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Annual Review of Microbiology

Volume 74, 2020

A Bacterial Tower of Babel: Quorum-Sensing Signaling Diversity and Its Evolution

Abstract

Quorum sensing is a process in which bacteria secrete and sense a diffusible molecule, thereby enabling bacterial groups to coordinate their behavior in a density-dependent manner. Quorum sensing has evolved multiple times independently, utilizing different molecular pathways and signaling molecules. A common theme among many quorum-sensing families is their wide range of signaling diversity—different variants within a family code for different signal molecules with a cognate receptor specific to each variant. This pattern of vast allelic polymorphism raises several questions—How do different signaling variants interact with one another? How is this diversity maintained? And how did it come to exist in the first place? Here we argue that social interactions between signaling variants can explain the emergence and persistence of signaling diversity throughout evolution. Finally, we extend the discussion to include cases where multiple diverse systems work in concert in a single bacterium.

Keyword(s): cell-cell communication, diversification, evolution, pherotypes, quorum sensing, social evolution
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2020-09-08
2024-04-18
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Literature Cited

  1. 1. 
    Aakre CD, Herrou J, Phung TN, Perchuk BS, Crosson S, Laub MT 2015. Evolving new protein-protein interaction specificity through promiscuous intermediates. Cell 163:3594–606
     [Google Scholar]
  2. 2. 
    Allan E, Hussain HA, Crawford KR, Miah S, Ascott ZK et al. 2007. Genetic variation in comC, the gene encoding competence-stimulating peptide (CSP) in Streptococcus mutans. FEMS Microbiol. Lett 268:147–51
     [Google Scholar]
  3. 3. 
    Ansaldi M, Dubnau D. 2004. Diversifying selection at the Bacillus quorum-sensing locus and determinants of modification specificity during synthesis of the ComX pheromone. J. Bacteriol. 186:115–21
     [Google Scholar]
  4. 4. 
    Ansaldi M, Marolt D, Stebe T, Mandic-Mulec I, Dubnau D 2002. Specific activation of the Bacillus quorum-sensing systems by isoprenylated pheromone variants. Mol. Microbiol. 44:1561–73
     [Google Scholar]
  5. 5. 
    Asfahl KL, Schuster M. 2017. Social interactions in bacterial cell-cell signaling. FEMS Microbiol. Rev. 41:192–107
     [Google Scholar]
  6. 6. 
    Auchtung JM, Lee CA, Monson RE, Lehman AP, Grossman AD 2005. Regulation of a Bacillus subtilis mobile genetic element by intercellular signaling and the global DNA damage response. PNAS 102:3512554–59
     [Google Scholar]
  7. 7. 
    Axelrod R, Hammond RA, Grafen A 2004. Altruism via kin-selection strategies that rely on arbitrary tags with which they coevolve. Evolution 58:81833–38
     [Google Scholar]
  8. 8. 
    Bannoehr J, Ben Zakour NL, Waller AS, Guardabassi L, Thoday KL et al. 2007. Population genetic structure of the Staphylococcus intermedius group: insights into agr diversification and the emergence of methicillin-resistant strains. J. Bacteriol. 189:238685–92
     [Google Scholar]
  9. 9. 
    Bareia T, Pollak S, Eldar A 2018. Self-sensing in Bacillus subtilis quorum-sensing systems. Nat. Microbiol. 3:183–89
     [Google Scholar]
  10. 10. 
    Barnard AML, Salmond GPC. 2007. Quorum sensing in Erwinia species. Anal. Bioanal. Chem. 387:2415–23
     [Google Scholar]
  11. 11. 
    Bassler BL, Wright M, Silverman MR 1994. Multiple signalling systems controlling expression of luminescence in Vibrio harveyi: sequence and function of genes encoding a second sensory pathway. Mol. Microbiol. 13:2273–86
     [Google Scholar]
  12. 12. 
    Ben-Zion I, Pollak S, Eldar A 2019. Clonality and non-linearity drive facultative-cooperation allele diversity. ISME J 13:3824–35
     [Google Scholar]
  13. 13. 
    Berngruber TW, Weissing FJ, Gandon S 2010. Inhibition of superinfection and the evolution of viral latency. J. Virol. 84:1910200–8
     [Google Scholar]
  14. 14. 
