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Volume 169, Issue 6

Evolution of cyclic di-GMP signalling on a short and long term time scale Open Access

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Graphical Abstract

 Graphical Abstract 

 

Abstract

Diversifying radiation of domain families within specific lineages of life indicates the importance of their functionality for the organisms. The foundation for the diversifying radiation of the cyclic di-GMP signalling network that occurred within the bacterial kingdom is most likely based in the outmost adaptability, flexibility and plasticity of the system. Integrative sensing of multiple diverse extra- and intracellular signals is made possible by the N-terminal sensory domains of the modular cyclic di-GMP turnover proteins, mutations in the protein scaffolds and subsequent signal reception by diverse receptors, which eventually rewires opposite host-associated as well as environmental life styles including parallel regulated target outputs. Natural, laboratory and microcosm derived microbial variants often with an altered multicellular biofilm behaviour as reading output demonstrated single amino acid substitutions to substantially alter catalytic activity including substrate specificity. Truncations and domain swapping of cyclic di-GMP signalling genes and horizontal gene transfer suggest rewiring of the network. Presence of cyclic di-GMP signalling genes on horizontally transferable elements in particular observed in extreme acidophilic bacteria indicates that cyclic di-GMP signalling and biofilm components are under selective pressure in these types of environments. On a short and long term evolutionary scale, within a species and in families within bacterial orders, respectively, the cyclic di-GMP signalling network can also rapidly disappear. To investigate variability of the cyclic di-GMP signalling system on various levels will give clues about evolutionary forces and discover novel physiological and metabolic pathways affected by this intriguing second messenger signalling system.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): biofilm , cyclic dinucleotides , EAL , evolution , GGDEF and HD-GYP
Funding
This study was supported by the:
  • Chinese Scholarship Council CSC
    • Principle Award Recipient: Lian-YingCao
  • Swedish Research Council for Natural and Engineering Sciences (Award 2022-04865)
    • Principle Award Recipient: UteRomling
© 2023 The Authors
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License. This article was made open access via a Publish and Read agreement between the Microbiology Society and the corresponding author’s institution.
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2023-06-29
2024-12-08
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References

  1. Chou S-H, Guiliani N, Lee VT, Römling U. Microbial Cyclic Di-Nucleotide Signaling Cham: Springer; 2020 [View Article]
     [Google Scholar]
  2. Yang F, Qian S, Tian F, Chen H, Hutchins W et al. The GGDEF-domain protein GdpX1 attenuates motility, exopolysaccharide production and virulence in Xanthomonas oryzae pv. oryzae. J Appl Microbiol 2016; 120:1646–1657 [View Article] [PubMed]
     [Google Scholar]
  3. Kakkar A, Verma RK, Samal B, Chatterjee S. Interplay between the cyclic di-GMP network and the cell-cell signalling components coordinates virulence-associated functions in Xanthomonas oryzae pv. oryzae. Environ Microbiol 2021; 23:5433–5462 [View Article] [PubMed]
     [Google Scholar]
  4. Cohen D, Melamed S, Millman A, Shulman G, Oppenheimer-Shaanan Y et al. Cyclic GMP–AMP signalling protects bacteria against viral infection. Nature 2019; 574:691–695 [View Article]
     [Google Scholar]
  5. Whiteley AT, Eaglesham JB, de Oliveira Mann CC, Morehouse BR, Lowey B et al. Bacterial cGAS-like enzymes synthesize diverse nucleotide signals. Nature 2019; 567:194–199 [View Article] [PubMed]
     [Google Scholar]
  6. Nelson JW, Breaker RR. The lost language of the RNA World. Sci Signal 2017; 10:483 [View Article]
     [Google Scholar]
  7. Galperin MY, Nikolskaya AN, Koonin EV. Novel domains of the prokaryotic two-component signal transduction systems. FEMS Microbiol Lett 2001; 203:11–21 [View Article] [PubMed]
     [Google Scholar]
  8. Römling U, Galperin MY, Gomelsky M. Cyclic di-GMP: the first 25 years of a universal bacterial second messenger. Microbiol Mol Biol Rev 2013; 77:1–52 [View Article] [PubMed]
     [Google Scholar]
  9. Xu Z, Zhang H, Zhang X, Jiang H, Liu C et al. Interplay between the bacterial protein deacetylase CobB and the second messenger c‐di‐ GMP. The EMBO Journal 2019; 38:18 [View Article]
     [Google Scholar]
  10. Collins AJ, Smith TJ, Sondermann H, O’Toole GA. From input to output: the Lap/c-di-GMP biofilm regulatory circuit. Annu Rev Microbiol 2020; 74:607–631 [View Article]
     [Google Scholar]
  11. Andrade MO, Alegria MC, Guzzo CR, Docena C, Rosa MCP et al. The HD-GYP domain of RpfG mediates a direct linkage between the Rpf quorum-sensing pathway and a subset of diguanylate cyclase proteins in the phytopathogen Xanthomonas axonopodis pv citri. Mol Microbiol 2006; 62:537–551 [View Article] [PubMed]
     [Google Scholar]
  12. Schirmer T, Jenal U. Structural and mechanistic determinants of c-di-GMP signalling. Nat Rev Microbiol 2009; 7:724–735 [View Article] [PubMed]
     [Google Scholar]
  13. Ximinies AD, Dou Y, Mishra A, Zhang K, Deivanayagam C et al. The oxidative stress-induced hypothetical protein PG_0686 in Porphyromonas gingivalis W83 is a novel diguanylate cyclase. Microbiol Spectr 2023; 11:e0441122 [View Article] [PubMed]
     [Google Scholar]
