1932

Abstract

The ChvG-ChvI two-component system is conserved among multiple . ChvG is a canonical two-component system sensor kinase with a single large periplasmic loop. Active ChvG directs phosphotransfer to its cognate response regulator ChvI, which controls transcription of target genes. In many alphaproteobacteria, ChvG is regulated by a third component, a periplasmic protein called ExoR, that maintains ChvG in an inactive state through direct interaction. Acidic pH stimulates proteolysis of ExoR, unfettering ChvG-ChvI to control its regulatory targets. Activated ChvI among different alphaproteobacteria controls a broad range of cellular processes, including symbiosis and virulence, exopolysaccharide production, biofilm formation, motility, type VI secretion, cellular metabolism, envelope composition, and growth. Low pH is a virulence signal in , but in other systems, conditions that cause envelope stress may also generally activate ChvG-ChvI. There is mounting evidence that these regulators influence diverse aspects of bacterial physiology, including but not limited to host interactions.

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2023-09-15
2024-06-24
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Literature Cited

  1. 1.
    Alakavuklar MA, Heckel BC, Stoner AM, Stembel JA, Fuqua C. 2021. Motility control through an anti-activation mechanism in Agrobacterium tumefaciens. Mol. Microbiol. 116:1281–97
    [Google Scholar]
  2. 2.
    Belanger L, Charles TC. 2013. Members of the Sinorhizobium meliloti ChvI regulon identified by a DNA binding screen. BMC Microbiol. 13:132
    [Google Scholar]
  3. 3.
    Belanger L, Dimmick KA, Fleming JS, Charles TC. 2009. Null mutations in Sinorhizobium meliloti exoS and chvI demonstrate the importance of this two-component regulatory system for symbiosis. Mol. Microbiol. 74:1223–37
    [Google Scholar]
  4. 4.
    Boel G, Mijakovic I, Maze A, Poncet S, Taha MK et al. 2003. Transcription regulators potentially controlled by HPr kinase/phosphorylase in Gram-negative bacteria. J. Mol. Microbiol. Biotechnol. 5:206–15
    [Google Scholar]
  5. 5.
    Bondarev V, Richter M, Romano S, Piel J, Schwedt A, Schulz-Vogt HN. 2013. The genus Pseudovibrio contains metabolically versatile bacteria adapted for symbiosis. Environ. Microbiol. 15:2095–113
    [Google Scholar]
  6. 6.
    Campbell GR, Sharypova LA, Scheidle H, Jones KM, Niehaus K et al. 2003. Striking complexity of lipopolysaccharide defects in a collection of Sinorhizobium meliloti mutants. J. Bacteriol. 185:3853–62
    [Google Scholar]
  7. 7.
    Cangelosi GA, Best EA, Martinetti G, Nester EW. 1991. Genetic analysis of Agrobacterium. Methods Enzymol. 204:384–97
    [Google Scholar]
  8. 8.
    Charles TC, Nester EW. 1993. A chromosomally encoded two-component sensory transduction system is required for virulence of Agrobacterium tumefaciens. J. Bacteriol. 175:6614–25
    [Google Scholar]
  9. 9.
    Chen EJ, Fisher RF, Perovich VM, Sabio EA, Long SR. 2009. Identification of direct transcriptional target genes of ExoS/ChvI two-component signaling in Sinorhizobium meliloti. J. Bacteriol. 191:6833–42
    [Google Scholar]
  10. 10.
    Chen EJ, Sabio EA, Long SR. 2008. The periplasmic regulator ExoR inhibits ExoS/ChvI two-component signalling in Sinorhizobium meliloti. Mol. Microbiol. 69:1290–303
    [Google Scholar]
  11. 11.
    Cheng HP, Walker GC. 1998. Succinoglycan production by Rhizobium meliloti is regulated through the ExoS-ChvI two-component regulatory system. J. Bacteriol. 180:20–26
    [Google Scholar]
  12. 12.
    Deutscher J, Ake FM, Derkaoui M, Zebre AC, Cao TN et al. 2014. The bacterial phosphoenolpyruvate:carbohydrate phosphotransferase system: regulation by protein phosphorylation and phosphorylation-dependent protein-protein interactions. Microbiol. Mol. Biol. Rev. 78:231–56
    [Google Scholar]
  13. 13.
    Doherty D, Leigh JA, Glazebrook J, Walker GC. 1988. Rhizobium meliloti mutants that overproduce the R. meliloti acidic calcofluor-binding exopolysaccharide. J. Bacteriol. 170:4249–56
    [Google Scholar]
  14. 14.
    Foreman DL, Vanderlinde EM, Bay DC, Yost CK. 2010. Characterization of a gene family of outer membrane proteins (ropB) in Rhizobium leguminosarum bv. viciae VF39SM and the role of the sensor kinase ChvG in their regulation. J. Bacteriol. 192:975–83
    [Google Scholar]
  15. 15.