    Bridges AA, Bassler BL. 2019. The intragenus and interspecies quorum-sensing autoinducers exert distinct control over Vibrio cholerae biofilm formation and dispersal. PLOS Biol 17:11e3000429
     [Google Scholar]
  15. 15. 
    Chandler JR, Heilmann S, Mittler JE, Greenberg EP 2012. Acyl-homoserine lactone-dependent eavesdropping promotes competition in a laboratory co-culture model. ISME J 6:122219–28
     [Google Scholar]
  16. 16. 
    Chen X, Schauder S, Potier N, Van Dorsselaer A, Pelczer I et al. 2002. Structural identification of a bacterial quorum-sensing signal containing boron. Nature 415:6871545–49
     [Google Scholar]
  17. 17. 
    Collins CH, Leadbetter JR, Arnold FH 2006. Dual selection enhances the signaling specificity of a variant of the quorum-sensing transcriptional activator LuxR. Nat. Biotechnol. 24:6708–12
     [Google Scholar]
  18. 18. 
    Cooper DG, Macdonald CR, Duff SJB, Kosaric N 1981. Enhanced production of surfactin from Bacillus subtilis by continuous product removal and metal cation additions. Appl. Environ. Microbiol. 42:3408–12
     [Google Scholar]
  19. 19. 
    Cornforth DM, Popat R, McNally L, Gurney J, Scott-Phillips TC et al. 2014. Combinatorial quorum sensing allows bacteria to resolve their social and physical environment. PNAS 111:114280–84
     [Google Scholar]
  20. 20. 
    Dandekar AA, Chugani S, Greenberg EP 2012. Bacterial quorum sensing and metabolic incentives to cooperate. Science 338:6104264–66
     [Google Scholar]
  21. 21. 
    Deng Y, Wu J, Tao F, Zhang L-H 2011. Listening to a new language: DSF-based quorum sensing in Gram-negative bacteria. Chem Rev 111:1160–73
     [Google Scholar]
  22. 22. 
    Diggle SP, Griffin AS, Campbell GS, West SA 2007. Cooperation and conflict in quorum-sensing bacterial populations. Nature 450:7168411–14
     [Google Scholar]
  23. 23. 
    Dogsa I, Choudhary KS, Marsetic Z, Hudaiberdiev S, Vera R et al. 2014. ComQXPA quorum sensing systems may not be unique to Bacillus subtilis: a census in prokaryotic genomes. PLOS ONE 9:5e96122
     [Google Scholar]
  24. 24. 
    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 411:6839813–17
     [Google Scholar]
  25. 25. 
    Dunny GM. 2013. Enterococcal sex pheromones: signaling, social behavior, and evolution. Annu. Rev. Genet. 47:457–82
     [Google Scholar]
  26. 26. 
    Eldar A. 2011. Social conflict drives the evolutionary divergence of quorum sensing. PNAS 108:3313635–40
     [Google Scholar]
  27. 27. 
    Emge P, Moeller J, Jang H, Rusconi R, Yawata Y et al. 2016. Resilience of bacterial quorum sensing against fluid flow. Sci. Rep. 6:33115
     [Google Scholar]
  28. 28. 
    Erez Z, Steinberger-Levy I, Shamir M, Doron S, Stokar-Avihail A et al. 2017. Communication between viruses guides lysis-lysogeny decisions. Nature 541:7638488–93
     [Google Scholar]
  29. 29. 
    Even-Tov E, Omer Bendori S, Pollak S, Eldar A 2016. Transient duplication-dependent divergence and horizontal transfer underlie the evolutionary dynamics of bacterial cell-cell signaling. PLOS Biol 14:12e2000330
     [Google Scholar]
  30. 30. 
    Even-Tov E, Omer Bendori S, Valastyan J, Ke X, Pollak S et al. 2016. Social evolution selects for redundancy in bacterial quorum sensing. PLOS Biol 14:2e1002386
     [Google Scholar]
  31. 31. 
    Fleuchot B, Guillot A, Mézange C, Besset C, Chambellon E et al. 2013. Rgg-associated SHP signaling peptides mediate cross-talk in streptococci. PLOS ONE 8:6e66042
     [Google Scholar]
  32. 32. 
