1932

Abstract

Bacteria depend on two-component systems to detect and respond to threats. Simple pathways comprise a single sensor kinase (SK) that detects a signal and activates a response regulator protein to mediate an appropriate output. These simple pathways with only a single SK are not well suited to making complex decisions where multiple different stimuli need to be evaluated. A recently emerging theme is the existence of multikinase networks (MKNs) where multiple SKs collaborate to detect and integrate numerous different signals to regulate a major lifestyle switch, e.g., between virulence, sporulation, biofilm formation, and cell division. In this review, the role of MKNs and the phosphosignaling mechanisms underpinning their signal integration and decision making are explored.

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2019-09-08
2024-03-28
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Literature Cited

  1. 1. 
    Aguilar C, Vlamakis H, Guzman A, Losick R, Kolter R 2010. KinD is a checkpoint protein linking spore formation to extracellular-matrix production in Bacillus subtilis biofilms. mBio 1:e00035–10
    [Google Scholar]
  2. 2. 
    Aldridge P, Paul R, Goymer P, Rainey P, Jenal U 2003. Role of the GGDEF regulator PleD in polar development of Caulobacter crescentus. Mol. Microbiol 47:1695–708
    [Google Scholar]
  3. 3. 
    Anetzberger C, Pirch T, Jung K 2009. Heterogeneity in quorum sensing-regulated bioluminescence of Vibrio harveyi. Mol. Microbiol 73:267–77
    [Google Scholar]
  4. 4. 
    Balasubramanian D, Schneper L, Kumari H, Mathee K 2013. A dynamic and intricate regulatory network determines Pseudomonas aeruginosa virulence. Nucleic Acids Res 41:1–20
    [Google Scholar]
  5. 5. 
    Bassler BL, Greenberg EP, Stevens AM 1997. Cross-species induction of luminescence in the quorum-sensing bacterium Vibrio harveyi. J. Bacteriol 179:4043–45
    [Google Scholar]
  6. 6. 
    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. 13:273–86
    [Google Scholar]
  7. 7. 
    Bastedo DP, Marczynski GT. 2009. CtrA response regulator binding to the Caulobacter chromosome replication origin is required during nutrient and antibiotic stress as well as during cell cycle progression. Mol. Microbiol. 72:139–54
    [Google Scholar]
  8. 8. 
    Bhagirath AY, Pydi SP, Li Y, Lin C, Kong W et al. 2017. Characterization of the direct interaction between hybrid sensor kinases PA1611 and RetS that controls biofilm formation and the type III secretion system in Pseudomonas aeruginosa. ACS Infect. Dis 3:162–75
    [Google Scholar]
  9. 9. 
    Bhuwan M, Lee HJ, Peng HL, Chang HY 2012. Histidine-containing phosphotransfer protein-B (HptB) regulates swarming motility through partner-switching system in Pseudomonas aeruginosa PAO1 strain. J. Biol. Chem. 287:1903–14
    [Google Scholar]
  10. 10. 
    Biondi EG, Reisinger SJ, Skerker JM, Arif M, Perchuk BS et al. 2006. Regulation of the bacterial cell cycle by an integrated genetic circuit. Nature 444:899
    [Google Scholar]
  11. 11. 
    Bordi C, Lamy MC, Ventre I, Termine E, Hachani A et al. 2010. Regulatory RNAs and the HptB/RetS signalling pathways fine-tune Pseudomonas aeruginosa pathogenesis. Mol. Microbiol. 76:1427–43
    [Google Scholar]
  12. 12. 
    Branda SS, González-Pastor JE, Ben-Yehuda S, Losick R, Kolter R 2001. Fruiting body formation by Bacillus subtilis. PNAS 98:11621–26
    [Google Scholar]
  13. 13. 
    Broder UN, Jaeger T, Jenal U 2016. LadS is a calcium-responsive kinase that induces acute-to-chronic virulence switch in Pseudomonas aeruginosa. Nat. Microbiol 2:16184
    [Google Scholar]
  14. 14. 
    Burkholder WF, Kurtser I, Grossman AD 2001. Replication initiation proteins regulate a developmental checkpoint in Bacillus subtilis. Cell 104:269–79
    [Google Scholar]
  15. 15. 
    Burrowes E, Baysse C, Adams C, O'Gara F 2006. Influence of the regulatory protein RsmA on cellular functions in Pseudomonas aeruginosa PAO1, as revealed by transcriptome analysis. Microbiology 152:405–18
    [Google Scholar]
  16. 16. 
    Cano DA, Domínguez-Bernal G, Tierrez A, Portillo FG-d, Casadesús J 2002. Regulation of capsule synthesis and cell motility in Salmonella enterica by the essential gene igaA. Genetics 162:1513–23
    [Google Scholar]
  17. 17. 
    Cao JG, Meighen EA. 1989. Purification and structural identification of an autoinducer for the luminescence system of Vibrio harveyi. J. Biol. Chem 264:21670–76
    [Google Scholar]
  18. 18. 
    Capra EJ, Perchuk BS, Skerker JM, Laub MT 2012. Adaptive mutations that prevent crosstalk enable the expansion of paralogous signaling protein families. Cell 150:222–32
    [Google Scholar]
  19. 19. 
