Regulation of biofilm formation in Salmonella enterica serovar Typhimurium

Future Microbiology

Volumn 9, Issue 11, 2014, Pages 1261-1282

  Simm, Roger ^a   Ahmad, Irfan ^b   Rhen, Mikael ^b   Guyon, Soazig Le ^b   Römling, Ute ^b  

^a OSLO UNIVERSITY HOSPITAL   (Norway)

^b KAROLINSKA INSTITUTE   (Sweden)

Author keywords

biofilm; bistability; CsgD; CsrA; cyclic di GMP; Dsb; Hfq; lytic transglycosylases; Salmonella enterica serovar Typhimurium; small RNAs

Indexed keywords

CELLULOSE; CYCLIC GMP; GLYCOSYLTRANSFERASE; PERIPLASMIC PROTEIN; REGULATOR PROTEIN; RNA BINDING PROTEIN; SMALL UNTRANSLATED RNA; TRANSCRIPTION FACTOR; BACTERIAL PROTEIN;

BACTERIAL CELL WALL; BACTERIAL METABOLISM; BACTERIAL VIRULENCE; BIOFILM; EXTRACELLULAR MATRIX; GENETIC TRANSCRIPTION; HOST; LYSIS; MORPHOTYPE; NONHUMAN; OXIDATION REDUCTION STATE; PHENOTYPE; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; REGULATORY MECHANISM; REGULON; REVIEW; SALMONELLA TYPHIMURIUM; ANIMAL; BINDING SITE; CELL WALL; GENE EXPRESSION REGULATION; GENE REGULATORY NETWORK; GENETICS; GROWTH, DEVELOPMENT AND AGING; HUMAN; METABOLISM; MICROBIOLOGY; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PATHOGENICITY; PHYSIOLOGY; SALMONELLA ENTERICA SEROVAR TYPHIMURIUM; SALMONELLOSIS; SEQUENCE ALIGNMENT; SIGNAL TRANSDUCTION; VIRULENCE;

SALMONELLA ENTERICA SUBSP. ENTERICA SEROVAR TYPHIMURIUM;

ANIMALS; BACTERIAL PROTEINS; BASE SEQUENCE; BINDING SITES; BIOFILMS; CELL WALL; GENE EXPRESSION REGULATION, BACTERIAL; GENE REGULATORY NETWORKS; HUMANS; MOLECULAR SEQUENCE DATA; RNA, SMALL UNTRANSLATED; SALMONELLA INFECTIONS; SALMONELLA TYPHIMURIUM; SEQUENCE ALIGNMENT; SIGNAL TRANSDUCTION; VIRULENCE;

EID: 84914669296     PISSN: 17460913     EISSN: 17460921     Source Type: Journal    
DOI: 10.2217/fmb.14.88     Document Type: Review

References (182)