    Frohlich KS, Forstner KU, Gitai Z. 2018. Post-transcriptional gene regulation by an Hfq-independent small RNA in Caulobacter crescentus. Nucleic Acids Res. 46:10969–82
    [Google Scholar]
  16. 16.
    Fujishige NA, Kapadia NN, Hirsch AM. 2006. A feeling for the micro-organism: structure on a small scale; biofilms on plant roots. Bot. J. Linnean Soc. 150:79–88
    [Google Scholar]
  17. 17.
    Geiger O, Sohlenkamp C, Vera-Cruz D, Medeot DB, Martinez-Aguilar L et al. 2021. ExoS/ChvI two-component signal-transduction system activated in the absence of bacterial phosphatidylcholine. Front. Plant Sci. 12:678976
    [Google Scholar]
  18. 18.
    Godessart P, Lannoy A, Dieu M, Van der Verren SE, Soumillion P et al. 2021. Beta-barrels covalently link peptidoglycan and the outer membrane in the alpha-proteobacterium Brucella abortus. Nat. Microbiol. 6:27–33
    [Google Scholar]
  19. 19.
    Guzman-Verri C, Manterola L, Sola-Landa A, Parra A, Cloeckaert A et al. 2002. The two-component system BvrR/BvrS essential for Brucella abortus virulence regulates the expression of outer membrane proteins with counterparts in members of the Rhizobiaceae. PNAS 99:12375–80
    [Google Scholar]
  20. 20.
    Heavner ME, Qiu WG, Cheng HP. 2015. Phylogenetic co-occurrence of ExoR, ExoS, and ChvI, components of the RSI bacterial invasion switch, suggests a key adaptive mechanism regulating the transition between free-living and host-invading phases in Rhizobiales. PLOS ONE 10:e0135655
    [Google Scholar]
  21. 21.
    Heckel BC, Tomlinson AD, Morton ER, Choi JH, Fuqua C. 2014. Agrobacterium tumefaciens exoR controls acid response genes and impacts exopolysaccharide synthesis, horizontal gene transfer, and virulence gene expression. J. Bacteriol. 196:3221–33
    [Google Scholar]
  22. 22.
    Hellweg C, Puhler A, Weidner S. 2009. The time course of the transcriptomic response of Sinorhizobium meliloti 1021 following a shift to acidic pH. BMC Microbiol. 9:37
    [Google Scholar]
  23. 23.
    Hoch JA, Silhavy TJ, eds. 1995. Two-Component Signal Transduction Washington, DC: ASM
    [Google Scholar]
  24. 24.
    Keating DH. 2007. The Sinorhizobium meliloti ExoR protein is required for the downregulation of lpsS transcription and succinoglycan biosynthesis in response to divalent cations. FEMS Microbiol. Lett. 267:23–29
    [Google Scholar]
  25. 25.
    Keating DH. 2007. Sinorhizobium meliloti SyrA mediates the transcriptional regulation of genes involved in lipopolysaccharide sulfation and exopolysaccharide biosynthesis. J. Bacteriol. 189:2510–20
    [Google Scholar]
  26. 26.
    Kolmar H, Waller PR, Sauer RT. 1996. The DegP and DegQ periplasmic endoproteases of Escherichia coli: specificity for cleavage sites and substrate conformation. J. Bacteriol. 178:5925–29
    [Google Scholar]
  27. 27.
    Li L, Jia Y, Hou Q, Charles TC, Nester EW, Pan SQ. 2002. A global pH sensor: Agrobacterium sensor protein ChvG regulates acid-inducible genes on its two chromosomes and Ti plasmid. PNAS 99:12369–74
    [Google Scholar]
  28. 28.
    Liu P, Wood D, Nester EW. 2005. Phosphoenolpyruvate carboxykinase is an acid-induced, chromosomally encoded virulence factor in Agrobacterium tumefaciens. J. Bacteriol. 187:6039–45
    [Google Scholar]
  29. 29.
    Lu HY, Luo L, Yang MH, Cheng HP. 2012. Sinorhizobium meliloti ExoR is the target of periplasmic proteolysis. J. Bacteriol. 194:4029–40
    [Google Scholar]
  30. 30.
    Ma LS, Hachani A, Lin JS, Filloux A, Lai EM. 2014. Agrobacterium tumefaciens deploys a superfamily of type VI secretion DNase effectors as weapons for interbacterial competition in planta. Cell Host Microbe 16:94–104
    [Google Scholar]
  31. 31.
    Manterola L, Moriyon I, Moreno E, Sola-Landa A, Weiss DS et al. 2005. The lipopolysaccharide of Brucella abortus BvrS/BvrR mutants contains lipid A modifications and has higher affinity for bactericidal cationic peptides. J. Bacteriol. 187:5631–39
    [Google Scholar]
  32. 32.
