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Cyclic di-GMP Signaling Systems in the Gram-Positive Bacillus cereus Group

  • Wen Yin
  • Lu Liu
  • Siyang Xu
  • Jin HeEmail author
Chapter
  • 108 Downloads

Abstract

Cyclic di-GMP is a nucleotide second messenger molecule widely distributed in Gram-negative bacteria and plays a central role in the regulation of bacterial metabolism and signaling. However, its importance in affecting Gram-positive bacterial physiology is less known. The Bacillus cereus group is an important class of Gram-positive Bacilli, including more than ten species such as B. thuringiensis, B. anthracis, and B. cereus with minute genetic differences. Intriguingly, there exist up to 13 cyclic di-GMP turnover enzymes containing functional domains GGDEF, EAL, or HD-GYP as well as signal sensor domains such as PAS and GAF domains in the B. cereus group strains, which are stimulated by environmental signals to regulate intracellular cyclic di-GMP concentration. Cyclic di-GMP can bind to downstream receptors or targets to perform its biological functions. Its downstream receptors or targets are mainly proteins and RNA aptamers, although protein receptors have not yet been reported in the B. cereus group strains. The RNA receptors are mostly riboswitches, including Bc1 RNA, Bc2 RNA, and Bc3-5 RNA. Cyclic di-GMP is involved extensively in affecting various physiological activities of bacteria, such as cell motility, biofilm formation, exopolysaccharides synthesis, and expression of pathogenic factors. In this chapter, we review the features of cyclic di-GMP turnover enzymes, the homeostasis of cyclic di-GMP, the study of receptors/targets, and the function of cyclic di-GMP in regulation of physiology in Gram-positive B. cereus group.

Keywords

Bacillus cereus group Cyclic di-GMP Diguanylate cyclase (DGC) Cyclic di-GMP-specific phosphodiesterase (PDE) Receptor Riboswitch Regulation functions 

Notes

Acknowledgments

This study was supported by the National Natural Science Foundation of China (grants 31770087 and 31970074) and the Fundamental Research Funds for the Central Universities (grants 2662015PY175 and 2662017PY112), and the China Postdoctoral Science Foundation (2018M630872). We would like to thank Shan-Ho Chou of NCHU Agricultural Biotechnology Center, Institute of Biochemistry, National Chung Hsing University for reading the manuscript and for insightful discussions.