1. Ohl ME, Miller SI. Salmonella: a model for bacterial pathogenesis. Annu. Rev. Med. 52, 259-274 (2001).
2. Rabsch W, Tschäpe H, Baümler AJ. Non-typhoidal salmonellosis: emerging problems. Microbes Infect. 3(3), 237-247 (2001).
3. Gordon MA. Salmonella infections in immunocompromised adults. J. Infect. 56(6), 413-422 (2008).
4. Shaw RE, Jones RE, Dodds RJ, Galpine JF. Biliary carrier of Salmonella Typhimurium treated by cholecystectomy. Lancet 267(6828), 71-72 (1954).
5. Levine MM, Black RE, Lanata C. Precise estimation of the numbers of chronic carriers of Salmonella Typhi in Santiago, Chile, an endemic area. J. Infect. Dis. 146(6), 724-726 (1982).
6. National Outbreak Reporting System (NORS). Foodborne Outbreak Online Database (FOOD) wwwn.cdc.gov/foodborneoutbreaks/
7. Lynch MF, Tauxe RV, Hedberg CW. The growing burden of foodborne outbreaks due to contaminated fresh produce: risks and opportunities. Epidemiol. Infect. 137(3), 307-315 (2009).
8. Sandvang D, Jensen LB, Baggesen DL, Baloda SB. Persistence of a Salmonella enterica serotype Typhimurium clone in Danish pig production units and farmhouse environment studied by pulsed field gel electrophoresis (PFGE). FEMS Microbiol. Lett. 187(1), 21-25 (2000).
9. Weigel RM, Nucera D, Qiao B et al. Testing an ecological model for transmission of Salmonella enterica in swine production ecosystems using genotyping data. Prev. Vet. Med. 81(4), 274-289 (2007).
10. Baloda SB, Christensen L, Trajcevska S. Persistence of a Salmonella enterica serovar Typhimurium DT12 clone in a piggery and in agricultural soil amended with Salmonella-contaminated slurry. Appl. Environ. Microbiol. 67(6), 2859-2862 (2001).
11. Dorr PM, Tadesse DA, Zewde BM, Fry P, Thakur S, Gebreyes WA. Longitudinal study of Salmonella dispersion and the role of environmental contamination in commercial swine production systems. Appl. Environ. Microbiol. 75(6), 1478-1486 (2009).
12. Hernandez-Reyes C, Schikora A. Salmonella, a cross-kingdom pathogen infecting humans and plants. FEMS Microbiol. Lett. 343(1), 1-7 (2013).
13. Hood SK, Zottola EA. Adherence to stainless steel by foodborne microorganisms during growth in model food systems. Int. J. Food Microbiol. 37(2-3), 145-153 (1997).
14. Prouty AM, Gunn JS. Comparative analysis of Salmonella enterica serovar Typhimurium biofilm formation on gallstones and on glass. Infect. Immun. 71(12), 7154-7158 (2003).
15. 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. 28(2), 249-264 (1998).
16. Ngwai YB, Adachi Y, Ogawa Y, Hara H. Characterization of biofilm-forming abilities of antibiotic-resistant Salmonella Typhimurium DT104 on hydrophobic abiotic surfaces. J. Microbiol. Immunol. Infect. 39(4), 278-291 (2006).
17. Lapidot A, Römling U, Yaron S. Biofilm formation and the survival of Salmonella Typhimurium on parsley. Int. J. Food Microbiol. 109(3), 229-233 (2006).
18. Cevallos-Cevallos JM, Gu G, Danyluk MD, Van Bruggen AH. Adhesion and splash dispersal of Salmonella enterica Typhimurium on tomato leaflets: effects of rdar morphotype and trichome density. Int. J. Food Microbiol. 160(1), 58-64 (2012).
19. Prouty AM, Schwesinger WH, Gunn JS. Biofilm formation and interaction with the surfaces of gallstones by Salmonella spp. Infect. Immun. 70(5), 2640-2649 (2002).
20. Boddicker JD, Ledeboer NA, Jagnow J, Jones BD, Clegg S. Differential binding to and biofilm formation on, HEp-2 cells by Salmonella enterica serovar Typhimurium is dependent upon allelic variation in the fimH gene of the fim gene cluster. Mol. Microbiol. 45(5), 1255-1265 (2002).