    Chambonnier G, Roux L, Redelberger D, Fadel F, Filloux A et al. 2016. The hybrid histidine kinase LadS forms a multicomponent signal transduction system with the GacS/GacA two-component system in Pseudomonas aeruginosa. PLOS Genet 12:e1006032
    [Google Scholar]
  20. 20. 
    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 415:545
    [Google Scholar]
  21. 21. 
    Chen Y, Cao S, Chai Y, Clardy J, Kolter R et al. 2012. A Bacillus subtilis sensor kinase involved in triggering biofilm formation on the roots of tomato plants. Mol. Microbiol. 85:418–30
    [Google Scholar]
  22. 22. 
    Chen YE, Tsokos CG, Biondi EG, Perchuk BS, Laub MT 2009. Dynamics of two phosphorelays controlling cell cycle progression in Caulobacter crescentus. J. Bacteriol 191:7417–29
    [Google Scholar]
  23. 23. 
    Childers WS, Xu Q, Mann TH, Mathews II, Blair JA et al. 2014. Cell fate regulation governed by a repurposed bacterial histidine kinase. PLOS Biol 12:e1001979
    [Google Scholar]
  24. 24. 
    Cho K, Zusman DR. 1999. Sporulation timing in Myxococcus xanthus is controlled by the espAB locus. Mol. Microbiol. 34:714–25
    [Google Scholar]
  25. 25. 
    Cho S-H, Szewczyk J, Pesavento C, Zietek M, Banzhaf M et al. 2014. Detecting envelope stress by monitoring β-barrel assembly. Cell 159:1652–64
    [Google Scholar]
  26. 26. 
    Coggan KA, Wolfgang MC. 2012. Global regulatory pathways and cross-talk control Pseudomonas aeruginosa environmental lifestyle and virulence phenotype. Curr. Issues Mol. Biol. 14:47–69
    [Google Scholar]
  27. 27. 
    Costerton JW, Stewart PS, Greenberg EP 1999. Bacterial biofilms: a common cause of persistent infections. Science 284:1318–22
    [Google Scholar]
  28. 28. 
    Cunningham KA, Burkholder WF. 2009. The histidine kinase inhibitor Sda binds near the site of autophosphorylation and may sterically hinder autophosphorylation and phosphotransfer to Spo0F. Mol. Microbiol. 71:659–77
    [Google Scholar]
  29. 29. 
    Devi SN, Vishnoi M, Kiehler B, Haggett L, Fujita M 2015. In vivo functional characterization of the transmembrane histidine kinase KinC in Bacillus subtilis. Microbiology 161:1092–104
    [Google Scholar]
  30. 30. 
    Diaz AR, Core LJ, Jiang M, Morelli M, Chiang CH et al. 2012. Bacillus subtilis RapA phosphatase domain interaction with its substrate, phosphorylated Spo0F, and its inhibitor, the PhrA peptide. J. Bacteriol. 194:1378–88
    [Google Scholar]
  31. 31. 
    Dubey BN, Lori C, Ozaki S, Fucile G, Plaza-Menacho I et al. 2016. Cyclic di-GMP mediates a histidine kinase/phosphatase switch by noncovalent domain cross-linking. Sci. Adv. 2:e1600823
    [Google Scholar]
  32. 32. 
    Dutta R, Yoshida T, Inouye M 2000. The critical role of the conserved Thr247 residue in the functioning of the osmosensor EnvZ, a histidine kinase/phosphatase, in Escherichia coli. J. Biol. Chem 275:38645–53
    [Google Scholar]
  33. 33. 
    Eswaramoorthy P, Duan D, Dinh J, Dravis A, Devi SN, Fujita M 2010. The threshold level of the sensor histidine kinase KinA governs entry into sporulation in Bacillus subtilis. J. Bacteriol 192:3870–82
    [Google Scholar]
  34. 34. 
    Farris C, Sanowar S, Bader MW, Pfuetzner R, Miller SI 2010. Antimicrobial peptides activate the Rcs regulon through the outer membrane lipoprotein RcsF. J. Bacteriol. 192:4894–903
    [Google Scholar]
  35. 35. 
    Francis VI, Stevenson EC, Porter SL 2017. Two-component systems required for virulence in Pseudomonas aeruginosa. FEMS Microbiol. Lett 364:fnx104
    [Google Scholar]
  36. 36. 
    Francis VI, Waters EM, Finton-James SE, Gori A, Kadioglu A et al. 2018. Multiple communication mechanisms between sensor kinases are crucial for virulence in Pseudomonas aeruginosa. Nat. Commun 9:2219
    [Google Scholar]
  37. 37. 
    Freeman JA, Bassler BL. 1999. A genetic analysis of the function of LuxO, a two-component response regulator involved in quorum sensing in Vibrio harveyi. Mol. Microbiol 31:665–77
    [Google Scholar]
  38. 38. 
    Freeman JA, Bassler BL. 1999. Sequence and function of LuxU: a two-component phosphorelay protein that regulates quorum sensing in Vibrio harveyi. J. Bacteriol 181:899–906
    [Google Scholar]
  39. 39. 
