Cyclic diguanylate inversely regulates motility and aggregation in clostridium difficile

Journal of Bacteriology

Volumn 194, Issue 13, 2012, Pages 3307-3316

  Purcell, Erin B ^a   McKee, Robert W ^a   McBride, Shonna M ^b   Waters, Christopher M ^c   Tamayo, Rita ^a  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^b TUFTS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c Michigan State University   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIC DIGUANYLATE; CYCLIC GMP; FLAGELLIN; GENOMIC DNA; GUANOSINE TRIPHOSPHATE; KANAMYCIN; NISIN; PHOSPHODIESTERASE; PHOSPHORUS 32; THIAMPHENICOL; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL COLONIZATION; BACTERIAL FLAGELLUM; BACTERIAL GENE; BACTERIAL GENOME; BACTERIAL GROWTH; BACTERIUM CULTURE; BIOFILM; CLOSTRIDIUM DIFFICILE; CLOSTRIDIUM INFECTION; CONTROLLED STUDY; DEGRADATION; DNA SEQUENCE; ENZYME ACTIVITY; ENZYME ASSAY; GENE OVEREXPRESSION; GRAM POSITIVE BACTERIUM; INTESTINE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN PURIFICATION; PROTEIN SYNTHESIS; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SCANNING ELECTRON MICROSCOPY; SECOND MESSENGER; SYNTHESIS; THIN LAYER CHROMATOGRAPHY;

BACTERIAL ADHESION; BACTERIAL PROTEINS; CLOSTRIDIUM DIFFICILE; CYCLIC GMP; ESCHERICHIA COLI PROTEINS; GENE EXPRESSION REGULATION, BACTERIAL; LOCOMOTION; PHOSPHORUS-OXYGEN LYASES;

BACTERIA (MICROORGANISMS); CLOSTRIDIUM DIFFICILE; NEGIBACTERIA; POSIBACTERIA;

EID: 84864023989     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.00100-12     Document Type: Article

References (73)