21. Ledeboer NA, Frye JG, Mcclelland M, Jones BD. Salmonella enterica serovar Typhimurium requires the Lpf, Pef, and Tafi fimbriae for biofilm formation on HEp-2 tissue culture cells and chicken intestinal epithelium. Infect. Immun. 74(6), 3156-3169 (2006).
22. Ledeboer NA, Jones BD. Exopolysaccharide sugars contribute to biofilm formation by Salmonella enterica serovar Typhimurium on HEp-2 cells and chicken intestinal epithelium. J. Bacteriol. 187(9), 3214-3226 (2005).
23. Watnick P, Kolter R. Biofilm, city of microbes. J. Bacteriol. 182(10), 2675-2679 (2000).
24. Stoodley P, Sauer K, Davies DG, Costerton JW. Biofilms as complex differentiated communities. Annu. Rev. Microbiol. 56, 187-209 (2002).
25. Donlan RM, Costerton JW. Biofilms: survival mechanisms of clinically relevant microorganisms. Clin. Microbiol. Rev. 15(2), 167-193 (2002).
26. Costerton JW, Stewart PS, Greenberg EP. Bacterial biofilms: a common cause of persistent infections. Science 284(5418), 1318-1322 (1999).
27. Davies D. Understanding biofilm resistance to antibacterial agents. Nat. Rev. Drug Discov. 2(2), 114-122 (2003).
28. Coetser SE, Cloete TE. Biofouling and biocorrosion in industrial water systems. Crit. Rev. Microbiol. 31(4), 213-232 (2005).
29. Van Houdt R, Michiels CW. Biofilm formation and the food industry, a focus on the bacterial outer surface. J. Appl. Microbiol. 109(4), 1117-1131 (2010).
30. Wenzel RP. Health care-associated infections: major issues in the early years of the 21st century. Clin. Infect. Dis. 45(Suppl. 1), S85-S88 (2007).
31. Hoiby N, Bjarnsholt T, Givskov M, Molin S, Ciofu O. Antibiotic resistance of bacterial biofilms. Int. J. Antimicrob. Agents 35(4), 322-332 (2010).
32. Jensen PO, Givskov M, Bjarnsholt T, Moser C. The immune system vs. Pseudomonas aeruginosa biofilms. FEMS Immunol. Med. Microbiol. 59(3), 292-305 (2010).
33. Römling U, Balsalobre C. Biofilm infections, their resilience to therapy and innovative treatment strategies. J. Intern. Med. 272(6), 541-561 (2012).
34. Aviles B, Klotz C, Eifert J, Williams R, Ponder M. Biofilms promote survival and virulence of Salmonella enterica sv. Tennessee during prolonged dry storage and after passage through an in vitro digestion system. Int. J. Food Microbiol. 162(3), 252-259 (2013).
35. Bridier A, Briandet R, Thomas V, Dubois-Brissonnet F. Resistance of bacterial biofilms to disinfectants: a review. Biofouling 27(9), 1017-1032 (2011).
36. Sutherland IW. The biofilm matrix-an immobilized but dynamic microbial environment. Trends Microbiol. 9(5), 222-227 (2001).
37. Römling U, Bian Z, Hammar M, Sierralta WD, Normark S. Curli fibers are highly conserved between Salmonella Typhimurium and Escherichia coli with respect to operon structure and regulation. J. Bacteriol. 180(3), 722-731 (1998).
38. Latasa C, Roux A, Toledo-Arana A et al. BapA, a large secreted protein required for biofilm formation and host colonization of Salmonella enterica serovar Enteritidis. Mol. Microbiol. 58(5), 1322-1339 (2005).
39. Römling U, Rohde M. Flagella modulate the multicellular behavior of Salmonella Typhimurium on the community level. FEMS Microbiol. Lett. 180(1), 91-102 (1999).
40. Zogaj X, Nimtz M, Rohde M, Bokranz W, Römling U. The multicellular morphotypes of Salmonella Typhimurium and Escherichia coli produce cellulose as the second component of the extracellular matrix. Mol. Microbiol. 39(6), 1452-1463 (2001).
41. Crawford RW, Gibson DL, Kay WW, Gunn JS. Identification of a bile-induced exopolysaccharide required for Salmonella biofilm formation on gallstone surfaces. Infect. Immun. 76(11), 5341-5349 (2008).
42. Gibson DL, White AP, Snyder SD et al. Salmonella produces an O-antigen capsule regulated by AgfD and important for environmental persistence. J. Bacteriol. 188(22), 7722-7730 (2006).