    Fujita M, González-Pastor JE, Losick R 2005. High- and low-threshold genes in the Spo0A regulon of Bacillus subtilis. J. Bacteriol 187:1357–68
    [Google Scholar]
  40. 40. 
    Fujita M, Losick R. 2005. Evidence that entry into sporulation in Bacillus subtilis is governed by a gradual increase in the level and activity of the master regulator Spo0A. Genes Dev 19:2236–44
    [Google Scholar]
  41. 41. 
    Furukawa S, Kuchma SL, O'Toole GA 2006. Keeping their options open: acute versus persistent infections. J. Bacteriol. 188:1211–17
    [Google Scholar]
  42. 42. 
    Gervais FG, Drapeau GR. 1992. Identification, cloning, and characterization of rcsF, a new regulator gene for exopolysaccharide synthesis that suppresses the division mutation ftsZ84 in Escherichia coli K-12. J. Bacteriol. 174:8016–22
    [Google Scholar]
  43. 43. 
    Gooderham WJ, Hancock REW. 2009. Regulation of virulence and antibiotic resistance by two-component regulatory systems in Pseudomonas aeruginosa. FEMS Microbiol. Rev 33:279–94
    [Google Scholar]
  44. 44. 
    Goodman AL, Kulasekara B, Rietsch A, Boyd D, Smith RS, Lory S 2004. A signaling network reciprocally regulates genes associated with acute infection and chronic persistence in Pseudomonas aeruginosa. Dev. Cell 7:745–54
    [Google Scholar]
  45. 45. 
    Goodman AL, Merighi M, Hyodo M, Ventre I, Filloux A, Lory S 2009. Direct interaction between sensor kinase proteins mediates acute and chronic disease phenotypes in a bacterial pathogen. Genes Dev 23:249–59
    [Google Scholar]
  46. 46. 
    Grau RR, de Oña P, Kunert M, Leñini C, Gallegos-Monterrosa R et al. 2015. A duo of potassium-responsive histidine kinases govern the multicellular destiny of Bacillus subtilis. mBio 6:e00581
    [Google Scholar]
  47. 47. 
    Guo X-P, Sun Y-C. 2017. New insights into the non-orthodox two component Rcs phosphorelay system. Front. Microbiol. 8:2014
    [Google Scholar]
  48. 48. 
    Hammer BK, Bassler BL. 2003. Quorum sensing controls biofilm formation in Vibrio cholerae. Mol. Microbiol 50:101–4
    [Google Scholar]
  49. 49. 
    Heeb S, Blumer C, Haas D 2002. Regulatory RNA as mediator in GacA/RsmA-dependent global control of exoproduct formation in Pseudomonas fluorescens CHA0. J. Bacteriol. 184:1046–56
    [Google Scholar]
  50. 50. 
    Henke JM, Bassler BL. 2004. Quorum sensing regulates type III secretion in Vibrio harveyi and Vibrio parahaemolyticus. J. Bacteriol 186:3794–805
    [Google Scholar]
  51. 51. 
    Henke JM, Bassler BL. 2004. Three parallel quorum-sensing systems regulate gene expression in Vibrio harveyi. J. Bacteriol 186:6902–14
    [Google Scholar]
  52. 52. 
    Heurlier K, Williams F, Heeb S, Dormond C, Pessi G et al. 2004. Positive control of swarming, rhamnolipid synthesis, and lipase production by the posttranscriptional RsmA/RsmZ system in Pseudomonas aeruginosa PAO1. J. Bacteriol. 186:2936–45
    [Google Scholar]
  53. 53. 
    Higgs PI, Cho KY, Whitworth DE, Evans LS, Zusman DR 2005. Four unusual two-component signal transduction homologs, RedC to RedF, are necessary for timely development in Myxococcus xanthus. J. Bacteriol 187:8191–95
    [Google Scholar]
  54. 54. 
    Higgs PI, Jagadeesan S, Mann P, Zusman DR 2008. EspA, an orphan hybrid histidine protein kinase, regulates the timing of expression of key developmental proteins of Myxococcus xanthus. J. Bacteriol 190:4416–26
    [Google Scholar]
  55. 55. 
    Hoang Y, Kroos L. 2018. Ultrasensitive response of developing Myxococcus xanthus to the addition of nutrient medium correlates with the level of MrpC. J. Bacteriol. 200:e00456–18
    [Google Scholar]
  56. 56. 
    Hsu JL, Chen HC, Peng HL, Chang HY 2008. Characterization of the histidine-containing phosphotransfer protein B-mediated multistep phosphorelay system in Pseudomonas aeruginosa PAO1. J. Biol. Chem. 283:9933–44
    [Google Scholar]
  57. 57. 
    Hurley A, Bassler BL. 2017. Asymmetric regulation of quorum-sensing receptors drives autoinducer-specific gene expression programs in Vibrio cholerae. PLOS Genet 13:e1006826
    [Google Scholar]
  58. 58. 