    Fuqua C, Winans SC, Greenberg EP 1996. Census and consensus in bacterial ecosystems: the LuxR-LuxI family of quorum-sensing transcriptional regulators. Annu. Rev. Microbiol. 50:727–51
     [Google Scholar]
  33. 33. 
    Gardner A, West SA. 2010. Greenbeards. Evolution 64:125–38
     [Google Scholar]
  34. 34. 
    Geisinger E, George EA, Muir TW, Novick RP 2008. Identification of ligand specificity determinants in AgrC, the Staphylococcus aureus quorum-sensing receptor. J. Biol. Chem. 283:148930–38
     [Google Scholar]
  35. 35. 
    Geisinger E, Muir TW, Novick RP 2009. agr receptor mutants reveal distinct modes of inhibition by staphylococcal autoinducing peptides. PNAS 106:41216–21
     [Google Scholar]
  36. 36. 
    Grafen A. 1990. Do animals really recognize kin. Anim. Behav. 39:142–54
     [Google Scholar]
  37. 37. 
    Griffin AS, West SA, Buckling A 2004. Cooperation and competition in pathogenic bacteria. Nature 430:1024–27
     [Google Scholar]
  38. 38. 
    Hamilton WD. 1964. The genetical evolution of social behaviour: I. J. Theor. Biol. 7:11–16
     [Google Scholar]
  39. 39. 
    Håvarstein LS, Gaustad P, Nes IF, Morrison DA 1996. Identification of the streptococcal competence-pheromone receptor. Mol. Microbiol. 21:4863–69
     [Google Scholar]
  40. 40. 
    Hawver LA, Jung SA, Ng W-L 2016. Specificity and complexity in bacterial quorum-sensing systems. FEMS Microbiol. Rev. 40:5738–52
     [Google Scholar]
  41. 41. 
    Henke JM, Bassler BL. 2004. Three parallel quorum-sensing systems regulate gene expression in Vibrio harveyi. J. Bacteriol 186:206902–14
     [Google Scholar]
  42. 42. 
    Henkel M, Schmidberger A, Kühnert C, Beuker J, Bernard T et al. 2013. Kinetic modeling of the time course of N-butyryl-homoserine lactone concentration during batch cultivations of Pseudomonas aeruginosa PAO1. Appl. Microbiol. Biotechnol. 97:177607–16
     [Google Scholar]
  43. 43. 
    Hense BA, Kuttler C, Müller J, Rothballer M, Hartmann A, Kreft J-U 2007. Does efficiency sensing unify diffusion and quorum sensing?. Nat. Rev. Microbiol. 5:3230–39
     [Google Scholar]
  44. 44. 
    Hense BA, Schuster M. 2015. Core principles of bacterial autoinducer systems. Microbiol. Mol. Biol. Rev. 79:1153–69
     [Google Scholar]
  45. 45. 
    Hoover SE, Perez AJ, Tsui H-CT, Sinha D, Smiley DL et al. 2015. A new quorum-sensing system (TprA/PhrA) for Streptococcus pneumoniae D39 that regulates a lantibiotic biosynthesis gene cluster. Mol. Microbiol. 97:2229–43
     [Google Scholar]
  46. 46. 
    Horswill AR, Stoodley P, Stewart PS, Parsek MR 2007. The effect of the chemical, biological, and physical environment on quorum sensing in structured microbial communities. Anal. Bioanal. Chem. 387:2371–80
     [Google Scholar]
  47. 47. 
    Jansen VAA, van Baalen M 2006. Altruism through beard chromodynamics. Nature 440:7084663–66
     [Google Scholar]
  48. 48. 
    Ji G, Beavis R, Novick RP 1997. Bacterial interference caused by autoinducing peptide variants. Science 276:53212027–30
     [Google Scholar]
  49. 49. 
    Ke X, Miller LC, Bassler BL 2015. Determinants governing ligand specificity of the Vibrio harveyi LuxN quorum-sensing receptor. Mol. Microbiol. 95:1127–42
     [Google Scholar]
  50. 50. 
    Kearns DB, Losick R. 2004. Swarming motility in undomesticated Bacillus subtilis. Mol. Microbiol. 49:3581–90
     [Google Scholar]
  51. 51. 