43. Wang H, Huang Y, Wu S et al. Extracellular DNA Inhibits Salmonella enterica serovar Typhimurium and S. enterica serovar Typhi biofilm development on abiotic surfaces. Curr. Microbiol. 68(2), 262-268 (2014).
44. Crull K, Rohde M, Westphal K et al. Biofilm formation by Salmonella enterica serovar Typhimurium colonizing solid tumours. Cell. Microbiol. 13(8), 1223-1233 (2011).
45. White AP, Gibson DL, Grassl GA et al. Aggregation via the red, dry, and rough morphotype is not a virulence adaptation in Salmonella enterica serovar Typhimurium. Infect. Immun. 76(3), 1048-1058 (2008).
46. Morgan E, Campbell JD, Rowe SC et al. Identification of host-specific colonization factors of Salmonella enterica serovar Typhimurium. Mol. Microbiol. 54(4), 994-1010 (2004).
47. Gonzalez-Escobedo G, Marshall JM, Gunn JS. Chronic and acute infection of the gall bladder by Salmonella Typhi: understanding the carrier state. Nat. Rev. Microbiol. 9(1), 9-14 (2011).
48. Bian Z, Brauner A, Li Y, Normark S. Expression of and cytokine activation by Escherichia coli curli fibers in human sepsis. J. Infect. Dis. 181(2), 602-612 (2000).
49. Humphries A, Deridder S, Baümler AJ. Salmonella enterica serotype Typhimurium fimbrial proteins serve as antigens during infection of mice. Infect. Immun. 73(9), 5329-5338 (2005).
50. Tukel C, Raffatellu M, Humphries AD et al. CsgA is a pathogen-associated molecular pattern of Salmonella enterica serotype Typhimurium that is recognized by Toll-like receptor 2. Mol. Microbiol. 58(1), 289-304 (2005).
51. Lamprokostopoulou A, Monteiro C, Rhen M, Römling U. Cyclic di-GMP signalling controls virulence properties of Salmonella enterica serovar Typhimurium at the mucosal lining. Environ. Microbiol. 12(1), 40-53 (2010).
52. Lapidot A, Yaron S. Transfer of Salmonella enterica serovar Typhimurium from contaminated irrigation water to parsley is dependent on curli and cellulose, the biofilm matrix components. J. Food Prot. 72(3), 618-623 (2009).
53. Gu G, Hu J, Cevallos-Cevallos JM, Richardson SM, Bartz JA, Van Bruggen AH. Internal colonization of Salmonella enterica serovar Typhimurium in tomato plants. PLoS ONE 6(11), e27340 (2011).
54. Römling U, Pesen D, Yaron S. Biofilms of Salmonella enterica. In: Salmonella: Molecular Biology and Pathogenesis. Rhen M, Maskell D, Mastroeni P, Threlfall J (Eds). Horizon Scientific Press, Wymondham, UK (2007).
55. Jonas K, Tomenius H, Kader A et al. Roles of curli, cellulose and BapA in Salmonella biofilm morphology studied by atomic force microscopy. BMC Microbiol. 7, 70 (2007).
56. Robijns SC, Roberfroid S, Van Puyvelde S et al. A GFP promoter fusion library for the study of Salmonella biofilm formation and the mode of action of biofilm inhibitors. Biofouling 30(5), 605-625 (2014).
57. Serra DO, Richter AM, Klauck G, Mika F, Hengge R. Microanatomy at cellular resolution and spatial order of physiological differentiation in a bacterial biofilm. MBIO 4(2), e00103-e00113 (2013).
58. Monds RD, O'Toole GA. The developmental model of microbial biofilms: ten years of a paradigm up for review. Trends Microbiol. 17(2), 73-87 (2009).
59. O'Toole G, Kaplan HB, Kolter R. Biofilm formation as microbial development. Annu. Rev. Microbiol. 54, 49-79 (2000).
60. Römling U, Bokranz W, Rabsch W, Zogaj X, Nimtz M, Tschäpe H. Occurrence and regulation of the multicellular morphotype in Salmonella serovars important in human disease. Int. J. Med. Microbiol. 293(4), 273-285 (2003).