    Hussein NA, Cho S-H, Laloux G, Siam R, Collet J-F 2018. Distinct domains of Escherichia coli IgaA connect envelope stress sensing and down-regulation of the Rcs phosphorelay across subcellular compartments. PLOS Genet 14:e1007398
    [Google Scholar]
  59. 59. 
    Huynh TN, Stewart V. 2011. Negative control in two-component signal transduction by transmitter phosphatase activity. Mol. Microbiol. 82:275–86
    [Google Scholar]
  60. 60. 
    Iniesta AA, Hillson NJ, Shapiro L 2010. Cell pole–specific activation of a critical bacterial cell cycle kinase. PNAS 107:7012–17
    [Google Scholar]
  61. 61. 
    Iniesta AA, McGrath PT, Reisenauer A, McAdams HH, Shapiro L 2006. A phospho-signaling pathway controls the localization and activity of a protease complex critical for bacterial cell cycle progression. PNAS 103:10935–40
    [Google Scholar]
  62. 62. 
    Jacobs C, Hung D, Shapiro L 2001. Dynamic localization of a cytoplasmic signal transduction response regulator controls morphogenesis during the Caulobacter cell cycle. PNAS 98:4095–100
    [Google Scholar]
  63. 63. 
    Jagadeesan S, Mann P, Schink CW, Higgs PI 2009. A novel “four-component” two-component signal transduction mechanism regulates developmental progression in Myxococcus xanthus. J. Biol. Chem 284:21435–45
    [Google Scholar]
  64. 64. 
    Jean-Pierre F, Tremblay J, Deziel E 2017. Broth versus surface-grown cells: differential regulation of RsmY/Z small RNAs in Pseudomonas aeruginosa by the Gac/HptB system. Front. Microbiol. 7:2168
    [Google Scholar]
  65. 65. 
    Jiang M, Shao W, Perego M, Hoch JA 2000. Multiple histidine kinases regulate entry into stationary phase and sporulation in Bacillus subtilis. Mol. Microbiol 38:535–42
    [Google Scholar]
  66. 66. 
    Jing X, Jaw J, Robinson HH, Schubot FD 2010. Crystal structure and oligomeric state of the RetS signaling kinase sensory domain. Proteins 78:1631–40
    [Google Scholar]
  67. 67. 
    Jung K, Fried L, Behr S, Heermann R 2012. Histidine kinases and response regulators in networks. Curr. Opin. Microbiol. 15:118–24
    [Google Scholar]
  68. 68. 
    Jung SA, Chapman CA, Ng W-L 2015. Quadruple quorum-sensing inputs control Vibrio cholerae virulence and maintain system robustness. PLOS Pathog 11:e1004837
    [Google Scholar]
  69. 69. 
    Kirkpatrick CL, Viollier PH. 2012. Decoding Caulobacter development. FEMS Microbiol. Rev. 36:193–205
    [Google Scholar]
  70. 70. 
    Kong W, Chen L, Zhao J, Shen T, Surette MG et al. 2013. Hybrid sensor kinase PA1611 in Pseudomonas aeruginosa regulates transitions between acute and chronic infection through direct interaction with RetS. Mol. Microbiol. 88:784–97
    [Google Scholar]
  71. 71. 
    Lapouge K, Schubert M, Allain FH, Haas D 2008. Gac/Rsm signal transduction pathway of γ-proteobacteria: from RNA recognition to regulation of social behaviour. Mol. Microbiol. 67:241–53
    [Google Scholar]
  72. 72. 
    Laskowski MA, Osborn E, Kazmierczak BI 2004. A novel sensor kinase–response regulator hybrid regulates type III secretion and is required for virulence in Pseudomonas aeruginosa. Mol. Microbiol 54:1090–103
    [Google Scholar]
  73. 73. 
    Laub MT, Chen SL, Shapiro L, McAdams HH 2002. Genes directly controlled by CtrA, a master regulator of the Caulobacter cell cycle. PNAS 99:4632–37
    [Google Scholar]
  74. 74. 
    Laub MT, Goulian M. 2007. Specificity in two-component signal transduction pathways. Annu. Rev. Genet. 41:121–45
    [Google Scholar]
  75. 75. 
    Laubacher ME, Ades SE. 2008. The Rcs phosphorelay is a cell envelope stress response activated by peptidoglycan stress and contributes to intrinsic antibiotic resistance. J. Bacteriol. 190:2065–74
    [Google Scholar]
  76. 76. 
    LeDeaux JR, Grossman AD. 1995. Isolation and characterization of kinC, a gene that encodes a sensor kinase homologous to the sporulation sensor kinases KinA and KinB in Bacillus subtilis. J. Bacteriol 177:166–75
    [Google Scholar]
  77. 77. 
    Lenz DH, Mok KC, Lilley BN, Kulkarni RV, Wingreen NS, Bassler BL 2004. The small RNA chaperone Hfq and multiple small RNAs control quorum sensing in Vibrio harveyi and Vibrio cholerae. Cell 118:69–82
    [Google Scholar]
  78. 78. 
    LeRoux M, Kirkpatrick RL, Montauti EI, Tran BQ, Peterson SB et al. 2015. Kin cell lysis is a danger signal that activates antibacterial pathways of Pseudomonas aeruginosa. eLife 4:e05701
    [Google Scholar]
  79. 79. 