    Kim MK, Ingremeau F, Zhao A, Bassler BL, Stone HA 2016. Local and global consequences of flow on bacterial quorum sensing. Nat. Microbiol. 1:15005
     [Google Scholar]
  52. 52. 
    Komarova NL. 2014. Spatial interactions and cooperation can change the speed of evolution of complex phenotypes. PNAS 111:Suppl. 310789–95
     [Google Scholar]
  53. 53. 
    Kotte A-K, Severn O, Bean Z, Schwarz K, Minton NP, Winzer K 2020. RRNPP-type quorum sensing affects solvent formation and sporulation in Clostridium acetobutylicum. . Microbiology 166:6579–92 https://doi.org/10.1099/mic.0.000916
    [Crossref] [Google Scholar]
  54. 54. 
    Lazazzera BA, Grossman AD. 1998. The ins and outs of peptide signaling. Trends Microbiol 6:7288–94
     [Google Scholar]
  55. 55. 
    Lazazzera BA, Solomon JM, Grossman AD 1997. An exported peptide functions intracellularly to contribute to cell density signaling in B. subtilis. . Cell 89:6917–25
     [Google Scholar]
  56. 56. 
    Le KY, Otto M. 2015. Quorum-sensing regulation in staphylococci—an overview. Front. Microbiol. 6:1174
     [Google Scholar]
  57. 57. 
    Lynch M, Hagner K. 2015. Evolutionary meandering of intermolecular interactions along the drift barrier. PNAS 112:1E30–38
     [Google Scholar]
  58. 58. 
    Lyons NA, Kraigher B, Stefanic P, Mandic-Mulec I, Kolter R 2016. A combinatorial kin discrimination system in Bacillus subtilis. Curr. Biol 26:6733–42
     [Google Scholar]
  59. 59. 
    Mandic-Mulec I, Kraigher B, Cepon U, Mahne I 2003. Variability of the quorum sensing system in natural isolates of Bacillus sp. Food Technol. Biotechnol. 41:123–28
     [Google Scholar]
  60. 60. 
    Manefield M, De Nys R, Kumar N, Read R, Givskov M et al. 1999. Evidence that halogenated furanones from Delisea pulchra inhibit acylated homoserine lactone (AHL)-mediated gene expression by displacing the AHL signal from its receptor protein. Microbiology 145:2283–91
     [Google Scholar]
  61. 61. 
    Martin SH, Wingfield BD, Wingfield MJ, Steenkamp ET 2011. Causes and consequences of variability in peptide mating pheromones of ascomycete fungi. Mol. Biol. Evol. 28:71987–2003
     [Google Scholar]
  62. 62. 
    Mathesius U, Mulders S, Gao M, Teplitski M, Caetano-Anollés G et al. 2003. Extensive and specific responses of a eukaryote to bacterial quorum-sensing signals. PNAS 100:31444–49
     [Google Scholar]
  63. 63. 
    Miller EL, Evans BA, Cornejo OE, Roberts IS, Rozen DE 2017. Pherotype polymorphism in Streptococcus pneumoniae has no obvious effects on population structure and recombination. Genome Biol. Evol. 9:102546–59
     [Google Scholar]
  64. 64. 
    Miller EL, Kjos M, Abrudan MI, Roberts IS, Veening JW, Rozen DE 2018. Eavesdropping and crosstalk between secreted quorum sensing peptide signals that regulate bacteriocin production in Streptococcus pneumoniae. . ISME J 12:102363–75
     [Google Scholar]
  65. 65. 
    Mitri S, Richard Foster K 2013. The genotypic view of social interactions in microbial communities. Annu. Rev. Genet. 47:247–73
     [Google Scholar]
  66. 66. 
    Mok KC. 2003. Vibrio harveyi quorum sensing: a coincidence detector for two autoinducers controls gene expression. EMBO J 22:4870–81
     [Google Scholar]
  67. 67. 
    Monnet V, Gardan R. 2015. Quorum-sensing regulators in Gram-positive bacteria: ‘cherchez le peptide. .’ Mol. Microbiol. 97:2181–84
     [Google Scholar]
  68. 68. 
    Morohoshi T, Kato M, Fukamachi K, Kato N, Ikeda T 2008. N-Acylhomoserine lactone regulates violacein production in Chromobacterium violaceum type strain ATCC12472. FEMS Microbiol. Lett. 12472:124–30
     [Google Scholar]
  69. 69. 