  14. Moradali MF, Ghods S, Bähre H, Lamont RJ, Scott DA et al. Atypical cyclic di-AMP signaling is essential for Porphyromonas gingivalis growth and regulation of cell envelope homeostasis and virulence. NPJ Biofilms Microbiomes 2022; 8:53 [View Article] [PubMed]
     [Google Scholar]
  15. Wang Y-C, Chin K-H, Tu Z-L, He J, Jones CJ et al. Nucleotide binding by the widespread high-affinity cyclic di-GMP receptor MshEN domain. Nat Commun 2016; 7:12481 [View Article] [PubMed]
     [Google Scholar]
  16. Sudarsan N, Lee ER, Weinberg Z, Moy RH, Kim JN et al. Riboswitches in eubacteria sense the second messenger cyclic di-GMP. Science 2008; 321:411–413 [View Article] [PubMed]
     [Google Scholar]
  17. Römling U. Is biofilm formation intrinsic to the origin of life?. Environ Microbiol 2023; 25:26–39 [View Article] [PubMed]
     [Google Scholar]
  18. Piazza A, Parra L, Ciancio Casalini L, Sisti F, Fernández J et al. Cyclic di-GMP signaling links biofilm formation and Mn(II) oxidation in Pseudomonas resinovorans. mBio 2022; 13:e0273422 [View Article] [PubMed]
     [Google Scholar]
  19. Kumar NG, Nieto V, Kroken AR, Jedel E, Grosser MR et al. Pseudomonas aeruginosa can diversify after host cell invasion to establish multiple intracellular niches. mBio 2022; 13: [View Article]
     [Google Scholar]
  20. Elgamoudi BA, Starr KS, Korolik V. Extracellular c-di-GMP plays a role in biofilm formation and dispersion of Campylobacter jejuni. Microorganisms 2022; 10:2030 [View Article] [PubMed]
     [Google Scholar]
  21. Zlatkov N, Näsman MEC, Uhlin BE. Metabolic and morphotypic trade-offs within the eco-evolutionary dynamics of Escherichia coli. Microbiol Spectr 2022; 10:e0067822 [View Article] [PubMed]
     [Google Scholar]
  22. Rice EW, Johnson CJ, Clark RM, Fox KR, Reasoner DJ et al. Chlorine and survival of “rugose” Vibrio cholerae. Lancet 1992; 340:740 [View Article] [PubMed]
     [Google Scholar]
  23. Römling U, Sierralta WD, Eriksson K, Normark S. Multicellular and aggregative behaviour of Salmonella typhimurium strains is controlled by mutations in the agfD promoter. Mol Microbiol 1998; 28:249–264 [View Article] [PubMed]
     [Google Scholar]
  24. Branda SS, González-Pastor JE, Ben-Yehuda S, Losick R, Kolter R. Fruiting body formation by Bacillus subtilis. Proc Natl Acad Sci U S A 2001; 98:11621–11626 [View Article] [PubMed]
     [Google Scholar]
  25. Rainey PB, Travisano M. Adaptive radiation in a heterogeneous environment. Nature 1998; 394:69–72 [View Article]
     [Google Scholar]
  26. Friedman L, Kolter R. Genes involved in matrix formation in Pseudomonas aeruginosa PA14 biofilms. Mol Microbiol 2004; 51:675–690 [View Article] [PubMed]
     [Google Scholar]
  27. White PB. The rugose variant of vibrios. J Pathol 1938; 46:1–6 [View Article]
     [Google Scholar]
  28. Prasad M, Obana N, Sakai K, Nagakubo T, Miyazaki S et al. Point mutations lead to increased levels of c-di-GMP and phenotypic changes to the colony biofilm morphology in Alcanivorax borkumensis SK2. Microbes Environ 2019; 34:104–107 [View Article] [PubMed]
     [Google Scholar]
  29. Beyhan S, Yildiz FH. Smooth to rugose phase variation in Vibrio cholerae can be mediated by a single nucleotide change that targets c-di-GMP signalling pathway. Mol Microbiol 2007; 63:995–1007 [View Article] [PubMed]
     [Google Scholar]
  30. Cao L-Y, Yang Y-F, Zhang X, Chen Y-H, Yao J-W et al. Deciphering molecular mechanism underlying self-flocculation of Zymomonas mobilis for robust production. Appl Environ Microbiol 2022; 88:e0239821 [View Article] [PubMed]
     [Google Scholar]
  31. Van Puyvelde S, Pickard D, Vandelannoote K, Heinz E, Barbé B et al. An African Salmonella Typhimurium ST313 sublineage with extensive drug-resistance and signatures of host adaptation. Nat Commun 2019; 10: [View Article]
     [Google Scholar]
  32. MacKenzie KD, Wang Y, Musicha P, Hansen EG, Palmer MB et al. Parallel evolution leading to impaired biofilm formation in invasive Salmonella strains. PLoS Genet 2019; 15:e1008233 [View Article]
     [Google Scholar]
  33. Singletary LA, Karlinsey JE, Libby SJ, Mooney JP, Lokken KL et al. Loss of multicellular behavior in epidemic African nontyphoidal Salmonella enterica serovar Typhimurium ST313 strain D23580. mBio 2016; 7: [View Article]
     [Google Scholar]
  34. Gerstel U, Römling U. Oxygen tension and nutrient starvation are major signals that regulate agfD promoter activity and expression of the multicellular morphotype in Salmonella typhimurium. Environ Microbiol 2001; 3:638–648 [View Article] [PubMed]
     [Google Scholar]
  35. White AP, Gibson DL, Kim W, Kay WW, Surette MG. Thin aggregative fimbriae and cellulose enhance long-term survival and persistence of Salmonella. J Bacteriol 2006; 188:3219–3227 [View Article]
     [Google Scholar]
  36. Uhlich GA, Keen JE, Elder RO. Variations in the csgD promoter of Escherichia coli O157:H7 associated with increased virulence in mice and increased invasion of HEp-2 cells. Infect Immun 2002; 70:395–399 [View Article] [PubMed]
     [Google Scholar]
  37. Cimdins A, Simm R, Li F, Lüthje P, Thorell K et al. Alterations of c-di-GMP turnover proteins modulate semi-constitutive rdar biofilm formation in commensal and uropathogenic Escherichia coli. Microbiologyopen 2017; 6:e00508 [View Article] [PubMed]
     [Google Scholar]
  38. Reyes Ruiz LM, King KA, Agosto-Burgos C, Gamez IS, Gadda NC et al. Coordinated modulation of multiple processes through phase variation of a c-di-GMP phosphodiesterase in Clostridioides difficile. PLoS Pathog 2022; 18:e1010677 [View Article] [PubMed]
     [Google Scholar]
  39. Dhungel BA, Govind R. Phase-variable expression of pdcB, a phosphodiesterase, influences sporulation in Clostridioides difficile. Mol Microbiol 2021; 116:1347–1360 [View Article] [PubMed]
     [Google Scholar]