    Lilley BN, Bassler BL. 2000. Regulation of quorum sensing in Vibrio harveyi by LuxO and Sigma-54. Mol. Microbiol. 36:940–54
    [Google Scholar]
  80. 80. 
    Lin CT, Huang YJ, Chu PH, Hsu JL, Huang CH, Peng HL 2006. Identification of an HptB-mediated multi-step phosphorelay in Pseudomonas aeruginosa PAO1. Res. Microbiol. 157:169–75
    [Google Scholar]
  81. 81. 
    López D, Fischbach MA, Chu F, Losick R, Kolter R 2009. Structurally diverse natural products that cause potassium leakage trigger multicellularity in Bacillus subtilis. PNAS 106:280–85
    [Google Scholar]
  82. 82. 
    Lorenz N, Shin JY, Jung K 2017. Activity, abundance, and localization of quorum sensing receptors in Vibrio harveyi. Front. Microbiol 8:634
    [Google Scholar]
  83. 83. 
    Lori C, Ozaki S, Steiner S, Böhm R, Abel S et al. 2015. Cyclic di-GMP acts as a cell cycle oscillator to drive chromosome replication. Nature 523:236
    [Google Scholar]
  84. 84. 
    Majdalani N, Gottesman S. 2005. The Rcs phosphorelay: a complex signal transduction system. Annu. Rev. Microbiol. 59:379–405
    [Google Scholar]
  85. 85. 
    Mann TH, Seth Childers W, Blair JA, Eckart MR, Shapiro L 2016. A cell cycle kinase with tandem sensory PAS domains integrates cell fate cues. Nat. Commun. 7:11454
    [Google Scholar]
  86. 86. 
    Mann TH, Shapiro L. 2018. Integration of cell cycle signals by multi-PAS domain kinases. PNAS 115:E7166–73
    [Google Scholar]
  87. 87. 
    Matroule J-Y, Lam H, Burnette DT, Jacobs-Wagner C 2004. Cytokinesis monitoring during development: rapid pole-to-pole shuttling of a signaling protein by localized kinase and phosphatase in Caulobacter. Cell 118:579–90
    [Google Scholar]
  88. 88. 
    McLoon AL, Kolodkin-Gal I, Rubinstein SM, Kolter R, Losick R 2011. Spatial regulation of histidine kinases governing biofilm formation in Bacillus subtilis. J. Bacteriol 193:679–85
    [Google Scholar]
  89. 89. 
    Meissner A, Wild V, Simm R, Rohde M, Erck C et al. 2007. Pseudomonas aeruginosa cupA-encoded fimbriae expression is regulated by a GGDEF and EAL domain-dependent modulation of the intracellular level of cyclic diguanylate. Environ. Microbiol. 9:2475–85
    [Google Scholar]
  90. 90. 
    Mike LA, Choby JE, Brinkman PR, Olive LQ, Dutter BF et al. 2014. Two-component system cross-regulation integrates Bacillus anthracis response to heme and cell envelope stress. PLOS Pathog 10:e1004044
    [Google Scholar]
  91. 91. 
    Mikkelsen H, Ball G, Giraud C, Filloux A 2009. Expression of Pseudomonas aeruginosa CupD fimbrial genes is antagonistically controlled by RcsB and the EAL-containing PvrR response regulators. PLOS ONE 4:e6018
    [Google Scholar]
  92. 92. 
    Mikkelsen H, Hui K, Barraud N, Filloux A 2013. The pathogenicity island encoded PvrSR/RcsCB regulatory network controls biofilm formation and dispersal in Pseudomonas aeruginosa PA14. Mol. Microbiol. 89:450–63
    [Google Scholar]
  93. 93. 
    Molle V, Fujita M, Jensen ST, Eichenberger P, González-Pastor JE et al. 2003. The Spo0A regulon of Bacillus subtilis. Mol. Microbiol 50:1683–701
    [Google Scholar]
  94. 94. 
    Neiditch MB, Federle MJ, Miller ST, Bassler BL, Hughson FM 2005. Regulation of LuxPQ receptor activity by the quorum-sensing signal autoinducer-2. Mol. Cell 18:507–18
    [Google Scholar]
  95. 95. 
    Neiditch MB, Federle MJ, Pompeani AJ, Kelly RC, Swem DL et al. 2006. Ligand-induced asymmetry in histidine sensor kinase complex regulates quorum sensing. Cell 126:1095–108
    [Google Scholar]
  96. 96. 
    Ng W-L, Bassler BL. 2009. Bacterial quorum-sensing network architectures. Annu. Rev. Genet. 43:197–222
    [Google Scholar]
  97. 97. 
    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. 79:1407–17
    [Google Scholar]
  98. 98. 
    Nicastro GG, Boechat AL, Abe CM, Kaihami GH, Baldini RL 2009. Pseudomonas aeruginosa PA14 cupD transcription is activated by the RcsB response regulator, but repressed by its putative cognate sensor RcsC. FEMS Microbiol. Lett. 301:115–23
    [Google Scholar]
  99. 99. 