    Moura-Alves P, Puyskens A, Stinn A, Klemm M, Guhlich-Bornhof U et al. 2019. Host monitoring of quorum sensing during Pseudomonas aeruginosa infection. Science 366:6472eaaw1629
     [Google Scholar]
  70. 70. 
    Mukherjee S, Bassler BL. 2019. Bacterial quorum sensing in complex and dynamically changing environments. Nat. Rev. Microbiol. 17:6371–82
     [Google Scholar]
  71. 71. 
    Neiditch MB, Capodagli GC, Prehna G, Federle MJ 2017. Genetic and structural analyses of RRNPP intercellular peptide signaling of gram-positive bacteria. Annu. Rev. Genet. 51:311–33
     [Google Scholar]
  72. 72. 
    Ng W-L, 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. 79:61407–17
     [Google Scholar]
  73. 73. 
    Novick RP, Geisinger E. 2008. Quorum sensing in staphylococci. Annu. Rev. Genet. 42:541–64
     [Google Scholar]
  74. 74. 
    Ohno S. 2013. Evolution by Gene Duplication New York: Springer Sci. Bus. Media
  75. 75. 
    Papenfort K, Bassler BL. 2016. Quorum sensing signal-response systems in Gram-negative bacteria. Nat. Rev. Microbiol. 14:9576–88
     [Google Scholar]
  76. 76. 
    Parashar V, Jeffrey PD, Neiditch MB 2013. Conformational change-induced repeat domain expansion regulates Rap phosphatase quorum-sensing signal receptors. PLOS Biol 11:3e1001512
     [Google Scholar]
  77. 77. 
    Perchat S, Dubois T, Zouhir S, Gominet M, Poncet S et al. 2011. A cell-cell communication system regulates protease production during sporulation in bacteria of the Bacillus cereus group. Mol. Microbiol. 82:3619–33
     [Google Scholar]
  78. 78. 
    Perchat S, Talagas A, Zouhir S, Poncet S, Bouillaut L et al. 2016. NprR, a moonlighting quorum sensor shifting from a phosphatase activity to a transcriptional activator. Microb. Cell 3:11573–75
     [Google Scholar]
  79. 79. 
    Perego M, Hoch JA. 1996. Cell-cell communication regulates the effects of protein aspartate phosphatases on the phosphorelay controlling development in Bacillus subtilis. . PNAS 93:41549–53
     [Google Scholar]
  80. 80. 
    Piewngam P, Zheng Y, Nguyen TH, Dickey SW, Joo HS et al. 2018. Pathogen elimination by probiotic Bacillus via signalling interference. Nature 562:7728532–37
     [Google Scholar]
  81. 81. 
    Pollak S, Omer-Bendori S, Even-Tov E, Lipsman V, Bareia T et al. 2016. Facultative cheating supports the coexistence of diverse quorum-sensing alleles. PNAS 113:82152–57
     [Google Scholar]
  82. 82. 
    Pollitt EJG, West SA, Crusz SA, Burton-Chellew MN, Diggle SP 2014. Cooperation, quorum sensing, and evolution of virulence in Staphylococcus aureus. Infect. . Immun 82:31045–51
     [Google Scholar]
  83. 83. 
    Pozzi G, Masala L, Iannelli F, Manganelli R, Håvarstein LS et al. 1996. Competence for genetic transformation in encapsulated strains of Streptococcus pneumoniae: two allelic variants of the peptide pheromone. J. Bacteriol. 178:206087–90
     [Google Scholar]
  84. 84. 
    Rainey PB, Rainey K. 2003. Evolution of cooperation and conflict in experimental bacterial populations. Nature 425:72–74
     [Google Scholar]
  85. 85. 
    Redfield RJ. 2002. Is quorum sensing a side effect of diffusion sensing. Trends Microbiol 10:8365–70
     [Google Scholar]
  86. 86. 
    Rezzonico F, Duffy B. 2008. Lack of genomic evidence of AI-2 receptors suggests a non-quorum sensing role for luxS in most bacteria. BMC Microbiol 8:1154
     [Google Scholar]
  87. 87. 