References

  1. 1.
    Vos P, Garrity G, Jones D, Krieg NR, Ludwig W, Rainey FA, Schleifer KH, Whitman W (2009) Bergey’s manual of systematic bacteriology, vol 3. The Firmicutes, 2nd edn. Springer, New York, p 1450. isbn:978-0-387-95041-9Google Scholar
  2. 2.
    Harwood CR, Mouillon JM, Pohl S, Arnau J (2018) Secondary metabolite production and the safety of industrially important members of the Bacillus subtilis group. FEMS Microbiol Rev 42:721–738PubMedPubMedCentralCrossRefGoogle Scholar
  3. 3.
    Liu Y, Du J, Lai Q, Zeng R, Ye D, Xu J, Shao Z (2017) Proposal of nine novel species of the Bacillus cereus group. Int J Syst Evol Microbiol 67:2499–2508PubMedCrossRefGoogle Scholar
  4. 4.
    Yu Z, He J, Wang J (2017) Molecular biology of Bacillus thuringiensis. Science Press, Bejing. isbn:978-7-03-054781-1Google Scholar
  5. 5.
    Ross P, Weinhouse H, Aloni Y, Michaeli D, Weinberger-Ohana P, Mayer R, Braun S, de Vroom E, van der Marel GA, van Boom JH, Benziman M (1987) Regulation of cellulose synthesis in Acetobacter xylinum by cyclic diguanylic acid. Nature 325:279–281PubMedCrossRefGoogle Scholar
  6. 6.
    Jenal U, Reinders A, Lori C (2017) Cyclic di-GMP: second messenger extraordinaire. Nat Rev Microbiol 15:271–284PubMedCrossRefGoogle Scholar
  7. 7.
    Matsutani M, Ito K, Azuma Y, Ogino H, Shirai M, Yakushi T, Matsushita K (2015) Adaptive mutation related to cellulose producibility in Komagataeibacter medellinensis (Gluconacetobacter xylinus) NBRC 3288. Appl Microbiol Biotechnol 99:7229–7240PubMedCrossRefGoogle Scholar
  8. 8.
    Chan C, Paul R, Samoray D, Amiot NC, Giese B, Jenal U, Schirmer T (2004) Structural basis of activity and allosteric control of diguanylate cyclase. Proc Natl Acad Sci U S A 101:17084–17089PubMedPubMedCentralCrossRefGoogle Scholar
  9. 9.
    Schmidt AJ, Ryjenkov DA, Gomelsky M (2005) The ubiquitous protein domain EAL is a cyclic diguanylate-specific phosphodiesterase: enzymatically active and inactive EAL domains. J Bacteriol 187:4774–4781PubMedPubMedCentralCrossRefGoogle Scholar
  10. 10.
    Sultan SZ, Pitzer JE, Boquoi T, Hobbs G, Miller MR, Motaleb MA (2011) Analysis of the HD-GYP domain cyclic dimeric GMP phosphodiesterase reveals a role in motility and the enzootic life cycle of Borrelia burgdorferi. Infect Immun 79:3273–3283PubMedPubMedCentralCrossRefGoogle Scholar
  11. 11.
    Laventie BJ, Sangermani M, Estermann F, Manfredi P, Planes R, Hug I, Jaeger T, Meunier E, Broz P, Jenal U (2019) A surface-induced asymmetric program promotes tissue colonization by Pseudomonas aeruginosa. Cell Host Microbe 25:140–152PubMedCrossRefGoogle Scholar
  12. 12.
    Chen Y, Chai Y, Guo JH, Losick R (2012) Evidence for cyclic Di-GMP-mediated signaling in Bacillus subtilis. J Bacteriol 194:5080–5090PubMedPubMedCentralCrossRefGoogle Scholar
  13. 13.
    Gao X, Mukherjee S, Matthews PM, Hammad LA, Kearns DB, Dann CE III (2013) Functional characterization of core components of the Bacillus subtilis cyclic-di-GMP signaling pathway. J Bacteriol 195:4782–4792PubMedPubMedCentralCrossRefGoogle Scholar
  14. 14.
    Subramanian S, Gao X, Dann CE III, Kearns DB (2017) MotI (DgrA) acts as a molecular clutch on the flagellar stator protein MotA in Bacillus subtilis. Proc Natl Acad Sci U S A 114:13537–13542PubMedPubMedCentralCrossRefGoogle Scholar
  15. 15.