  40. Pérez-Mendoza D, Coulthurst SJ, Humphris S, Campbell E, Welch M et al. A multi-repeat adhesin of the phytopathogen, Pectobacterium atrosepticum, is secreted by A Type I pathway and is subject to complex regulation involving a non-canonical diguanylate cyclase. Mol Microbiol 2011; 82:719–733 [View Article] [PubMed]
     [Google Scholar]
  41. Hallberg ZF, Wang XC, Wright TA, Nan B, Ad O et al. Hybrid promiscuous (Hypr) GGDEF enzymes produce cyclic AMP-GMP (3′, 3′-cGAMP). Proc Natl Acad Sci 2016; 113:1790–1795 [View Article]
     [Google Scholar]
  42. Lowry RC, Hallberg ZF, Till R, Simons TJ, Nottingham R et al. Production of 3’,3’-cGAMP by a Bdellovibrio bacteriovorus promiscuous GGDEF enzyme, Bd0367, regulates exit from prey by gliding motility. PLoS Genet 2022; 18:e1010164 [View Article] [PubMed]
     [Google Scholar]
  43. Bobrov AG, Kirillina O, Ryjenkov DA, Waters CM, Price PA et al. Systematic analysis of cyclic di-GMP signalling enzymes and their role in biofilm formation and virulence in Yersinia pestis. Mol Microbiol 2011; 79:533–551 [View Article] [PubMed]
     [Google Scholar]
  44. Sun YC, Jarrett CO, Bosio CF, Hinnebusch BJ. Retracing the evolutionary path that led to flea-borne transmission of Yersinia pestis. Cell Host & Microbe 2014; 15:578–586 [View Article]
     [Google Scholar]
  45. Simm R, Morr M, Kader A, Nimtz M, Römling U. GGDEF and EAL domains inversely regulate cyclic di-GMP levels and transition from sessility to motility. Mol Microbiol 2004; 53:1123–1134 [View Article] [PubMed]
     [Google Scholar]
  46. Paul K, Nieto V, Carlquist WC, Blair DF, Harshey RM. The c-di-GMP binding protein YcgR controls flagellar motor direction and speed to affect chemotaxis by a “backstop brake” mechanism. Mol Cell 2010; 38:128–139 [View Article] [PubMed]
     [Google Scholar]
  47. Simm R, Remminghorst U, Ahmad I, Zakikhany K, Römling U. A role for the EAL-like protein STM1344 in regulation of CsgD expression and motility in Salmonella enterica serovar Typhimurium. J Bacteriol 2009; 191:3928–3937 [View Article] [PubMed]
     [Google Scholar]
  48. Ahmad I, Wigren E, Le Guyon S, Vekkeli S, Blanka A et al. The EAL-like protein STM1697 regulates virulence phenotypes, motility and biofilm formation in Salmonella typhimurium. Mol Microbiol 2013; 90:1216–1232 [View Article] [PubMed]
     [Google Scholar]
  49. Zhang F, Li B, Dong H, Chen M, Yao S et al. YdiV regulates Escherichia coli ferric uptake by manipulating the DNA-binding ability of Fur in a SlyD-dependent manner. Nucleic Acids Res 2020; 48:9571–9588 [View Article] [PubMed]
     [Google Scholar]
  50. El Mouali Y, Kim H, Ahmad I, Brauner A, Liu Y et al. Stand-alone EAL domain proteins form a distinct subclass of EAL proteins involved in regulation of cell motility and biofilm formation in enterobacteria. J Bacteriol 2017; 199:18 [View Article] [PubMed]
     [Google Scholar]
  51. Römling U, Liang ZX, Dow JM. Progress in understanding the molecular basis underlying functional diversification of cyclic dinucleotide turnover proteins. J Bacteriol 2017; 199:e00790-16 [View Article] [PubMed]
     [Google Scholar]
  52. Hisert KB, MacCoss M, Shiloh MU, Darwin KH, Singh S et al. A glutamate-alanine-leucine (EAL) domain protein of Salmonella controls bacterial survival in mice, antioxidant defence and killing of macrophages: role of cyclic diGMP. Mol Microbiol 2005; 56:1234–1245 [View Article] [PubMed]
     [Google Scholar]
  53. Yue Y, Wang W, Ma Y, Song N, Jia H et al. Cooperative regulation of flagellar synthesis by two EAL-like proteins upon Salmonella entry into host cells. Microbiol Spectr 2023; 11:e0285922 [View Article] [PubMed]
     [Google Scholar]
  54. Tal R, Wong HC, Calhoon R, Gelfand D, Fear AL et al. Three cdg operons control cellular turnover of cyclic di-GMP in Acetobacter xylinum: genetic organization and occurrence of conserved domains in isoenzymes. J Bacteriol 1998; 180:4416–4425 [View Article] [PubMed]
     [Google Scholar]
  55. Rao F, Qi Y, Chong HS, Kotaka M, Li B et al. The functional role of a conserved loop in EAL domain-based cyclic di-GMP-specific phosphodiesterase. J Bacteriol 2009; 191:4722–4731 [View Article] [PubMed]
     [Google Scholar]
  56. Holland LM, O’Donnell ST, Ryjenkov DA, Gomelsky L, Slater SR et al. A Staphylococcal GGDEF domain protein regulates biofilm formation independently of cyclic dimeric GMP. J Bacteriol 2008; 190:5178–5189 [View Article]
     [Google Scholar]
  57. Christen M, Christen B, Folcher M, Schauerte A, Jenal U. Identification and characterization of a cyclic di-GMP-specific phosphodiesterase and its allosteric control by GTP. J Biol Chem 2005; 280:30829–30837 [View Article] [PubMed]
     [Google Scholar]
  58. Kazmierczak BI, Lebron MB, Murray TS. Analysis of FimX, a phosphodiesterase that governs twitching motility in Pseudomonas aeruginosa. Mol Microbiol 2006; 60:1026–1043 [View Article] [PubMed]
     [Google Scholar]
  59. Rao F, See RY, Zhang D, Toh DC, Ji Q et al. YybT is a signaling protein that contains a cyclic dinucleotide phosphodiesterase domain and a GGDEF domain with ATPase activity. J Biol Chem 2010; 285:473–482 [View Article] [PubMed]
     [Google Scholar]
  60. Zlatkov N, Uhlin BE. Absence of global stress regulation in Escherichia coli promotes pathoadaptation and novel c-di-GMP-dependent metabolic capability. Sci Rep 2019; 9:2600 [View Article] [PubMed]
     [Google Scholar]
  61. Li F, Lüthje P, Shafeeq S, Ahl M, Trcek J et al. Evolution towards small colony variants of pandemic multidrug resistant ST131 Escherichia coli isolates from a 10-year bone infection. bioRxiv 2022 [View Article]
     [Google Scholar]
  62. Herbst S, Lorkowski M, Sarenko O, Nguyen TKL, Jaenicke T et al. Transmembrane redox control and proteolysis of PdeC, a novel type of c‐di‐ GMP phosphodiesterase. The EMBO Journal 2018; 37: [View Article]