    Robinson DA, Monk AB, Cooper JE, Feil EJ, Enright MC 2005. Evolutionary genetics of the accessory gene regulator (agr) locus in Staphylococcus aureus. J. . Bacteriol 187:248312–21
     [Google Scholar]
  88. 88. 
    Rousset F, Roze D. 2007. Constraints on the origin and maintenance of genetic kin recognition. Evolution 61:102320–30
     [Google Scholar]
  89. 89. 
    Sandoz KM, Mitzimberg SM, Schuster M 2007. Social cheating in Pseudomonas aeruginosa quorum sensing. PNAS 104:4015876–81
     [Google Scholar]
  90. 90. 
    Santorelli LA, Thompson CRL, Villegas E, Svetz J, Dinh C et al. 2008. Facultative cheater mutants reveal the genetic complexity of cooperation in social amoebae. Nature 451:71821107–10
     [Google Scholar]
  91. 91. 
    Sayou C, Monniaux M, Nanao MH, Moyroud E, Brockington SF et al. 2014. A promiscuous intermediate underlies the evolution of LEAFY DNA binding specificity. Science 343:6171645–48
     [Google Scholar]
  92. 92. 
    Schaefer AL, Hanzelka BL, Eberhard A, Greenberg EP 1996. Quorum sensing in Vibrio fischeri: probing autoinducer-LuxR interactions with autoinducer analogs. J. Bacteriol. 178:102897–901
     [Google Scholar]
  93. 93. 
    Schuster M, Sexton JD, Diggle SP, Greenberg EP 2013. Acyl-homoserine lactone quorum sensing: from evolution to application. Annu. Rev. Microbiol. 67:43–63
     [Google Scholar]
  94. 94. 
    Schuster M, Lostroh CP, Ogi T, Greenberg EP 2003. Identification, timing, and signal specificity of Pseudomonas aeruginosa quorum-controlled genes: a transcriptome analysis. J. Bacteriol. 185:72066–79
     [Google Scholar]
  95. 95. 
    Schuster M, Sexton DJ, Hense BA 2017. Why quorum sensing controls private goods. Front. Microbiol. 8:885
     [Google Scholar]
  96. 96. 
    Shanker E, Morrison DA, Talagas A, Nessler S, Federle MJ, Prehna G 2016. Pheromone recognition and selectivity by ComR proteins among Streptococcus species. PLOS Pathog 12:12e1005979
     [Google Scholar]
  97. 97. 
    Silpe JE, Bassler BL. 2019. A host-produced quorum-sensing autoinducer controls a phage lysis-lysogeny decision. Cell 176:1–2268–80.e13
     [Google Scholar]
  98. 98. 
    Slamti L, Lereclus D. 2002. A cell-cell signaling peptide activates the PlcR virulence regulon in bacteria of the Bacillus cereus group. EMBO J 21:174550–59
     [Google Scholar]
  99. 99. 
    Slamti L, Lereclus D. 2005. Specificity and polymorphism of the PlcR-PapR quorum-sensing system in the Bacillus cereus group. Society 187:31182–87
     [Google Scholar]
  100. 100. 
    Smith P, Cozart J, Lynn BK, Alberts E, Frangipani E, Schuster M 2019. Bacterial cheaters evade punishment by cyanide. iScience 19:101–9
     [Google Scholar]
  101. 101. 
    Stokar-Avihail A, Tal N, Erez Z, Lopatina A, Sorek R 2019. Widespread utilization of peptide communication in phages infecting soil and pathogenic bacteria. Cell Host Microbe 25:5746–55.e5
     [Google Scholar]
  102. 102. 
    Strassmann JE, Gilbert OM, Queller DC 2011. Kin discrimination and cooperation in microbes. Annu. Rev. Microbiol. 65:349–67
     [Google Scholar]
  103. 103. 
    Strassmann JE, Zhu Y, Queller DC 2000. Altruism and social cheating in the social amoeba Dictyostelium discoideum. . Nature 408:6815965–67
     [Google Scholar]
  104. 104. 
    Sung JML, Chantler PD, Lloyd DH 2006. Accessory gene regulator locus of Staphylococcus intermedius. Infect. . Immun 74:52947–56
     [Google Scholar]
  105. 105. 