    Fagerlund A, Smith V, Rohr AK, Lindback T, Parmer MP, Andersson KK, Reubsaet L, Okstad OA (2016) Cyclic diguanylate regulation of Bacillus cereus group biofilm formation. Mol Microbiol 101:471–494PubMedCrossRefGoogle Scholar
  16. 16.
    Tang Q, Yin K, Qian H, Zhao Y, Wang W, Chou SH, Fu Y, He J (2016) Cyclic di-GMP contributes to adaption and virulence of Bacillus thuringiensis through a riboswitch-regulated collagen adhesion protein. Sci Rep 6:28807PubMedPubMedCentralCrossRefGoogle Scholar
  17. 17.
    Sudarsan N, Lee ER, Weinberg Z, Moy RH, Kim JN, Link KH, Breaker RR (2008) Riboswitches in eubacteria sense the second messenger cyclic di-GMP. Science 321:411–413PubMedPubMedCentralCrossRefGoogle Scholar
  18. 18.
    Galperin MY (2005) A census of membrane-bound and intracellular signal transduction proteins in bacteria: bacterial IQ, extroverts and introverts. BMC Microbiol 5:35PubMedPubMedCentralCrossRefGoogle Scholar
  19. 19.
    Henry JT, Crosson S (2011) Ligand-binding PAS domains in a genomic, cellular, and structural context. Annu Rev Microbiol 65:261–286PubMedPubMedCentralCrossRefGoogle Scholar
  20. 20.
    Fu Y, Yu Z, Liu S, Chen B, Zhu L, Li Z, Chou SH, He J (2018) C-di-GMP regulates various phenotypes and insecticidal activity of Gram-positive Bacillus thuringiensis. Front Microbiol 9:45PubMedPubMedCentralCrossRefGoogle Scholar
  21. 21.
    Chou SH, Galperin MY (2016) Diversity of cyclic di-GMP-binding proteins and mechanisms. J Bacteriol 198:32–46PubMedCrossRefGoogle Scholar
  22. 22.
    Benach J, Swaminathan SS, Tamayo R, Handelman SK, Folta-Stogniew E, Ramos JE, Forouhar F, Neely H, Seetharaman J, Camill A, Hunt JF (2007) The structural basis of cyclic diguanylate signal transduction by PilZ domains. EMBO J 26:5153–5166PubMedPubMedCentralCrossRefGoogle Scholar
  23. 23.
    Pratt JT, Tamayo R, Tischler AD, Camilli A (2007) PilZ domain proteins bind cyclic diguanylate and regulate diverse processes in Vibrio cholerae. J Biol Chem 282:12860–12870PubMedPubMedCentralCrossRefGoogle Scholar
  24. 24.
    Ryjenkov DA, Simm R, Romling U, Gomelsky M (2006) 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 281:30310–30314PubMedCrossRefGoogle Scholar
  25. 25.
    Pultz IS, Christen M, Kulasekara HD, Kennard A, Kulasekara B, Miller SI (2012) The response threshold of Salmonella PilZ domain proteins is determined by their binding affinities for c-di-GMP. Mol Microbiol 86:1424–1440PubMedPubMedCentralCrossRefGoogle Scholar
  26. 26.
    Christen M, Christen B, Allan MG, Folcher M, Jenö P, Grzesiek S, Jenal U (2007) DgrA is a member of a new family of cyclic diguanosine monophosphate receptors and controls flagellar motor function in Caulobacter crescentus. Proc Natl Acad Sci U S A 104:4112–4117PubMedPubMedCentralCrossRefGoogle Scholar
  27. 27.
    Merighi M, Lee VT, Hyodo M, Hayakawa Y, Lory S (2007) The second messenger bis-(3′-5′)-cyclic-GMP and its PilZ domain-containing receptor Alg44 are required for alginate biosynthesis in Pseudomonas aeruginosa. Mol Microbiol 65:876–895PubMedCrossRefGoogle Scholar
  28. 28.
    Wilksch JJ, Yang J, Clements A, Gabbe JL, Short KR, Cao H, Cavaliere R, James CE, Whitchurch CB, Schembri MA, Chuah ML, Liang ZX, Wijburg OL, Jenney AW, Lithgow T, Strugnell RA (2011) MrkH, a novel c-di-GMP-dependent transcriptional activator, controls Klebsiella pneumoniae biofilm formation by regulating type 3 fimbriae expression. PLoS Pathog 7:e1002204PubMedPubMedCentralCrossRefGoogle Scholar