    Mantis NJ, Winans SC. 1992. The Agrobacterium tumefaciens vir gene transcriptional activator virG is transcriptionally induced by acid pH and other stress stimuli. J. Bacteriol. 174:1189–96
    [Google Scholar]
  33. 33.
    Mantis NJ, Winans SC. 1993. The chromosomal response regulatory gene chvI of Agrobacterium tumefaciens complements an Escherichia coli phoB mutation and is required for virulence. J. Bacteriol. 175:6626–36
    [Google Scholar]
  34. 34.
    Mittl PR, Schneider-Brachert W. 2007. Sel1-like repeat proteins in signal transduction. Cell Signal 19:20–31
    [Google Scholar]
  35. 35.
    Okamura H, Hanaoka S, Nagadoi A, Makino K, Nishimura Y. 2000. Structural comparison of the PhoB and OmpR DNA-binding/transactivation domains and the arrangement of PhoB molecules on the phosphate box. J. Mol. Biol. 295:1225–36
    [Google Scholar]
  36. 36.
    Onyeziri MC, Hardy GG, Natarajan R, Xu J, Reynolds IP et al. 2022. Dual adhesive unipolar polysaccharides synthesized by overlapping biosynthetic pathways in Agrobacterium tumefaciens. Mol. Microbiol. 117:1023–47
    [Google Scholar]
  37. 37.
    Osteras M, Stanley J, Finan TM. 1995. Identification of Rhizobium-specific intergenic mosaic elements within an essential two-component regulatory system of Rhizobium species. J. Bacteriol. 177:5485–94
    [Google Scholar]
  38. 38.
    Parkinson JS, Kofoid EC. 1992. Communication modules in bacterial signaling proteins. Annu. Rev. Genet. 26:71–112
    [Google Scholar]
  39. 39.
    Petersen TN, Brunak S, von Heijne G, Nielsen H. 2011. SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat. Methods 8:785–86
    [Google Scholar]
  40. 40.
    Pinedo CA, Gage DJ. 2009. HPrK regulates succinate-mediated catabolite repression in the gram-negative symbiont Sinorhizobium meliloti. J. Bacteriol. 191:298–309
    [Google Scholar]
  41. 41.
    Pukatzki S, McAuley SB, Miyata ST. 2009. The type VI secretion system: translocation of effectors and effector-domains. Curr. Opin. Microbiol. 12:11–17
    [Google Scholar]
  42. 42.
    Quebatte M, Dehio M, Tropel D, Basler A, Toller I et al. 2010. The BatR/BatS two-component regulatory system controls the adaptive response of Bartonella henselae during human endothelial cell infection. J. Bacteriol. 192:3352–67
    [Google Scholar]
  43. 43.
    Ratib NR, Sabio EY, Mendoza C, Barnett MJ, Clover SB et al. 2018. Genome-wide identification of genes directly regulated by ChvI and a consensus sequence for ChvI binding in Sinorhizobium meliloti. Mol. Microbiol. 110:596–615
    [Google Scholar]
  44. 44.
    Rotter C, Muhlbacher S, Salamon D, Schmitt R, Scharf B. 2006. Rem, a new transcriptional activator of motility and chemotaxis in Sinorhizobium meliloti. J. Bacteriol. 188:6932–42
    [Google Scholar]
  45. 45.
    Russell AB, Hood RD, Bui NK, LeRoux M, Vollmer W, Mougous JD. 2011. Type VI secretion delivers bacteriolytic effectors to target cells. Nature 475:343–47
    [Google Scholar]
  46. 46.
    Saenz HL, Engel P, Stoeckli MC, Lanz C, Raddatz G et al. 2007. Genomic analysis of Bartonella identifies type IV secretion systems as host adaptability factors. Nat. Genet. 39:1469–76
    [Google Scholar]
  47. 47.
    Sandoz KM, Moore RA, Beare PA, Patel AV, Smith RE et al. 2021. Beta-barrel proteins tether the outer membrane in many Gram-negative bacteria. Nat. Microbiol. 6:19–26
    [Google Scholar]
  48. 48.
    Schaper S, Wendt H, Bamberger J, Sieber V, Schmid J, Becker A. 2019. A bifunctional UDP-sugar 4-epimerase supports biosynthesis of multiple cell surface polysaccharides in Sinorhizobium meliloti. J. Bacteriol. 201:e00801–18
    [Google Scholar]
  49. 49.
    Sola-Landa A, Pizarro-Cerda J, Grillo MJ, Moreno E, Moriyon I et al. 1998. A two-component regulatory system playing a critical role in plant pathogens and endosymbionts is present in Brucella abortus and controls cell invasion and virulence. Mol. Microbiol. 29:125–38
    [Google Scholar]
  50. 50.
