daykin M, Wallace A, Williams P, Stewart GS, Grierson D (1999) Plants genetically modified to produce N-acylhomoserine lactones communicate with bacteria. Nat Biotechnol 17:1017–1020CrossRefPubMedGoogle Scholar
  20. Fuqua C, Parsek MR, Greenberg EP (2001) Regulation of gene expression by cell-to-cell communication: acyl-homoserine lactone quorum sensing. Annu Rev Genet 35:439–468CrossRefPubMedGoogle Scholar
  21. García-Contreras R, Maeda T, Wood TK (2016) Can resistance against quorum-sensing interference be selected? ISME J 10:4–10CrossRefPubMedGoogle Scholar
  22. He YW, Zhang LH (2008) Quorum sensing and virulence regulation in Xanthomonas campestris. FEMS Microbiol Rev 32:842–857CrossRefPubMedGoogle Scholar
  23. He Y-W, Je W, Cha J-S, Zhang L-H (2010) Rice bacterial blight pathogen Xanthomonas oryzae pv. oryzae produces multiple DSF-family signals in regulation of virulence factor production. BMC Microbiol 10:187CrossRefPubMedPubMedCentralGoogle Scholar
  24. Higgins DA, Pomianek ME, Kraml CM, Taylor RK, Semmelhack MF, Bassler BL (2007) The major Vibrio cholerae autoinducer and its role in virulence factor production. Nature 450:883–886CrossRefPubMedGoogle Scholar
  25. Hogan DA, Vik A, Kolter R (2004) A Pseudomonas aeruginosa quorum-sensing molecule influences Candida albicans morphology. Mol Microbiol 54:1212–1223CrossRefPubMedGoogle Scholar
  26. Jimenez PN, Koch G, Thompson JA, Xavier KB, Cool RH, Quax WJ (2012) The multiple signaling systems regulating virulence in Pseudomonas aeruginosa. Microbiol Mol Biol Rev 76:46–65CrossRefPubMedGoogle Scholar
  27. Kai K, Ohnishi H, Shimatani M, Ishikawa S, Mori Y, Kiba A, Ohnishi K, Tabuchi M, Hikichi Y (2015) Methyl 3-hydroxymyristate, a diffusible signal mediating phc quorum sensing in Ralstonia solanacearum. Chembiochem 16:2309–2318CrossRefPubMedGoogle Scholar
  28. Kato JY, Funa N, Watanabe H, Ohnishi Y, Horinouchi S (2007) Biosynthesis of gamma-butyrolactone autoregulators that switch on secondary metabolism and morphological development in Streptomyces. Proc Natl Acad Sci U S A 104:2378–2383CrossRefPubMedPubMedCentralGoogle Scholar
  29. LaSarre B, Federle MJ (2013) Exploiting quorum sensing to confuse bacterial pathogens. Microbiol Mol Biol Rev 77:73–111CrossRefPubMedPubMedCentralGoogle Scholar
  30. Lindow S, Newman K, Chatterjee S, Baccari C, Lavarone AT, Ionescu M (2014) Production of Xylella fastidiosa diffusible signal factor in transgenic grape causes pathogen confusion and reduction in severity of Pierce’s disease. Mol Plant-Microbe Interact 27:244–254CrossRefPubMedGoogle Scholar
  31. Mae A, Montesano M, Koiv V, Palva ET (2001) Transgenic plants producing the bacterial pheromone N-acyl-homoserine lactone exhibit enhanced resistance to the bacterial phytopathogen Erwinia carotovora. Mol Plant-Microbe Interact 14:1035–1042CrossRefPubMedGoogle Scholar
  32. McCarthy Y, Yang L, Twomey KB, Sass A, Tolker-Nielsen T, Mahenthiralingam E, Dow JM, Ryan RP (2010) A sensor kinase recognizing the cell-cell signal BDSF (cis-2-dodecenoic acid) regulates virulence in Burkholderia cenocepacia. Mol Microbiol 77:1220–1236CrossRefPubMedGoogle Scholar
  33. Newman KL, Chatterjee S, Ho KA, Lindow SE (2008) Virulence of plant pathogenic bacteria attenuated by degradation of fatty acid cell-to-cell signaling factors. Mol Plant-Microbe Interact 21:326–334CrossRefPubMedGoogle Scholar
  34. Ng WL, Bassler BL (2009) Bacterial quorum-sensing network architectures. Annu Rev Genet 43:197–222CrossRefPubMedPubMedCentralGoogle Scholar
  35. Ng WL, Perez LJ, Wei Y, Kraml C, Semmelhack MF, Bassler BL (2011) Signal production and detection specificity in Vibrio CqsA/CqsS quorum-sensing systems. Mol Microbiol 79:1407–1417CrossRefPubMedPubMedCentralGoogle Scholar
  36. Pappas KM, Weingart CL, Winans SC (2004) Chemical communication in proteobacteria: biochemical and structural studies of signal synthases and receptors required for intercellular signalling. Mol Microbiol 53:755–769CrossRefPubMedGoogle Scholar
  37. Platt TG, Fuqua C (2010) What’s in a name? The semantics of quorum sensing. Trends Microbiol 18:383–387CrossRefPubMedPubMedCentralGoogle Scholar