     [Google Scholar]
  63. Spurbeck RR, Tarrien RJ, Mobley HLT, Miller JF. Enzymatically active and inactive phosphodiesterases and diguanylate cyclases are involved in regulation of motility or sessility in Escherichia coli CFT073. mBio 2012; 3:e00307-12 [View Article] [PubMed]
     [Google Scholar]
  64. Farr AD, Remigi P, Rainey PB. Adaptive evolution by spontaneous domain fusion and protein relocalization. Nat Ecol Evol 2017; 1:1562–1568 [View Article] [PubMed]
     [Google Scholar]
  65. Römling U. Is biofilm formation intrinsic to the origin of life?. Environ Microbiol 2023; 25:26–39 [View Article] [PubMed]
     [Google Scholar]
  66. Liu Y, Lee C, Li F, Trcek J, Bähre H et al. A cyclic Di-GMP network is present in gram-positive Streptococcus and gram-negative Proteus species. ACS Infect Dis 2020; 6:2672–2687 [View Article]
     [Google Scholar]
  67. Martín-Rodríguez AJ, Higdon SM, Thorell K, Tellgren-Roth C, Sjöling Å et al. Comparative genomics of cyclic di-GMP metabolism and chemosensory pathways in Shewanella algae strains: novel bacterial sensory domains and functional insights into lifestyle regulation. mSystems 2022; 7:e0151821 [View Article] [PubMed]
     [Google Scholar]
  68. Ojha R, Dittmar AA, Severin GB, Koestler BJ. Shigella flexneri diguanylate cyclases regulate virulence. J Bacteriol 2021; 203:e0024221 [View Article] [PubMed]
     [Google Scholar]
  69. Chanin RB, Nickerson KP, Llanos-Chea A, Sistrunk JR. Shigella flexneri adherence factor expression in in vivo-like conditions. mSphere 2019; 4:
     [Google Scholar]
  70. Doore SM, Subramanian S, Tefft NM, Morona R, TerAvest MA et al. Large metabolic rewiring from small genomic changes between strains of Shigella flexneri. J Bacteriol 2021; 203:11 [View Article] [PubMed]
     [Google Scholar]
  71. Lindenberg S, Klauck G, Pesavento C, Klauck E, Hengge R. The EAL domain protein YciR acts as a trigger enzyme in a c-di-GMP signalling cascade in E. coli biofilm control. EMBO J 2013; 32:2001–2014 [View Article] [PubMed]
     [Google Scholar]
  72. Abel S, Bucher T, Nicollier M, Hug I, Kaever V et al. Bi-modal distribution of the second messenger c-di-GMP controls cell fate and asymmetry during the caulobacter cell cycle. PLoS Genet 2013; 9:e1003744 [View Article]
     [Google Scholar]
  73. Lai TH, Kumagai Y, Hyodo M, Hayakawa Y, Rikihisa Y. The Anaplasma phagocytophilum PleC histidine kinase and PleD diguanylate cyclase two-component system and role of cyclic Di-GMP in host cell infection. J Bacteriol 2009; 191:693–700 [View Article] [PubMed]
     [Google Scholar]
  74. Römling U. Cyclic Di-GMP (c-Di-GMP) goes into host cells—c-Di-GMP signaling in the obligate intracellular pathogen Anaplasma phagocytophilum. J Bacteriol 2009; 191:683–686 [View Article]
     [Google Scholar]
  75. Blötz C, Treffon K, Kaever V, Schwede F, Hammer E et al. Identification of the components involved in cyclic Di-AMP signaling in Mycoplasma pneumoniae. Front Microbiol 2017; 8:1328 [View Article] [PubMed]
     [Google Scholar]
  76. Barker JR, Koestler BJ, Carpenter VK, Burdette DL, Waters CM et al. STING-dependent recognition of cyclic di-AMP mediates type I interferon responses during Chlamydia trachomatis infection. mBio 2013; 4:e00018–00013 [View Article]
     [Google Scholar]
  77. Heermann R, Fuchs TM. Comparative analysis of the Photorhabdus luminescens and the Yersinia enterocolitica genomes: uncovering candidate genes involved in insect pathogenicity. BMC Genomics 2008; 9:40 [View Article]
     [Google Scholar]
  78. Brown NL, Misra TK, Winnie JN, Schmidt A, Seiff M et al. The nucleotide sequence of the mercuric resistance operons of plasmid R100 and transposon Tn501: further evidence for mer genes which enhance the activity of the mercuric ion detoxification system. Mol Gen Genet 1986; 202:143–151 [View Article]
     [Google Scholar]
  79. Hyde DR, Tu CP. tnpM: a novel regulatory gene that enhances Tn21 transposition and suppresses cointegrate resolution. Cell 1985; 42:629–638 [View Article] [PubMed]
     [Google Scholar]
  80. Bordeleau E, Brouillette E, Robichaud N, Burrus V. Beyond antibiotic resistance: integrating conjugative elements of the SXT/R391 family that encode novel diguanylate cyclases participate to c-di-GMP signalling in Vibrio cholerae. Environ Microbiol 2010; 12:510–523 [View Article] [PubMed]
     [Google Scholar]
  81. Madsen JS, Hylling O, Jacquiod S, Pécastaings S, Hansen LH et al. An intriguing relationship between the cyclic diguanylate signaling system and horizontal gene transfer. ISME J 2018; 12:2330–2334 [View Article] [PubMed]
     [Google Scholar]
  82. Richter AM, Povolotsky TL, Wieler LH, Hengge R. Cyclic-di-GMP signalling and biofilm-related properties of the Shiga toxin-producing 2011 German outbreak Escherichia coli O104:H4. EMBO Mol Med 2014; 6:1622–1637 [View Article] [PubMed]
     [Google Scholar]
  83. Mikkelsen H, Ball G, Giraud C, Filloux A. Expression of Pseudomonas aeruginosa CupD fimbrial genes is antagonistically controlled by RcsB and the EAL-containing PvrR response regulators. PLoS One 2009; 4:e6018 [View Article] [PubMed]
     [Google Scholar]
  84. Parreira VR, Ojha S, Lepp D, Mehdizadeh Gohari I, Zhou H et al. Necrotic enteritis locus 1 diguanylate cyclase and phosphodiesterase (cyclic-di-GMP) gene mutation attenuates virulence in an avian necrotic enteritis isolate of Clostridium perfringens. Vet Microbiol 2017; 208:69–73 [View Article] [PubMed]
     [Google Scholar]
  85. Kamal SM, Simpson DJ, Wang Z, Gänzle M, Römling U. Horizontal transmission of stress resistance genes shape the ecology of beta- and gamma-proteobacteria. Front Microbiol 2021; 12:696522 [View Article] [PubMed]
     [Google Scholar]