    Swem LR, Swem DL, O'Loughlin CT, Gatmaitan R, Zhao B et al. 2009. A quorum-sensing antagonist targets both membrane-bound and cytoplasmic receptors and controls bacterial pathogenicity. Mol. Cell 35:2143–53
     [Google Scholar]
  106. 106. 
    Teplitski M, Robinson JB, Bauer WD 2000. Plants secrete substances that mimic bacterial N-acyl homoserine lactone signal activities and affect population density-dependent behaviors in associated bacteria. Mol. Plant-Microbe Interact. 13:6637–48
     [Google Scholar]
  107. 107. 
    Tortosa P, Logsdon L, Kraigher B, Itoh Y 2001. Specificity and genetic polymorphism of the Bacillus competence quorum-sensing system. Society 183:2451–60
     [Google Scholar]
  108. 108. 
    Tran L-SP, Nagai T, Itoh Y 2000. Divergent structure of the ComQXPA quorum-sensing components: molecular basis of strain-specific communication mechanism in Bacillus subtilis. Mol. Microbiol 37:51159–71
     [Google Scholar]
  109. 109. 
    Voichek M, Maaß S, Kroniger T, Becher D, Sorek R 2019. Peptide-based quorum sensing systems in Paenibacillus polymyxa. bioRxiv 767517
  110. 110. 
    Wall D. 2016. Kin recognition in bacteria. Annu. Rev. Microbiol. 70:143–60
     [Google Scholar]
  111. 111. 
    Wang M, Schaefer AL, Dandekar AA, Greenberg EP 2015. Quorum sensing and policing of Pseudomonas aeruginosa social cheaters. PNAS 112:72187–91
     [Google Scholar]
  112. 112. 
    Waters CM, Bassler BL. 2005. Quorum sensing: cell-to-cell communication in bacteria. Annu. Rev. Cell Dev. Biol. 21:319–46
     [Google Scholar]
  113. 113. 
    West SA, Diggle SP, Buckling A, Gardner A, Griffin AS 2007. The social lives of microbes. Annu. Rev. Ecol. Evol. Syst. 38:53–77
     [Google Scholar]
  114. 114. 
    West SA, Griffin AS, Gardner A, Diggle SP 2006. Social evolution theory for microorganisms. Nat. Rev. Microbiol. 4:8597–607
     [Google Scholar]
  115. 115. 
    Whatmore AM, Barcus VA, Dowson CG 1999. Genetic diversity of the streptococcal competence (com) gene locus. J. Bacteriol. 181:103144–54
     [Google Scholar]
  116. 116. 
    Whiteley M, Diggle SP, Greenberg EP 2017. Progress in and promise of bacterial quorum sensing research. Nature 551:7680313–20
     [Google Scholar]
  117. 117. 
    Wilder CN, Diggle SP, Schuster M 2011. Cooperation and cheating in Pseudomonas aeruginosa: the roles of the las, rhl and pqs quorum-sensing systems. ISME J 5:81332–43
     [Google Scholar]
  118. 118. 
    Wuster A, Babu MM. 2008. Conservation and evolutionary dynamics of the agr cell-to-cell communication system across firmicutes. J. Bacteriol. 190:2743–46
     [Google Scholar]
  119. 119. 
    Zhou L, Slamti L, Lereclus D, Raymond B 2020. Optimal response to quorum-sensing signals varies in different host environments with different pathogen group size. mBio 11:3e00535–20
     [Google Scholar]
  120. 120. 
    Zhou L, Slamti L, Nielsen-LeRoux C, Lereclus D, Raymond B 2014. The social biology of quorum sensing in a naturalistic host pathogen system. Curr. Biol. 24:202417–22
     [Google Scholar]
  121. 121. 
    Zhou L, Zhang L-H, Cámara M, He Y-W 2017. The DSF family of quorum sensing signals: diversity, biosynthesis, and turnover. Trends Microbiol 25:4293–303
     [Google Scholar]
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A Bacterial Tower of Babel: Quorum-Sensing Signaling Diversity and Its Evolution
Annual Review of Microbiology 74, 587 (2020); https://doi.org/10.1146/annurev-micro-012220-063740
/content/journals/10.1146/annurev-micro-012220-063740
/content/journals/10.1146/annurev-micro-012220-063740
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  • Article Type: Review Article

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