    Noriega CE, Lin H-Y, Chen L-L, Williams SB, Stewart V 2010. Asymmetric cross-regulation between the nitrate-responsive NarX–NarL and NarQ–NarP two-component regulatory systems from Escherichia coli K-12. Mol. Microbiol. 75:394–412
    [Google Scholar]
  100. 100. 
    Ohlsen KL, Grimsley JK, Hoch JA 1994. Deactivation of the sporulation transcription factor Spo0A by the Spo0E protein phosphatase. PNAS 91:1756–60
    [Google Scholar]
  101. 101. 
    Parashar V, Mirouze N, Dubnau DA, Neiditch MB 2011. Structural basis of response regulator dephosphorylation by Rap phosphatases. PLOS Biol 9:e1000589
    [Google Scholar]
  102. 102. 
    Paul R, Abel S, Wassmann P, Beck A, Heerklotz H, Jenal U 2007. Activation of the diguanylate cyclase PleD by phosphorylation-mediated dimerization. J. Biol. Chem. 282:29170–77
    [Google Scholar]
  103. 103. 
    Paul R, Jaeger T, Abel S, Wiederkehr I, Folcher M et al. 2008. Allosteric regulation of histidine kinases by their cognate response regulator determines cell fate. Cell 133:452–61
    [Google Scholar]
  104. 104. 
    Perego M. 2001. A new family of aspartyl phosphate phosphatases targeting the sporulation transcription factor Spo0A of Bacillus subtilis. Mol. Microbiol 42:133–43
    [Google Scholar]
  105. 105. 
    Perego M, Brannigan JA. 2001. Pentapeptide regulation of aspartyl-phosphate phosphatases. Peptides 22:1541–47
    [Google Scholar]
  106. 106. 
    Perego M, Cole SP, Burbulys D, Trach K, Hoch JA 1989. Characterization of the gene for a protein kinase which phosphorylates the sporulation-regulatory proteins Spo0A and Spo0F of Bacillus subtilis. J. Bacteriol 171:6187–96
    [Google Scholar]
  107. 107. 
    Perego M, Hanstein C, Welsh KM, Djavakhishvili T, Glaser P, Hoch JA 1994. Multiple protein-aspartate phosphatases provide a mechanism for the integration of diverse signals in the control of development in B. subtilis. Cell 79:1047–55
    [Google Scholar]
  108. 108. 
    de las Mercedes Pescaretti M, Farizano JV, Morero R, Delgado MA 2013. A novel insight on signal transduction mechanism of RcsCDB system in Salmonella enterica serovar Typhimurium. PLOS ONE 8:e72527
    [Google Scholar]
  109. 109. 
    Pessi G, Williams F, Hindle Z, Heurlier K, Holden MTG et al. 2001. The global posttranscriptional regulator RsmA modulates production of virulence determinants and N-acylhomoserine lactones in Pseudomonas aeruginosa. J. Bacteriol 183:6676–83
    [Google Scholar]
  110. 110. 
    Petrova OE, Gupta K, Liao J, Goodwine JS, Sauer K 2017. Divide and conquer: The Pseudomonas aeruginosa two-component hybrid SagS enables biofilm formation and recalcitrance of biofilm cells to antimicrobial agents via distinct regulatory circuits. Environ. Microbiol. 19:2005–24
    [Google Scholar]
  111. 111. 
    Petrova OE, Sauer K. 2010. The novel two-component regulatory system BfiSR regulates biofilm development by controlling the small RNA rsmZ through CafA. J. Bacteriol. 192:5275–88
    [Google Scholar]
  112. 112. 
    Petrova OE, Sauer K. 2011. SagS contributes to the motile-sessile switch and acts in concert with BfiSR to enable Pseudomonas aeruginosa biofilm formation. J. Bacteriol. 193:6614–28
    [Google Scholar]
  113. 113. 
    Plener L, Lorenz N, Reiger M, Ramalho T, Gerland U, Jung K 2015. The phosphorylation flow of the Vibrio harveyi quorum-sensing cascade determines levels of phenotypic heterogeneity in the population. J. Bacteriol. 197:1747–56
    [Google Scholar]
  114. 114. 
    Podgornaia AI, Laub MT. 2013. Determinants of specificity in two-component signal transduction. Curr. Opin. Microbiol. 16:156–62
    [Google Scholar]
  115. 115. 
    Quisel JD, Burkholder WF, Grossman AD 2001. In vivo effects of sporulation kinases on mutant Spo0A proteins in Bacillus subtilis. J. Bacteriol 183:6573–78
    [Google Scholar]
  116. 116. 
    Quon KC, Marczynski GT, Shapiro L 1996. Cell cycle control by an essential bacterial two-component signal transduction protein. Cell 84:83–93
    [Google Scholar]
  117. 117. 
    Quon KC, Yang B, Domian IJ, Shapiro L, Marczynski GT 1998. Negative control of bacterial DNA replication by a cell cycle regulatory protein that binds at the chromosome origin. PNAS 95:120–25
    [Google Scholar]
  118. 118. 