1. Albert-Weissenberger C, et al. 2010. Control of flagellar gene regulation in Legionella pneumophila and its relation to growth phase. J. Bacteriol. 192:446-455.
2. Beyhan S, Tischler AD, Camilli A, Yildiz FH. 2006. Transcriptome and phenotypic responses of Vibrio cholerae to increased cyclic di-GMP level. J. Bacteriol. 188:3600 -3613.
3. Bobrov AG, et al. 2011. Systematic analysis of cyclic di-GMP signalling enzymes and their role in biofilm formation and virulence in Yersinia pestis. Mol. Microbiol. 79:533-551.
4. Boehm A, et al. 2010. Second messenger-mediated adjustment of bacterial swimming velocity. Cell 141:107-116.
5. Bordeleau E, Fortier LC, Malouin F, Burrus V. 2011. c-di-GMP turnover in Clostridium difficile is controlled by a plethora of diguanylate cyclases and phosphodiesterases. PLoS Genet. 7:e1002039. doi:10.1371/ journal.pgen.1002039.
6. Chang AL, et al. 2001. Phosphodiesterase A1, a regulator of cellulose synthesis in Acetobacter xylinum, is a heme-based sensor. Biochemistry 40:3420 -3426.
7. Chen YF, Helmann JD. 1992. Restoration of motility to an Escherichia coli fliA flagellar mutant by a Bacillus subtilis sigma factor. Proc. Natl. Acad. Sci. U. S. A. 89:5123-5127.
8. Christen M, et al. 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- 4117.
9. Christen M, Christen B, Folcher M, Schauerte A, Jenal U. 2005. Identification and characterization of a cyclic di-GMP specific phosphodiesterase and its allosteric control by GTP. J. Biol. Chem. 280:30829 -30837.
10. Da Re S, Ghigo JM. 2006. A CsgD-independent pathway for cellulose production and biofilm formation in Escherichia coli. J. Bacteriol. 188: 3073-3087.
11. Deneve C, Janoir C, Poilane I, Fantinato C, Collignon A. 2009. New trends in Clostridium difficile virulence and pathogenesis. Int. J. Antimicrob. Agents. 33(Suppl. 1):S24 -S38.
12. Dingle TC, Mulvey GL, Armstrong GD. 2011. Mutagenic analysis of the Clostridium difficile flagellar proteins, FliC and FliD, and their contribution to virulence in hamsters. Infect. Immun. 79:4061- 4067.
13. Duerig A, et al. 2009. Second messenger-mediated spatiotemporal control of protein degradation regulates bacterial cell cycle progression. Genes Dev. 23:93-104.
14. Emerson JE, Stabler RA, Wren BW, Fairweather NF. 2008. Microarray analysis of the transcriptional responses of Clostridium difficile to environmental and antibiotic stress. J. Med. Microbiol. 57:757-764.
15. Fagan RP, Fairweather NF. 2011. Clostridium difficile has two parallel and essential Sec secretion systems. J. Biol. Chem. 286:27483-27493.
16. Faruque SM, et al. 2006. Transmissibility of cholera: in vivo-formed biofilms and their relationship to infectivity and persistence in the environment. Proc. Natl. Acad. Sci. U. S. A. 103:6350-6355.
17. Galperin MY. 2005. A census of membrane-bound and intracellular signal transduction proteins in bacteria: bacterial IQ, extroverts and introverts. BMC Microbiol. 5:35.
18. Galperin MY, Nikolskaya AN, Koonin EV. 2001. Novel domains of the prokaryotic two-component signal transduction systems. FEMS Microbiol. Lett. 203:11-21.
19. Goulding D, et al. 2009. Distinctive profiles of infection and pathology in hamsters infected with Clostridium difficile strains 630 and B1. Infect. Immun. 77:5478 -5485.
20. Guzman LM, Belin D, Carson MJ, Beckwith J. 1995. Tight regulation, modulation, and high-level expression by vectors containing the arabinose PBAD promoter. J. Bacteriol. 177:4121- 4130.
21. Hickman JW, Tifrea DF, Harwood CS. 2005. A chemosensory system that regulates biofilm formation through modulation of cyclic diguanylate levels. Proc. Natl. Acad. Sci. U. S. A. 102:14422-14427.
22. Hisert KB, et al. 2005. 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. 56: 1234-1245.
23. Holland LM, et al. 2008. A staphylococcal GGDEF domain protein regulates biofilm formation independently of cyclic dimeric GMP. J. Bacteriol. 190:5178 -5189.
24. Huang B, Whitchurch CB, Mattick JS. 2003. FimX, a multidomain protein connecting environmental signals to twitching motility in Pseudomonas aeruginosa. J. Bacteriol. 185:7068 -7076.
25. Hughes KJ, Everiss KD, Kovach ME, Peterson KM. 1994. Sequence analysis of the Vibrio cholerae acfD gene reveals the presence of an overlapping reading frame, orfZ, which encodes a protein that shares sequence similarity to the FliA and FliC products of Salmonella. Gene 146:79-82.