    Sourjik V, Muschler P, Scharf B, Schmitt R. 2000. VisN and VisR are global regulators of chemotaxis, flagellar, and motility genes in Sinorhizobium (Rhizobium) meliloti. J. Bacteriol. 182:782–88
    [Google Scholar]
  51. 51.
    Stein BJ, Fiebig A, Crosson S. 2021. The ChvG-ChvI and NtrY-NtrX two-component systems coordinately regulate growth of Caulobacter crescentus. J. Bacteriol. 203:e0019921
    [Google Scholar]
  52. 52.
    Stonestrom A, Barabote RD, Gonzalez CF, Saier MH Jr. 2005. Bioinformatic analyses of bacterial HPr kinase/phosphorylase homologues. Res. Microbiol. 156:443–51
    [Google Scholar]
  53. 53.
    Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S. 2011. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 28:2731–39
    [Google Scholar]
  54. 54.
    Tomlinson AD, Ramey-Hartung B, Day TW, Merritt PM, Fuqua C. 2010. Agrobacterium tumefaciens ExoR represses succinoglycan biosynthesis and is required for biofilm formation and motility. Microbiology 156:2670–81
    [Google Scholar]
  55. 55.
    Vanderlinde EM, Yost CK. 2012. Mutation of the sensor kinase chvG in Rhizobium leguminosarum negatively impacts cellular metabolism, outer membrane stability, and symbiosis. J. Bacteriol. 194:768–77
    [Google Scholar]
  56. 56.
    Viadas C, Rodriguez MC, Sangari FJ, Gorvel JP, Garcia-Lobo JM, Lopez-Goni I. 2010. Transcriptome analysis of the Brucella abortus BvrR/BvrS two-component regulatory system. PLOS ONE 5:e10216
    [Google Scholar]
  57. 57.
    Wang C, Kemp J, Da Fonseca IO, Equi RC, Sheng X et al. 2010. Sinorhizobium meliloti 1021 loss-of-function deletion mutation in chvI and its phenotypic characteristics. Mol. Plant Microbe Interact. 23:153–60
    [Google Scholar]
  58. 58.
    Wells DH, Chen EJ, Fisher RF, Long SR. 2007. ExoR is genetically coupled to the ExoS-ChvI two-component system and located in the periplasm of Sinorhizobium meliloti. Mol. Microbiol. 64:647–64
    [Google Scholar]
  59. 59.
    Wiech EM, Cheng HP, Singh SM. 2015. Molecular modeling and computational analyses suggests that the Sinorhizobium meliloti periplasmic regulator protein ExoR adopts a superhelical fold and is controlled by a unique mechanism of proteolysis. Protein Sci. 24:319–27
    [Google Scholar]
  60. 60.
    Williams MA, Aliashkevich A, Krol E, Kuru E, Bouchier JM et al. 2021. Unipolar peptidoglycan synthesis in the Rhizobiales requires an essential class A penicillin-binding protein. mBio 12:e0234621
    [Google Scholar]
  61. 61.
    Williams MA, Bouchier JM, Mason AK, Brown PJB. 2022. Activation of ChvG-ChvI regulon by cell wall stress confers resistance to β-lactam antibiotics and initiates surface spreading in Agrobacterium tumefaciens. PLOS Genet. 18:12e1010274
    [Google Scholar]
  62. 62.
    Winans SC. 1990. Transcriptional induction of an Agrobacterium regulatory gene at tandem promoters by plant-released phenolic compounds, phosphate starvation, and acidic growth media. J. Bacteriol. 172:2433–38
    [Google Scholar]
  63. 63.
    Winans SC. 1992. Two-way chemical signaling in Agrobacterium-plant interactions. Microbiol. Rev. 56:12–31
    [Google Scholar]
  64. 64.
    Wu CF, Lin JS, Shaw GC, Lai EM. 2012. Acid-induced type VI secretion system is regulated by ExoR-ChvG/ChvI signaling cascade in Agrobacterium tumefaciens. PLOS Pathog. 8:e1002938
    [Google Scholar]
  65. 65.
    Yao SY, Luo L, Har KJ, Becker A, Ruberg S et al. 2004. Sinorhizobium meliloti ExoR and ExoS proteins regulate both succinoglycan and flagellum production. J. Bacteriol. 186:6042–49
    [Google Scholar]
  66. 66.
    Yuan ZC, Liu P, Saenkham P, Kerr K, Nester EW. 2008. Transcriptome profiling and functional analysis of Agrobacterium tumefaciens reveals a general conserved response to acidic conditions (pH 5.5) and a complex acid-mediated signaling involved in Agrobacterium-plant interactions. J. Bacteriol. 190:494–507
    [Google Scholar]
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