  38. Polkade AV, Mantri SS, Patwekar UJ, Jangid K (2016) Quorum sensing: an under-explored phenomenon in the phylum actinobacteria. Front Microbiol 7:131CrossRefPubMedPubMedCentralGoogle Scholar
  39. Römling U, Galperin MY, Gomelsky M (2013) Cyclic di-GMP: the first 25 years of a universal bacterial second messenger. Microbiol Mol Biol Rev 77:1–52CrossRefPubMedPubMedCentralGoogle Scholar
  40. Ryan RP, An SQ, Allan JH, McCarthy Y, Dow JM (2015) The DSF family of cell-cell signals: an expanding class of bacterial virulence regulators. PLoS Pathog 11:e1004986CrossRefPubMedPubMedCentralGoogle Scholar
  41. Schaefer AL, Greenberg EP, Oliver CM, Oda Y, Huang JJ, Bittan-Banin G, Peres CM, Schmidt S, Juhaszova K, Sufrin JR, Harwood CS (2008) A new class of homoserine lactone quorum-sensing signals. Nature 454:595–599CrossRefPubMedGoogle Scholar
  42. Schenk ST, Hernández-Reyes C, Samans B, Stein E, Neumann C, Schikora M, Reichelt M, Mithöfer A, Becker A, Kogel KH, Schikora A (2014) N-acyl-homoserine lactone primes plants for cell wall reinforcement and induces resistance to bacterial pathogens via the salicylic acid/oxylipin pathway. Plant Cell 26:2708–2723CrossRefPubMedPubMedCentralGoogle Scholar
  43. Short FL, Murdoch SL, Ryan RP (2014) Polybacterial human disease: the ills of social networking. Trends Microbiol 22:508–516CrossRefPubMedPubMedCentralGoogle Scholar
  44. Slater H, Alvarez-Morales A, Barber CE, Daniels MJ, Dow JM (2000) A two-component system involving an HD-GYP domain protein links cell-cell signalling to pathogenicity gene expression in Xanthomonas campestris. Mol Microbiol 38:986–1003CrossRefPubMedGoogle Scholar
  45. Suppiger A, Eshwar AK, Stephan R, Kaever V, Eberl L, Lehner A (2016) The DSF type quorum sensing signalling system RpfF/R regulates diverse phenotypes in the opportunistic pathogen cronobacter. Sci Rep 6:18753CrossRefPubMedPubMedCentralGoogle Scholar
  46. Takano E (2006) Gamma-butyrolactones: streptomyces signalling molecules regulating antibiotic production and differentiation. Curr Opin Microbiol 9:287–294CrossRefPubMedGoogle Scholar
  47. Takano E, Chakraburtty R, Nihira T, Yamada Y, Bibb MJ (2001) A complex role for the gamma-butyrolactone SCB1 in regulating antibiotic production in Streptomyces coelicolor A3(2). Mol Microbiol 41:1015–1028CrossRefPubMedGoogle Scholar
  48. Teplitski M, Mathesius U, Rumbaugh KP (2011) Perception and degradation of N-acyl homoserine lactone quorum sensing signals by mammalian and plant cells. Chem Rev 111:100–116CrossRefPubMedGoogle Scholar
  49. Wang LH, He Y, Gao Y, Wu JE, Dong YH, He C, Wang SX, Weng LX, Xu JL, Tay L, Fang RX, Zhang LH (2004) A bacterial cell-cell communication signal with cross-kingdom structural analogues. Mol Microbiol 51:903–912CrossRefPubMedGoogle Scholar
  50. Waters CM, Bassler BL (2005) Quorum sensing: cell-to-cell communication in bacteria. Annu Rev Cell Dev Biol 21:319–346CrossRefPubMedGoogle Scholar
  51. Wei Y, Perez LJ, Ng WL, Semmelhack MF, Bassler BL (2011) Mechanism of Vibrio cholerae autoinducer-1 biosynthesis. ACS Chem Biol 6:356–365CrossRefPubMedPubMedCentralGoogle Scholar
  52. Whitehead NA, Barnard AM, Slater H, Simpson NJ, Salmond GP (2001) Quorum-sensing in gram-negative bacteria. FEMS Microbiol Rev 25:365–404CrossRefPubMedGoogle Scholar
  53. Wu F, Menn DJ, Wang X (2014) Quorum-sensing crosstalk-driven synthetic circuits: from unimodality to trimodality. Chem Biol 21:1629–1638CrossRefPubMedPubMedCentralGoogle Scholar
  54. Zhou L, Yu Y, Chen X, Diab AA, Ruan L, He J, Wang H, He YW (2015a) The multiple DSF-family QS signals are synthesized from carbohydrate and branched-chain amino acids via the FAS elongation cycle. Sci Rep 5:13294CrossRefPubMedPubMedCentralGoogle Scholar
  55. Zhou L, Wang XY, Sun S, Yang LC, Jiang BL, He YW (2015b) Identification and characterization of naturally occurring DSF-family quorum sensing signal turnover system in the phytopathogen Xanthomonas. Environ Microbiol 17:4646–4658CrossRefPubMedGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  1. 1.School of MicrobiologyUniversity College CorkCorkIreland

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