  86. Almblad H, Randall TE, Liu F, Leblanc K, Groves RA et al. Bacterial cyclic diguanylate signaling networks sense temperature. Nat Commun 2021; 12: [View Article]
     [Google Scholar]
  87. Nguyen SV, Harhay GP, Bono JL, Smith TPL, Harhay DM. Genome sequence of the thermotolerant foodborne pathogen Salmonella enterica serovar senftenberg ATCC 43845 and phylogenetic analysis of loci encoding increased protein quality control mechanisms. mSystems 2017; 2:e00190-16 [View Article] [PubMed]
     [Google Scholar]
  88. Castro M, Diaz M, Moya-Beltran A, Guiliani N. Cyclic di-GMP signaling in extreme acidophilic bacteria. In Chou S-H, Guiliani N, Lee VT, Römling U. eds Microbial Cyclic Di-Nucleotide Signaling Cham, Switzerland: Springer; 2020 [View Article]
     [Google Scholar]
  89. Moya-Beltrán A, Rojas-Villalobos C, Díaz M, Guiliani N, Quatrini R et al. Nucleotide second messenger-based signaling in extreme acidophiles of the Acidithiobacillus species complex: partition between the core and variable gene complements. Front Microbiol 2019; 10:381 [View Article]
     [Google Scholar]
  90. An S, Caly DL, McCarthy Y, Murdoch SL, Ward J et al. Novel cyclic di-GMP effectors of the YajQ protein family control bacterial virulence. PLoS Pathog 2014; 10:e1004429 [View Article]
     [Google Scholar]
  91. Ryjenkov DA, Simm R, Römling U, Gomelsky M. The PilZ domain is a receptor for the second messenger c-di-GMP: the PilZ domain protein YcgR controls motility in enterobacteria. J Biol Chem 2006; 281:30310–30314 [View Article] [PubMed]
     [Google Scholar]
  92. Amikam D, Galperin MY. PilZ domain is part of the bacterial c-di-GMP binding protein. Bioinformatics 2006; 22:3–6 [View Article] [PubMed]
     [Google Scholar]
  93. Benach J, Swaminathan SS, Tamayo R, Handelman SK, Folta-Stogniew E et al. The structural basis of cyclic diguanylate signal transduction by PilZ domains. EMBO J 2007; 26:5153–5166 [View Article] [PubMed]
     [Google Scholar]
  94. Guzzo CR, Dunger G, Salinas RK, Farah CS. Structure of the PilZ-FimXEAL-c-di-GMP complex responsible for the regulation of bacterial type IV pilus biogenesis. J Mol Biol 2013; 425:2174–2197 [View Article] [PubMed]
     [Google Scholar]
  95. Ryan RP, McCarthy Y, Kiely PA, O’Connor R, Farah CS et al. Dynamic complex formation between HD-GYP, GGDEF and PilZ domain proteins regulates motility in Xanthomonas campestris. Mol Microbiol 2012; 86:557–567 [View Article] [PubMed]
     [Google Scholar]
  96. Van Gundy T, Patel D, Bowler BE, Rothfuss MT, Hall AJ et al. c-di-GMP regulates activity of the PlzA RNA chaperone from the Lyme disease spirochete. Mol Microbiol 2023; 119:711–727 [View Article] [PubMed]
     [Google Scholar]
  97. Grassmann AA, Tokarz R, Golino C, McLain MA, Groshong AM et al. BosR and PlzA reciprocally regulate RpoS function to sustain Borrelia burgdorferi in ticks and mammals. J Clin Invest 2023; 133: [View Article]
     [Google Scholar]
  98. Galperin MY, Chou S-H. Structural Conservation and Diversity of PilZ-Related Domains. J Bacteriol 2020; 202:e00664-19 [View Article] [PubMed]
     [Google Scholar]
  99. Römling U. Cyclic di-GMP, an established secondary messenger still speeding up. Environ Microbiol 2012; 14:1817–1829 [View Article]
     [Google Scholar]
  100. Chou S-H, Galperin MY. Diversity of cyclic Di-GMP-binding proteins and mechanisms. J Bacteriol 2016; 198:32–46 [View Article]
     [Google Scholar]
  101. Christen B, Christen M, Paul R, Schmid F, Folcher M et al. Allosteric control of cyclic di-GMP signaling. J Biol Chem 2006; 281:32015–32024 [View Article] [PubMed]
     [Google Scholar]
  102. Duerig A, Abel S, Folcher M, Nicollier M, Schwede T et al. Second messenger-mediated spatiotemporal control of protein degradation regulates bacterial cell cycle progression. Genes Dev 2009; 23:93–104 [View Article] [PubMed]
     [Google Scholar]
  103. Smith SC, Joshi KK, Zik JJ, Trinh K, Kamajaya A et al. Cell cycle-dependent adaptor complex for ClpXP-mediated proteolysis directly integrates phosphorylation and second messenger signals. Proc Natl Acad Sci USA 2014; 111:14229–14234 [View Article]
     [Google Scholar]
  104. Lee VT, Matewish JM, Kessler JL, Hyodo M, Hayakawa Y et al. A cyclic-di-GMP receptor required for bacterial exopolysaccharide production. Mol Microbiol 2007; 65:1474–1484 [View Article]
     [Google Scholar]
  105. Fineran PC, Williamson NR, Lilley KS, Salmond GPC. Virulence and prodigiosin antibiotic biosynthesis in Serratia are regulated pleiotropically by the GGDEF/EAL domain protein, PigX. J Bacteriol 2007; 189:7653–7662 [View Article] [PubMed]
     [Google Scholar]
  106. Kharadi RR, Sundin GW. CsrD regulates amylovoran biosynthesis and virulence in Erwinia amylovora in a novel cyclic-di-GMP dependent manner. Mol Plant Pathol 2022; 23:1154–1169 [View Article] [PubMed]
     [Google Scholar]
  107. Potts AH, Leng Y, Babitzke P, Romeo T. Examination of Csr regulatory circuitry using epistasis analysis with RNA-seq (Epi-seq) confirms that CsrD affects gene expression via CsrA, CsrB and CsrC. Sci Rep 2018; 8:5373 [View Article] [PubMed]
     [Google Scholar]
  108. Llontop EE, Cenens W, Favaro DC, Sgro GG, Salinas RK et al. The PilB-PilZ-FimX regulatory complex of the Type IV pilus from Xanthomonas citri. PLoS Pathog 2021; 17:e1009808 [View Article]
     [Google Scholar]
  109. Wei C, Wang S, Liu P, Cheng S-T, Qian G et al. The PdeK-PdeR two-component system promotes unipolar localization of FimX and pilus extension in Xanthomonas oryzae pv. oryzicola. Sci Signal 2021; 14:700 [View Article]
     [Google Scholar]
  110. Collins AJ, Pastora AB, Smith TJ, O’Toole GA, Brun YV. MapA, a second large RTX adhesin conserved across the Pseudomonads, contributes to biofilm formation by Pseudomonas fluorescens. J Bacteriol 2020; 202:18 [View Article]