    Rabin RS, Stewart V. 1992. Either of two functionally redundant sensor proteins, NarX and NarQ, is sufficient for nitrate regulation in Escherichia coli K-12. PNAS 89:8419–23
    [Google Scholar]
  119. 119. 
    Rabin RS, Stewart V. 1993. Dual response regulators (NarL and NarP) interact with dual sensors (NarX and NarQ) to control nitrate- and nitrite-regulated gene expression in Escherichia coli K-12. J. Bacteriol. 175:3259–68
    [Google Scholar]
  120. 120. 
    Raghavan V, Groisman EA. 2010. Orphan and hybrid two-component system proteins in health and disease. Curr. Opin. Microbiol. 13:226–31
    [Google Scholar]
  121. 121. 
    Reisinger SJ, Huntwork S, Viollier PH, Ryan KR 2007. DivL performs critical cell cycle functions in Caulobacter crescentus independent of kinase activity. J. Bacteriol. 189:8308–20
    [Google Scholar]
  122. 122. 
    Robinson M, Son B, Kroos D, Kroos L 2014. Transcription factor MrpC binds to promoter regions of hundreds of developmentally-regulated genes in Myxococcus xanthus. BMC Genom 15:1123
    [Google Scholar]
  123. 123. 
    Rowland SL, Burkholder WF, Cunningham KA, Maciejewski MW, Grossman AD, King GF 2004. Structure and mechanism of action of Sda, an inhibitor of the histidine kinases that regulate initiation of sporulation in Bacillus subtilis. Mol. Cell 13:689–701
    [Google Scholar]
  124. 124. 
    Ruvolo MV, Mach KE, Burkholder WF 2006. Proteolysis of the replication checkpoint protein Sda is necessary for the efficient initiation of sporulation after transient replication stress in Bacillus subtilis. Mol. Microbiol 60:1490–508
    [Google Scholar]
  125. 125. 
    Schramm A, Lee B, Higgs PI 2012. Intra- and inter-protein phosphorylation between two hybrid histidine kinases controls Myxococcus xanthus developmental progression. J. Biol. Chem. 287:25060–72
    [Google Scholar]
  126. 126. 
    Silversmith RE. 2010. Auxiliary phosphatases in two-component signal transduction. Curr. Opin. Microbiol. 13:177–83
    [Google Scholar]
  127. 127. 
    Siryaporn A, Goulian M. 2010. Characterizing cross-talk in vivo: avoiding pitfalls and overinterpretation. Methods Enzymol 471:1–16
    [Google Scholar]
  128. 128. 
    Skerker JM, Perchuk BS, Siryaporn A, Lubin EA, Ashenberg O et al. 2008. Rewiring the specificity of two-component signal transduction systems. Cell 133:1043–54
    [Google Scholar]
  129. 129. 
    Skerker JM, Prasol MS, Perchuk BS, Biondi EG, Laub MT 2005. Two-component signal transduction pathways regulating growth and cell cycle progression in a bacterium: a system-level analysis. PLOS Biol 3:e334
    [Google Scholar]
  130. 130. 
    Smits WK, Bongiorni C, Veening J-W, Hamoen LW, Kuipers OP, Perego M 2007. Temporal separation of distinct differentiation pathways by a dual specificity Rap-Phr system in Bacillus subtilis. Mol. Microbiol 65:103–20
    [Google Scholar]
  131. 131. 
    Stein EA, Cho K, Higgs PI, Zusman DR 2006. Two Ser/Thr protein kinases essential for efficient aggregation and spore morphogenesis in Myxococcus xanthus. Mol. Microbiol 60:1414–31
    [Google Scholar]
  132. 132. 
    Stewart V, Bledsoe PJ. 2003. Synthetic lac operator substitutions for studying the nitrate- and nitrite-responsive NarX-NarL and NarQ-NarP two-component regulatory systems of Escherichia coli K-12. J. Bacteriol. 185:2104–11
    [Google Scholar]
  133. 133. 
    Stock AM, Robinson VL, Goudreau PN 2000. Two-component signal transduction. Annu. Rev. Biochem. 69:183–215
    [Google Scholar]
  134. 134. 
    Swartzman E, Silverman M, Meighen EA 1992. The luxR gene product of Vibrio harveyi is a transcriptional activator of the lux promoter. J. Bacteriol. 174:7490–93
    [Google Scholar]
  135. 135. 
    Takeda S-i, Fujisawa Y, Matsubara M, Aiba H, Mizuno T 2001. A novel feature of the multistep phosphorelay in Escherichia coli: a revised model of the RcsC → YojN → RcsB signalling pathway implicated in capsular synthesis and swarming behaviour. Mol. Microbiol. 40:440–50
    [Google Scholar]
  136. 136. 
    Timmen M, Bassler BL, Jung K 2006. AI-1 influences the kinase activity but not the phosphatase activity of LuxN of Vibrio harveyi. J. Biol. Chem 281:24398–404
    [Google Scholar]
  137. 137. 
    Trach KA, Hoch JA. 1993. Multisensory activation of the phosphorelay initiating sporulation in Bacillus subtilis—identification and sequence of the protein-kinase of the alternate pathway. Mol. Microbiol. 8:69–79
    [Google Scholar]
  138. 138. 