26. Huitema E, Pritchard S, Matteson D, Radhakrishnan SK, Viollier PH. 2006. Bacterial birth scar proteins mark future flagellum assembly site. Cell 124:1025-1037.
27. Kader A, Simm R, Gerstel U, Morr M, Romling U. 2006. Hierarchical involvement of various GGDEF domain proteins in rdar morphotype development of Salmonella enterica serovar Typhimurium. Mol. Microbiol. 60:602- 616.
28. Kazmierczak BI, Lebron MB, Murray TS. 2006. Analysis of FimX, a phosphodiesterase that governs twitching motility in Pseudomonas aeruginosa. Mol. Microbiol. 60:1026 -1043.
29. Kim YK, McCarter LL. 2007. ScrG, a GGDEF-EAL protein, participates in regulating swarming and sticking in Vibrio parahaemolyticus. J. Bacteriol. 189:4094-4107.
30. Kulasakara H, et al. 2006. Analysis of Pseudomonas aeruginosa diguanylate cyclases and phosphodiesterases reveals a role for bis-(3'-5')-cyclic-GMP in virulence. Proc. Natl. Acad. Sci. U. S. A. 103:2839 -2844.
31. Lawley TD, et al. 2009. Antibiotic treatment of clostridium difficile carrier mice triggers a supershedder state, spore-mediated transmission, and severe disease in immunocompromised hosts. Infect. Immun. 77:3661- 3669.
32. Macfarlane S, Dillon JF. 2007. Microbial biofilms in the human gastrointestinal tract. J. Appl. Microbiol. 102:1187-1196.
33. Malone JG, et al. 2010. YfiBNR mediates cyclic di-GMP dependent small colony variant formation and persistence in Pseudomonas aeruginosa. PLoS Pathog. 6:e1000804. doi:10.1371/journal.ppat.1000804.
34. McBride SM, Sonenshein AL. 2011. Identification of a genetic locus responsible for antimicrobial peptide resistance in Clostridium difficile. Infect. Immun. 79:167-176.
35. Mendez-Ortiz MM, Hyodo M, Hayakawa Y, Membrillo-Hernandez J. 2006. Genome-wide transcriptional profile of Escherichia coli in response to high levels of the second messenger 3',5'-cyclic diguanylic acid. J. Biol. Chem. 281:8090-8099.
36. Monds RD, Newell PD, Gross RH, O'Toole GA. 2007. Phosphatedependent modulation of c-di-GMP levels regulates Pseudomonas fluorescens Pf0-1 biofilm formation by controlling secretion of the adhesin LapA. Mol. Microbiol. 63:656-679.
37. 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. 106:3461-3466.
38. O'Brien JA, Lahue BJ, Caro JJ, Davidson DM. 2007. The emerging infectious challenge of clostridium difficile-associated disease in Massachusetts hospitals: clinical and economic consequences. Infect. Control Hosp. Epidemiol. 28:1219 -1227.
39. Osorio CG, et al. 2005. Second-generation recombination-based in vivo expression technology for large-scale screening for Vibrio cholerae genes induced during infection of the mouse small intestine. Infect. Immun. 73:972-980.
40. Paul K, Nieto V, Carlquist WC, Blair DF, Harshey RM. 2010. The c-di-GMP binding protein YcgR controls flagellar motor direction and speed to affect chemotaxis by a "backstop brake" mechanism. Mol. Cell 38:128 -139.
41. Paul R, et al. 2004. Cell cycle-dependent dynamic localization of a bacterial response regulator with a novel di-guanylate cyclase output domain. Genes Dev. 18:715-727.
42. Pechine S, et al. 2005. Immunological properties of surface proteins of Clostridium difficile. J. Med. Microbiol. 54:193-196.
43. 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 -12870.
44. Reynolds CB, Emerson JE, de la Riva L, Fagan RP, Fairweather NF. 2011. The Clostridium difficile cell wall protein CwpV is antigenically variable between strains, but exhibits conserved aggregation-promoting function. PLoS Pathog. 7:e1002024. doi:10.1371/journal.ppat.1002024.
45. Romling U, Gomelsky M, Galperin MY. 2005. c-di-GMP: the dawning of a novel bacterial signalling system. Mol. Microbiol. 57:629-639.
46. Ross P, Mayer R, Benziman M. 1991. Cellulose biosynthesis and function in bacteria. Microbiol. Rev. 55:35-58.
47. Ross P, et al. 1986. Control of cellulose synthesis Acetobacter xylinum. A unique guanyl oligonucleotide is the immediate activator of the cellulose synthase. Carbohydr. Res. 149:101-117.
48. Ryan RP, et al. 2006. Cell-cell signaling in Xanthomonas campestris involves an HD-GYP domain protein that functions in cyclic di-GMP turnover. Proc. Natl. Acad. Sci. U. S. A. 103:6712- 6717.
49. 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: 30310-30314.