     [Google Scholar]
  111. Krasteva PV, Fong JCN, Shikuma NJ, Beyhan S, Navarro MVAS et al. Vibrio cholerae VpsT regulates matrix production and motility by directly sensing cyclic di-GMP. Science 2010; 327:866–868 [View Article]
     [Google Scholar]
  112. Zakikhany K, Harrington CR, Nimtz M, Hinton JCD, Römling U. Unphosphorylated CsgD controls biofilm formation in Salmonella enterica serovar Typhimurium. Mol Microbiol 2010; 77:771–786 [View Article] [PubMed]
     [Google Scholar]
  113. Leduc JL, Roberts GP. Cyclic di-GMP allosterically inhibits the CRP-like protein (Clp) of Xanthomonas axonopodis pv. citri. J Bacteriol 2009; 191:7121–7122 [View Article] [PubMed]
     [Google Scholar]
  114. Chin K-H, Lee Y-C, Tu Z-L, Chen C-H, Tseng Y-H et al. The cAMP receptor-like protein CLP is a novel c-di-GMP receptor linking cell-cell signaling to virulence gene expression in Xanthomonas campestris. J Mol Biol 2010; 396:646–662 [View Article] [PubMed]
     [Google Scholar]
  115. Tao F, He YW, Wu DH, Swarup S, Zhang LH. The cyclic nucleotide monophosphate domain of Xanthomonas campestris global regulator Clp defines a new class of cyclic di-GMP effectors. J Bacteriol 2010; 192:1020–1029 [View Article] [PubMed]
     [Google Scholar]
  116. Chen CH, Lin NT, Hsiao YM, Yang CY, Tseng YH. Two non-consensus Clp binding sites are involved in upregulation of the gum operon involved in xanthan polysaccharide synthesis in Xanthomonas campestris pv. campestris. Res Microbiol 2010; 161:583–589 [View Article] [PubMed]
     [Google Scholar]
  117. Lu X-H, An S-Q, Tang D-J, McCarthy Y, Tang J-L et al. RsmA regulates biofilm formation in Xanthomonas campestris through a regulatory network involving cyclic di-GMP and the Clp transcription factor. PLoS One 2012; 7:e52646 [View Article]
     [Google Scholar]
  118. Kuzmich S, Blumenkamp P, Meier D, Szadkowski D, Goesmann A et al. CRP-like transcriptional regulator MrpC curbs c-di-GMP and 3′,3′-cGAMP nucleotide levels during development in Myxococcus xanthus. mBio 2022; 13: [View Article]
     [Google Scholar]
  119. Fazli M, O’Connell A, Nilsson M, Niehaus K, Dow JM et al. The CRP/FNR family protein Bcam1349 is a c-di-GMP effector that regulates biofilm formation in the respiratory pathogen Burkholderia cenocepacia. Mol Microbiol 2011; 82:327–341 [View Article] [PubMed]
     [Google Scholar]
  120. Liu C, Sun D, Liu J, Chen Y, Zhou X et al. cAMP and c-di-GMP synergistically support biofilm maintenance through the direct interaction of their effectors. Nat Commun 2022; 13: [View Article]
     [Google Scholar]
  121. Davis R, Écija-Conesa A, Gallego-Jara J, de Diego T, Filippova EV et al. An acetylatable lysine controls CRP function in E. coli. Mol Microbiol 2018; 107:116–131 [View Article] [PubMed]
     [Google Scholar]
  122. Ro C, Cashel M, Fernández-Coll L, Koestler BJ. The secondary messenger ppGpp interferes with cAMP-CRP regulon by promoting CRP acetylation in Escherichia coli. PLoS One 2021; 16:e0259067 [View Article]
     [Google Scholar]
  123. An S-Q, Allan JH, McCarthy Y, Febrer M, Dow JM et al. The PAS domain-containing histidine kinase RpfS is a second sensor for the diffusible signal factor of Xanthomonas campestris. Mol Microbiol 2014; 92:586–597 [View Article] [PubMed]
     [Google Scholar]
  124. Han S, Shen D, Wang Y-C, Chou S-H, Gomelsky M et al. A YajQ-LysR-like, cyclic di-GMP-dependent system regulating biosynthesis of an antifungal antibiotic in a crop-protecting bacterium, Lysobacter enzymogenes. Mol Plant Pathol 2020; 21:218–229 [View Article] [PubMed]
     [Google Scholar]
  125. Iyer LM, Leipe DD, Koonin EV, Aravind L. Evolutionary history and higher order classification of AAA+ ATPases. J Struct Biol 2004; 146:11–31 [View Article] [PubMed]
     [Google Scholar]
  126. Leipe DD, Wolf YI, Koonin EV, Aravind L. Classification and evolution of P-loop GTPases and related ATPases. J Mol Biol 2002; 317:41–72 [View Article] [PubMed]
     [Google Scholar]
  127. Matsuyama BY, Krasteva PV, Baraquet C, Harwood CS, Sondermann H et al. Mechanistic insights into c-di-GMP-dependent control of the biofilm regulator FleQ from Pseudomonas aeruginosa. Proc Natl Acad Sci 2016; 113:E209–18 [View Article] [PubMed]
     [Google Scholar]
  128. Chakraborty S, Biswas M, Dey S, Agarwal S, Chakrabortty T et al. The heptameric structure of the flagellar regulatory protein FlrC is indispensable for ATPase activity and disassembled by cyclic-di-GMP. J Biol Chem 2020; 295:16960–16974 [View Article] [PubMed]
     [Google Scholar]
  129. Chakrabortty T, Roy Chowdhury S, Ghosh B, Sen U. Crystal structure of VpsR revealed novel dimeric architecture and c-di-GMP binding site: mechanistic implications in oligomerization, ATPase activity and DNA binding. J Mol Biol 2022; 434:167354 [View Article] [PubMed]
     [Google Scholar]
  130. Osbourne DO, Soo VW, Konieczny I, Wood TK. Polyphosphate, cyclic AMP, guanosine tetraphosphate, and c-di-GMP reduce in vitro Lon activity. Bioengineered 2014; 5:264–268 [View Article] [PubMed]
     [Google Scholar]
  131. Joshi A, Mahmoud SA, Kim S-K, Ogdahl JL, Lee VT et al. c-di-GMP inhibits LonA-dependent proteolysis of TfoY in Vibrio cholerae. PLoS Genet 2020; 16:e1008897 [View Article]
     [Google Scholar]
  132. Floyd KA, Lee CK, Xian W, Nametalla M, Valentine A et al. c-di-GMP modulates type IV MSHA pilus retraction and surface attachment in Vibrio cholerae. Nat Commun 2020; 11: [View Article]
     [Google Scholar]
  133. Roelofs KG, Jones CJ, Helman SR, Shang X, Orr MW et al. Systematic identification of cyclic-di-GMP binding proteins in Vibrio cholerae reveals a novel class of cyclic-di-GMP-binding ATPases associated with Type II secretion systems. PLoS Pathog 2015; 11:e1005232 [View Article] [PubMed]