    Tsokos CG, Perchuk BS, Laub MT 2011. A dynamic complex of signaling proteins uses polar localization to regulate cell-fate asymmetry in Caulobacter crescentus. Dev. Cell 20:329–41
    [Google Scholar]
  139. 139. 
    Tu KC, Bassler BL. 2007. Multiple small RNAs act additively to integrate sensory information and control quorum sensing in Vibrio harveyi. Genes Dev 21:221–33
    [Google Scholar]
  140. 140. 
    Ueki T, Inouye S. 2003. Identification of an activator protein required for the induction of fruA, a gene essential for fruiting body development in Myxococcus xanthus. PNAS 100:8782–87
    [Google Scholar]
  141. 141. 
    Utsumi R. 2017. Bacterial signal transduction networks via connectors and development of the inhibitors as alternative antibiotics. Biosci. Biotechnol. Biochem. 81:1663–69
    [Google Scholar]
  142. 142. 
    Valentini M, Gonzalez D, Mavridou DAI, Filloux A 2018. Lifestyle transitions and adaptive pathogenesis of Pseudomonas aeruginosa. Curr. Opin. Microbiol 41:15–20
    [Google Scholar]
  143. 143. 
    Valentini M, Laventie B-J, Moscoso J, Jenal U, Filloux A 2016. The diguanylate cyclase HsbD intersects with the HptB regulatory cascade to control Pseudomonas aeruginosa biofilm and motility. PLOS Genet 12:e1006354
    [Google Scholar]
  144. 144. 
    Ventre I, Goodman AL, Vallet-Gely I, Vasseur P, Soscia C et al. 2006. Multiple sensors control reciprocal expression of Pseudomonas aeruginosa regulatory RNA and virulence genes. PNAS 103:171–76
    [Google Scholar]
  145. 145. 
    Wall E, Majdalani N, Gottesman S 2018. The complex Rcs regulatory cascade. Annu. Rev. Microbiol. 72:111–39
    [Google Scholar]
  146. 146. 
    Wang L, Grau R, Perego M, Hoch JA 1997. A novel histidine kinase inhibitor regulating development in Bacillussubtilis. Genes Dev 11:2569–79
    [Google Scholar]
  147. 147. 
    Waters CM, Bassler BL. 2006. The Vibrio harveyi quorum-sensing system uses shared regulatory components to discriminate between multiple autoinducers. Genes Dev 20:2754–67
    [Google Scholar]
  148. 148. 
    Wehland M, Bernhard F. 2000. The RcsAB box: characterization of a new operator essential for the regulation of exopolysaccharide biosynthesis in enteric bacteria. J. Biol. Chem. 275:7013–20
    [Google Scholar]
  149. 149. 
    Wehland M, Kiecker C, Coplin DL, Kelm O, Saenger W, Bernhard F 1999. Identification of an RcsA/RcsB recognition motif in the promoters of exopolysaccharide biosynthetic operons from Erwinia amylovora and Pantoea stewartii subspecies stewartii. J. Biol. Chem 274:3300–7
    [Google Scholar]
  150. 150. 
    Wheeler RT, Shapiro L. 1999. Differential localization of two histidine kinases controlling bacterial cell differentiation. Mol. Cell 4:683–94
    [Google Scholar]
  151. 151. 
    Whitworth DE, Millard A, Hodgson DA, Hawkins PF 2008. Protein-protein interactions between two-component system transmitter and receiver domains of Myxococcus xanthus. Proteomics 8:1839–42
    [Google Scholar]
  152. 152. 
    Willett JW, Tiwari N, Müller S, Hummels KR, Houtman JCD et al. 2013. Specificity residues determine binding affinity for two-component signal transduction systems. mBio 4:e00420–13
    [Google Scholar]
  153. 153. 
    Wojnowska M, Yan J, Sivalingam GN, Cryar A, Gor J et al. 2013. Autophosphorylation activity of a soluble hexameric histidine kinase correlates with the shift in protein conformational equilibrium. Chem. Biol. 20:1411–20
    [Google Scholar]
  154. 154. 
    Workentine ML, Chang L, Ceri H, Turner RJ 2009. The GacS-GacA two-component regulatory system of Pseudomonas fluorescens: a bacterial two-hybrid analysis. FEMS Microbiol. Lett. 292:50–56
    [Google Scholar]
  155. 155. 
    Wu R, Gu M, Wilton R, Babnigg G, Kim Y et al. 2013. Insight into the sporulation phosphorelay: crystal structure of the sensor domain of Bacillus subtilis histidine kinase, KinD. Protein Sci 22:564–76
    [Google Scholar]
  156. 156. 
    Wuichet K, Cantwell BJ, Zhulin IB 2010. Evolution and phyletic distribution of two-component signal transduction systems. Curr. Opin. Microbiol. 13:219–25
    [Google Scholar]
  157. 157. 
    Xavier KB, Bassler BL. 2003. LuxS quorum sensing: more than just a numbers game. Curr. Opin. Microbiol. 6:191–97
    [Google Scholar]
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