50. Ryjenkov DA, Tarutina M, Moskvin OV, Gomelsky M. 2005. Cyclic diguanylate is a ubiquitous signaling molecule in bacteria: insights into biochemistry of the GGDEF protein domain. J. Bacteriol. 187:1792-1798.
51. 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. 187:4774-4781.
52. Sebaihia M, et al. 2006. The multidrug-resistant human pathogen Clostridium difficile has a highly mobile, mosaic genome. Nat. Genet. 38:779- 786.
53. Seshasayee AS, Fraser GM, Luscombe NM. 2010. Comparative genomics of cyclic-di-GMP signalling in bacteria: post-translational regulation and catalytic activity. Nucleic Acids Res. 38:5970 -5981.
54. Shang F, et al. 2009. The Staphylococcus aureus GGDEF domainc-containing protein, GdpS, influences protein A gene expression in a cyclic diguanylic acid-independent manner. Infect. Immun. 77:2849 -2856.
55. Shimizu T, et al. 2002. Complete genome sequence of Clostridium perfringens, an anerobic flesh-eater. Proc. Natl. Acad. Sci. U. S. A. 99:996-1001.
56. Simm R, Morr M, Kader A, Nimtz M, Romling U. 2004. GGDEF and EAL domains inversely regulate cyclic di-GMP levels and transition from sessility to motility. Mol. Microbiol. 53:1123-1134.
57. Simm R, Morr M, Remminghorst U, Andersson M, Romling U. 2009. Quantitative determination of cyclic diguanosine monophosphate concentrations in nucleotide extracts of bacteria by matrix-assisted laser desorption/ ionization-time-of-flight mass spectrometry. Anal. Biochem. 386:53-58.
58. Skarin H, Håfström T, Westerberg J, Segerman B. 2011. Clostridium botulinum group III: a group with dual identity shaped by plasmids, phages and mobile elements. BMC Genomics 12:185. doi:10.1186/1471-2164-12-185.
59. Smith CJ, Markowitz SM, Macrina FL. 1981. Transferable tetracycline resistance in Clostridium difficile. Antimicrob. Agents Chemother. 19: 997-1003.
60. Sommerfeldt N, et al. 2009. Gene expression patterns and differential input into curli fimbriae regulation of all GGDEF/EAL domain proteins in Escherichia coli. Microbiology 155:1318 -1331.
61. Stabler RA, et al. 2009. Comparative genome and phenotypic analysis of Clostridium difficile 027 strains provides insight into the evolution of a hypervirulent bacterium. Genome Biol. 10:R102. doi:10.1186/gb-2009-10-9-r102.
62. Starnbach MN, Lory S. 1992. The fliA (rpoF) gene of Pseudomonas aeruginosa encodes an alternative sigma factor required for flagellin synthesis. Mol. Microbiol. 6:459-469.
63. Sudarsan N, et al. 2008. Riboswitches in eubacteria sense the second messenger cyclic di-GMP. Science 321:411- 413.
64. Tamayo R, Schild S, Pratt JT, Camilli A. 2008. Role of cyclic di-GMP during El Tor biotype Vibrio cholerae infection: characterization of the in vivo-induced cyclic di-GMP phosphodiesterase CdpA. Infect. Immun. 76: 1617-1627.
65. Tamayo R, Tischler AD, Camilli A. 2005. The EAL domain protein VieA is a cyclic diguanylate phosphodiesterase. J. Biol. Chem. 280:33324 - 33330.
66. Tasteyre A, Barc MC, Collignon A, Boureau H, Karjalainen T. 2001. Role of FliC and FliD flagellar proteins of Clostridium difficile in adherence and gut colonization. Infect. Immun. 69:7937-7940.
67. Thormann KM, et al. 2006. Control of formation and cellular detachment from Shewanella oneidensis MR-1 biofilms by cyclic di-GMP. J. Bacteriol. 188:2681-2691.
68. Tischler AD, Camilli A. 2004. Cyclic diguanylate (c-di-GMP) regulates Vibrio cholerae biofilm formation. Mol. Microbiol. 53:857- 869.
69. Tischler ADa AC. 2005. Cyclic diguanylate regulates Vibrio cholerae virulence gene expression. Infect. Immun. 73:5873-5882.
70. Tran NT, Den Hengst CD, Gomez-Escribano JP, Buttner MJ. 2011. Identification and characterization of CdgB, a diguanylate cyclase involved in developmental processes in Streptomyces coelicolor. J. Bacteriol. 193:3100 -3108.
71. Twine SM, et al. 2009. Motility and flagellar glycosylation in Clostridium difficile. J. Bacteriol. 191:7050 -7062.
72. Vial PA, et al. 1988. Characterization of enteroadherent-aggregative Escherichia coli, a putative agent of diarrheal disease. J. Infect. Dis. 158: 70-79.
73. Zogaj X, Nimtz M, Rohde M, Bokranz W, Romling U. 2001. The multicellular morphotypes of Salmonella typhimurium and Escherichia coli produce cellulose as the second component of the extracellular matrix. Mol. Microbiol. 39:1452-1463.