     [Google Scholar]
  134. Trampari E, Stevenson CEM, Little RH, Wilhelm T, Lawson DM et al. Bacterial rotary export ATPases are allosterically regulated by the nucleotide second messenger cyclic-di-GMP. J Biol Chem 2015; 290:24470–24483 [View Article] [PubMed]
     [Google Scholar]
  135. Manikandan K, Prasad D, Srivastava A, Singh N, Dabeer S et al. The second messenger cyclic di-AMP negatively regulates the expression of Mycobacterium smegmatis recA and attenuates DNA strand exchange through binding to the C-terminal motif of mycobacterial RecA proteins. Mol Microbiol 2018; 109:600–614 [View Article] [PubMed]
     [Google Scholar]
  136. Kaczmarczyk A, Hempel AM, von Arx C, Böhm R, Dubey BN et al. Precise timing of transcription by c-di-GMP coordinates cell cycle and morphogenesis in Caulobacter. Nat Commun 2020; 11: [View Article]
     [Google Scholar]
  137. Nesper J, Hug I, Kato S, Hee C-S, Habazettl JM et al. Cyclic di-GMP differentially tunes a bacterial flagellar motor through a novel class of CheY-like regulators. Elife 2017; 6:e28842 [View Article] [PubMed]
     [Google Scholar]
  138. Doerfel LK, Wohlgemuth I, Kothe C, Peske F, Urlaub H et al. EF-P is essential for rapid synthesis of proteins containing consecutive proline residues. Science 2013; 339:85–88 [View Article] [PubMed]
     [Google Scholar]
  139. Guo Q, Cui B, Wang M, Li X, Tan H et al. Elongation factor P modulates Acinetobacter baumannii physiology and virulence as a cyclic dimeric guanosine monophosphate effector. Proc Natl Acad Sci 2022; 119:41 [View Article]
     [Google Scholar]
  140. Steiner S, Lori C, Boehm A, Jenal U. Allosteric activation of exopolysaccharide synthesis through cyclic di-GMP-stimulated protein-protein interaction. The EMBO journal 2013; 32:354–368 [View Article] [PubMed]
     [Google Scholar]
  141. Nelson JW, Sudarsan N, Phillips GE, Stav S, Lünse CE et al. Control of bacterial exoelectrogenesis by c-AMP-GMP. Proceedings of the National Academy of Sciences of the United States of America 2015; 112:5389–5394 [View Article] [PubMed]
     [Google Scholar]
  142. Kader A, Simm R, Gerstel U, Morr M, Römling U. Hierarchical involvement of various GGDEF domain proteins in rdar morphotype development of Salmonella enterica serovar Typhimurium. Mol Microbiol 2006; 60:602–616 [View Article] [PubMed]
     [Google Scholar]
  143. Römling U. Cyclic di-GMP signaling in Salmonella enterica serovar Typhimurium. In Chou S-H, Guiliani N, Lee VT, Römling U. eds Microbial Cyclic Di-Nucleotide Signaling Cham, Switzerland: Springer; 2020 pp 395–426 [View Article]
     [Google Scholar]
  144. Hay ID, Remminghorst U, Rehm BHA. MucR, a novel membrane-associated regulator of alginate biosynthesis in Pseudomonas aeruginosa. Appl Environ Microbiol 2009; 75:1110–1120 [View Article] [PubMed]
     [Google Scholar]
  145. Bantinaki E, Kassen R, Knight CG, Robinson Z, Spiers AJ et al. Adaptive divergence in experimental populations of Pseudomonas fluorescens. III. Mutational origins of wrinkly spreader diversity. Genetics 2007; 176:441–453 [View Article] [PubMed]
     [Google Scholar]
  146. McDonald MJ, Gehrig SM, Meintjes PL, Zhang X-X, Rainey PB. Adaptive divergence in experimental populations of Pseudomonas fluorescens . IV. Genetic constraints guide evolutionary trajectories in a parallel adaptive radiation. Genetics 2009; 183:1041–1053 [View Article]
     [Google Scholar]
  147. Lind PA, Farr AD, Rainey PB. Experimental evolution reveals hidden diversity in evolutionary pathways. Elife 2015; 4:e07074 [View Article] [PubMed]
     [Google Scholar]
  148. Lind PA, Libby E, Herzog J, Rainey PB. Predicting mutational routes to new adaptive phenotypes. Elife 2019; 8:e38822 [View Article] [PubMed]
     [Google Scholar]
  149. Lind PA, Farr AD, Rainey PB. Evolutionary convergence in experimental Pseudomonas populations. ISME J 2017; 11:589–600 [View Article] [PubMed]
     [Google Scholar]
  150. Besse A, Groleau M-C, Trottier M, Vincent AT, Déziel E et al. Pseudomonas aeruginosa strains from both clinical and environmental origins readily adopt a stable small-colony-variant phenotype resulting from single mutations in c-di-GMP pathways. J Bacteriol 2022; 204:10 [View Article]
     [Google Scholar]
  151. Malone JG, Jaeger T, Spangler C, Ritz D, Spang A et al. YfiBNR mediates cyclic di-GMP dependent small colony variant formation and persistence in Pseudomonas aeruginosa. PLoS Pathog 2010; 6:e1000804 [View Article] [PubMed]
     [Google Scholar]
  152. Wang D, Dorosky RJ, Han CS, Lo C-C, Dichosa AEK et al. Adaptation genomics of a small-colony variant in a Pseudomonas chlororaphis 30-84 biofilm. Appl Environ Microbiol 2015; 81:890–899 [View Article] [PubMed]
     [Google Scholar]
  153. Gloag ES, Marshall CW, Snyder D, Lewin GR, Harris JS et al. Pseudomonas aeruginosa interstrain dynamics and selection of hyperbiofilm mutants during a chronic infection. mBio 2019; 10: [View Article]
     [Google Scholar]
  154. Traverse CC, Mayo-Smith LM, Poltak SR, Cooper VS. Tangled bank of experimentally evolved Burkholderia biofilms reflects selection during chronic infections. Proc Natl Acad Sci 2013; 110:E250–9 [View Article] [PubMed]
     [Google Scholar]
  155. Brock MT, Fedderly GC, Borlee GI, Russell MM, Filipowska LK et al. Pseudomonas aeruginosa variants obtained from veterinary clinical samples reveal a role for cyclic di-GMP in biofilm formation and colony morphology. Microbiology 2017; 163:1613–1625 [View Article] [PubMed]
     [Google Scholar]
  156. Zeng Z, Lin S, Li Q, Wang W, Wang Y et al. Molecular basis of wrinkled variants isolated from Pseudoalteromonas lipolytica biofilms. Front Microbiol 2022; 13:797197 [View Article] [PubMed]
     [Google Scholar]