  29. 29.
    Wang F, He Q, Su K, Gao F, Huang Y, Lin Z, Zhu D, Gu L (2016) The PilZ domain of MrkH represents a novel DNA binding motif. Protein Cell 7:766–772PubMedPubMedCentralCrossRefGoogle Scholar
  30. 30.
    Russell MH, Bible AN, Fang X, Gooding JR, Campagna SR, Gomelsky M, Alexandre G (2013) Integration of the second messenger c-di-GMP into the chemotactic signaling pathway. mBio 4:e00001–e00013PubMedPubMedCentralCrossRefGoogle Scholar
  31. 31.
    Baraquet C, Harwood CS (2013) Cyclic diguanosine monophosphate represses bacterial flagella synthesis by interacting with the Walker A motif of the enhancer-binding protein FleQ. Proc Natl Acad Sci U S A 110:18478–18483PubMedPubMedCentralCrossRefGoogle Scholar
  32. 32.
    Krasteva PV, Fong JC, Shikuma NJ, Beyhan S, Navarro MV, Yildiz FH, Sondermann H (2010) Vibrio cholerae VpsT regulates matrix production and motility by directly sensing cyclic di-GMP. Science 327:866–868PubMedPubMedCentralCrossRefGoogle Scholar
  33. 33.
    Tao F, He YW, Wu DH, Swarup S, Zhang LH (2010) The cyclic nucleotide monophosphate domain of Xanthomonas campestris global regulator Clp defines a new class of cyclic di-GMP effectors. J Bacteriol 192:1020–1029PubMedCrossRefGoogle Scholar
  34. 34.
    Fazli M, O'Connell A, Nilsson M, Niehaus K, Dow JM, Givskov M, Ryan RP, Tolker-Nielsen T (2011) The CRP/FNR family protein Bcam1349 is a c-di-GMP effector that regulates biofilm formation in the respiratory pathogen Burkholderia cenocepacia. Mol Microbiol 82:327–341PubMedCrossRefGoogle Scholar
  35. 35.
    Christen B, Christen M, Paul R, Schmid F, Folcher M, Jenoe P, Meuwly M, Jenal U (2006) Allosteric control of cyclic di-GMP signaling. J Biol Chem 281:32015–32024PubMedCrossRefGoogle Scholar
  36. 36.
    De N, Navarro MV, Raghavan RV, Sondermann H (2009) Determinants for the activation and autoinhibition of the diguanylate cyclase response regulator WspR. J Mol Biol 393:619–633PubMedPubMedCentralCrossRefGoogle Scholar
  37. 37.
    Lee VT, Matewish JM, Kessler JL, Hyodo M, Hayakawa Y, Lory S (2007) A cyclic-di-GMP receptor required for bacterial exopolysaccharide production. Mol Microbiol 65:1474–1484PubMedPubMedCentralCrossRefGoogle Scholar
  38. 38.
    Abel S, Chien P, Wassmann P, Schirmer T, Kaever V, Laub MT, Baker TA, Jenal U (2011) Regulatory cohesion of cell cycle and cell differentiation through interlinked phosphorylation and second messenger networks. Mol Cell 43:550–560PubMedPubMedCentralCrossRefGoogle Scholar
  39. 39.
    Duerig A, Abel S, Folcher M, Nicollier M, Schwede T, Amiot N, Giese B, Jenal U (2009) Second messenger-mediated spatiotemporal control of protein degradation regulates bacterial cell cycle progression. Genes Dev 23:93–104PubMedPubMedCentralCrossRefGoogle Scholar
  40. 40.
    Qi Y, Chuah ML, Dong X, Xie K, Luo Z, Tang K, Liang ZX (2011) Binding of cyclic diguanylate in the non-catalytic EAL domain of FimX induces a long-range conformational change. J Biol Chem 286:2910–2917PubMedCrossRefGoogle Scholar
  41. 41.
    Navarro MV, Newell PD, Krasteva PV, Chatterjee D, Madden DR, O’Toole GA, Sondermann H (2011) Structural basis for c-di-GMP-mediated inside-out signaling controlling periplasmic proteolysis. PLoS Biol 9:e1000588PubMedPubMedCentralCrossRefGoogle Scholar
  42. 42.