  157. Blanka A, Düvel J, Dötsch A, Klinkert B, Abraham W-R et al. Constitutive production of c-di-GMP is associated with mutations in a variant of Pseudomonas aeruginosa with altered membrane composition. Sci Signal 2015; 8:372 [View Article] [PubMed]
     [Google Scholar]
  158. Kim W, Racimo F, Schluter J, Levy SB, Foster KR. Importance of positioning for microbial evolution. Proc Natl Acad Sci 2014; 111:E1639–1647 [View Article]
     [Google Scholar]
  159. Kim W, Levy SB, Foster KR. Rapid radiation in bacteria leads to a division of labour. Nat Commun 2016; 7:10508 [View Article] [PubMed]
     [Google Scholar]
  160. Kessler C, Kim W. Identification of cyclic-di-GMP-modulating protein residues by bidirectionally evolving a social behavior in Pseudomonas fluorescens. mSystems 2022; 7:e0073722 [View Article] [PubMed]
     [Google Scholar]
  161. Røder HL, Herschend J, Russel J, Andersen MF, Madsen JS et al. Enhanced bacterial mutualism through an evolved biofilm phenotype. ISME J 2018; 12:2608–2618 [View Article] [PubMed]
     [Google Scholar]
  162. Potts AH, Guo Y, Ahmer BMM, Romeo T, Roop RM. Role of CsrA in stress responses and metabolism important for Salmonella virulence revealed by integrated transcriptomics. PLoS One 2019; 14:e0211430 [View Article]
     [Google Scholar]
  163. Leng Y, Vakulskas CA, Zere TR, Pickering BS, Watnick PI et al. Regulation of CsrB/C sRNA decay by EIIA(Glc) of the phosphoenolpyruvate: carbohydrate phosphotransferase system. Mol Microbiol 2016; 99:627–639 [View Article] [PubMed]
     [Google Scholar]
  164. Dubey BN, Lori C, Ozaki S, Fucile G, Plaza-Menacho I et al. Cyclic di-GMP mediates a histidine kinase/phosphatase switch by noncovalent domain cross-linking. Sci Adv 2016; 2: [View Article]
     [Google Scholar]
  165. Goymer P, Kahn SG, Malone JG, Gehrig SM, Spiers AJ et al. Adaptive divergence in experimental populations of Pseudomonas fluorescens. II. Role of the GGDEF regulator WspR in evolution and development of the wrinkly spreader phenotype. Genetics 2006; 173:515–526 [View Article] [PubMed]
     [Google Scholar]
  166. Xu K, Wang L, Xiong D, Chen H, Tong X et al. The Wsp chemosensory system modulates c-di-GMP-dependent biofilm formation by integrating DSF quorum sensing through the WspR-RpfG complex in Lysobacter. NPJ Biofilms Microbiomes 2022; 8:97 [View Article] [PubMed]
     [Google Scholar]
  167. Xu L, Venkataramani P, Ding Y, Liu Y, Deng Y et al. A cyclic di-GMP-binding adaptor protein interacts with histidine kinase to regulate two-component signaling. J Biol Chem 2016; 291:16112–16123 [View Article] [PubMed]
     [Google Scholar]
  168. Higgins DG, Thompson JD, Gibson TJ. Using CLUSTAL for multiple sequence alignments. Methods Enzymol 1996; 266:383–402 [View Article] [PubMed]
     [Google Scholar]
  169. Kumar S, Stecher G, Li M, Knyaz C, Tamura K. MEGA X: Molecular Evolutionary Genetics Analysis across computing platforms. Mol Biol Evol 2018; 35:1547–1549 [View Article] [PubMed]
     [Google Scholar]
  170. Hengge R, Galperin MY, Ghigo J-M, Gomelsky M, Green J et al. Systematic nomenclature for GGDEF and EAL domain-containing cyclic Di-GMP turnover proteins of Escherichia coli. J Bacteriol 2016; 198:7–11 [View Article]
     [Google Scholar]
  171. Branchu P, Hindré T, Fang X, Thomas R, Gomelsky M et al. The c-di-GMP phosphodiesterase VmpA absent in Escherichia coli K12 strains affects motility and biofilm formation in the enterohemorrhagic O157:H7 serotype. Vet Immunol Immunopathol 2013; 152:132–140 [View Article] [PubMed]
     [Google Scholar]
  172. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol 1990; 215:403–410 [View Article] [PubMed]
     [Google Scholar]
  173. Ryjenkov DA, Simm R, Römling U, Gomelsky M. The Pilz domain protein Ycgr is a C-Di-GMP receptor that affects motility in Enterobacteria. in preparation 2006
     [Google Scholar]
  174. Jusufovic N, Savage CR, Saylor TC, Brissette CA, Zückert WR et al. Borrelia burgdorferi PlzA is a c-di-GMP dependent DNA and RNA binding protein. bioRxiv2023.01.30.526351 2023 [View Article] [PubMed]
     [Google Scholar]
  175. Sheng S, Xin L, Yam JKH, Salido MM, Khong NZJ et al. The MapZ-Mediated Methylation of Chemoreceptors Contributes to Pathogenicity of Pseudomonas aeruginosa. Frontiers in microbiology 2019; 10:67 [View Article] [PubMed]
     [Google Scholar]
  176. Zhang LH. A novel C-di-GMP effector linking intracellular virulence regulon to quorum sensing and hypoxia sensing. Virulence 2010; 1:391–394 [View Article] [PubMed]
     [Google Scholar]
  177. Marden JN, Dong Q, Roychowdhury S, Berleman JE, Bauer CE. Cyclic GMP controls Rhodospirillum centenum cyst development. Molecular microbiology 2011; 79:600–615 [View Article] [PubMed]
     [Google Scholar]
  178. Hickman JW, Harwood CS. Identification of FleQ from Pseudomonas aeruginosa as a c-di-GMP-responsive transcription factor. Mol Microbiol 2008; 69:376–389 [View Article] [PubMed]
     [Google Scholar]
  179. Abel S, Chien P, Wassmann P, Schirmer T, Kaever V et al. Regulatory cohesion of cell cycle and cell differentiation through interlinked phosphorylation and second messenger networks. Mol Cell 2011; 43:550–560 [View Article] [PubMed]
     [Google Scholar]
  180. Paul R, Weiser S, Amiot NC, Chan C, Schirmer T et al. Cell cycle-dependent dynamic localization of a bacterial response regulator with a novel di-guanylate cyclase output domain. Genes Dev 2004; 18:715–727 [View Article] [PubMed]
     [Google Scholar]
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Evolution of cyclic di-GMP signalling on a short and long term time scale
Microbiology 169, 001354 (2023); https://doi.org/10.1099/mic.0.001354
/content/journal/micro/10.1099/mic.0.001354
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