    Newell PD, Monds RD, O’Toole GA (2009) LapD is a bis-(3′,5′)-cyclic dimeric GMP-binding protein that regulates surface attachment by Pseudomonas fluorescens Pf0–1. Proc Natl Acad Sci U S A 106:3461–3466PubMedPubMedCentralCrossRefGoogle Scholar
  43. 43.
    Wang YC, Chin KH, Tu ZL, He J, Jones CJ, Sanchez DZ, Yildiz FH, Galperin MY, Chou SH (2016) Nucleotide binding by the widespread high-affinity cyclic di-GMP receptor MshEN domain. Nat Commun 7:12481PubMedPubMedCentralCrossRefGoogle Scholar
  44. 44.
    Tuckerman JR, Gonzalez G, Gilles-Gonzalez MA (2011) Cyclic di-GMP activation of polynucleotide phosphorylase signal-dependent RNA processing. J Mol Biol 407:633–639PubMedCrossRefGoogle Scholar
  45. 45.
    Lee ER, Baker JL, Weinberg Z, Sudarsan N, Breaker RR (2010) An allosteric self-splicing ribozyme triggered by a bacterial second messenger. Science 329:845–848PubMedPubMedCentralCrossRefGoogle Scholar
  46. 46.
    Amikam D, Galperin MY (2006) PilZ domain is part of the bacterial c-di-GMP binding protein. Bioinformatics 22:3–6PubMedCrossRefGoogle Scholar
  47. 47.
    Hickman JW, Harwood CS (2008) Identification of FleQ from Pseudomonas aeruginosa as a c-di-GMP-responsive transcription factor. Mol Microbiol 69:376–389PubMedPubMedCentralCrossRefGoogle Scholar
  48. 48.
    Romling U, Galperin MY, Gomelsky M (2013) Cyclic di-GMP: the first 25 years of a universal bacterial second messenger. Microbiol Mol Biol Rev 77:1–52PubMedPubMedCentralCrossRefGoogle Scholar
  49. 49.
    Zhou H, Zheng C, Su J, Chen B, Fu Y, Xie Y, Tang Q, Chou SH, He J (2016) Characterization of a natural triple-tandem c-di-GMP riboswitch and application of the riboswitch-based dual-fluorescence reporter. Sci Rep 6:20871PubMedPubMedCentralCrossRefGoogle Scholar
  50. 50.
    Yang Y, Li Y, Gao T, Zhang Y, Wang Q (2018) C-di-GMP turnover influences motility and biofilm formation in Bacillus amyloliquefaciens PG12. Res Microbiol 169:205–213PubMedCrossRefGoogle Scholar
  51. 51.
    Lee HS, Gu F, Ching SM, Lam Y, Chua KL (2010) CdpA is a Burkholderia pseudomallei cyclic di-GMP phosphodiesterase involved in autoaggregation, flagellum synthesis, motility, biofilm formation, cell invasion, and cytotoxicity. Infect Immun 78:1832–1840PubMedPubMedCentralCrossRefGoogle Scholar
  52. 52.
    Boehm A, Kaiser M, Li H, Spangler C, Kasper CA, Ackermann M, Kaever V, Sourjik V, Roth V, Jenal U (2010) Second messenger-mediated adjustment of bacterial swimming velocity. Cell 141:107–116PubMedCrossRefGoogle Scholar
  53. 53.
    Toyofuku M, Inaba T, Kiyokawa T, Obana N, Yawata Y, Nomura N (2016) Environmental factors that shape biofilm formation. Biosci Biotechnol Biochem 80:7–12PubMedCrossRefGoogle Scholar
  54. 54.
    Li XH, Kim SK, Lee JH (2017) Anti-biofilm effects of anthranilate on a broad range of bacteria. Sci Rep 7:8604PubMedPubMedCentralCrossRefGoogle Scholar
  55. 55.
    Purcell EB, Tamayo R (2016) Cyclic diguanylate signaling in Gram-positive bacteria. FEMS Microbiol Rev 40:753–773PubMedPubMedCentralCrossRefGoogle Scholar
  56. 56.
    Woodward JJ, Iavarone AT, Portnoy DA (2010) C-di-AMP secreted by intracellular Listeria monocytogenes activates a host type I interferon response. Science 328:1703–1705PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2020

Authors and Affiliations

  1. 1.State Key Laboratory of Agricultural MicrobiologyCollege of Life Science and Technology, Huazhong Agricultural UniversityWuhanPeople’s Republic of China

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