61. Castelijn GA, Van Der Veen S, Zwietering MH, Moezelaar R, Abee T. Diversity in biofilm formation and production of curli fimbriae and cellulose of Salmonella Typhimurium strains of different origin in high and low nutrient medium. Biofouling 28(1), 51-63 (2012).
62. Vestby LK, Moretro T, Ballance S, Langsrud S, Nesse LL. Survival potential of wild type cellulose deficient Salmonella from the feed industry. BMC Vet. Res. 5, 43 (2009).
63. Old DC, Corneil I, Gibson LF, Thomson AD, Duguid JP. Fimbriation, pellicle formation and the amount of growth of Salmonellas in broth. J. Gen. Microbiol. 51(1), 1-16 (1968).
64. Grantcharova N, Peters V, Monteiro C, Zakikhany K, Römling U. Bistable expression of CsgD in biofilm development of Salmonella enterica serovar Typhimurium. J. Bacteriol. 192(2), 456-466 (2010).
65. Barak JD, Gorski L, Naraghi-Arani P, Charkowski AO. Salmonella enterica virulence genes are required for bacterial attachment to plant tissue. Appl. Environ. Microbiol. 71(10), 5685-5691 (2005).
66. Barak JD, Jahn CE, Gibson DL, Charkowski AO. The role of cellulose and O-antigen capsule in the colonization of plants by Salmonella enterica. Mol. Plant Microbe Interact. 20(9), 1083-1091 (2007).
67. Solano C, Garcia B, Valle J et al. Genetic analysis of Salmonella enteritidis biofilm formation: critical role of cellulose. Mol. Microbiol. 43(3), 793-808 (2002).
68. Shaw RK, Lasa I, Garcia BM et al. Cellulose mediates attachment of Salmonella enterica Serovar Typhimurium to tomatoes. Environ. Microbiol. Rep. 3(5), 569-573 (2011).
69. Brandl MT, Carter MQ, Parker CT, Chapman MR, Huynh S, Zhou Y. Salmonella biofilm formation on Aspergillus niger involves cellulose-chitin interactions. PLoS ONE 6(10), e25553 (2011).
70. Balbontín R, Vlamakis H, Kolter R. Mutualistic interaction between Salmonella enterica and Aspergillus niger and its effects on Zea mays colonization. Microb. Biotechnol. 7(6), 589-600 (2014).
71. Robbe-Saule V, Jaumouille V, Prevost MC et al. Crl activates transcription initiation of RpoS-regulated genes involved in the multicellular behavior of Salmonella enterica serovar Typhimurium. J. Bacteriol. 188(11), 3983-3994 (2006).
72. Typas A, Barembruch C, Possling A, Hengge R. Stationary phase reorganisation of the Escherichia coli transcription machinery by Crl protein, a fine-tuner of sigmas activity and levels. EMBO J. 26(6), 1569-1578 (2007).
73. Bougdour A, Lelong C, Geiselmann J. Crl, a low temperature-induced protein in Escherichia coli that binds directly to the stationary phase sigma subunit of RNA polymerase. J. Biol. Chem. 279(19), 19540-19550 (2004).
74. White AP, Weljie AM, Apel D et al. A global metabolic shift is linked to Salmonella multicellular development. PLoS ONE 5(7), e11814 (2010).
75. Hamilton S, Bongaerts RJ, Mulholland F et al. The transcriptional programme of Salmonella enterica serovar Typhimurium reveals a key role for tryptophan metabolism in biofilms. BMC Genomics 10, 599 (2009).
76. Zakikhany K, Harrington CR, Nimtz M, Hinton JC, Römling U. Unphosphorylated CsgD controls biofilm formation in Salmonella enterica serovar Typhimurium. Mol. Microbiol. 77(3), 771-786 (2010).
77. Römling U, Rohde M, Olsen A, Normark S, Reinköster J. AgfD, the checkpoint of multicellular and aggregative behaviour in Salmonella typhimurium regulates at least two independent pathways. Mol. Microbiol. 36(1), 10-23 (2000).
78. 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. 53(4), 1123-1134 (2004).
79. Ross P, Weinhouse H, Aloni Y et al. Regulation of cellulose synthesis in Acetobacter xylinum by cyclic diguanylic acid. Nature 325(6101), 279-281 (1987).
80. 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. 281(41), 30310-30314 (2006).
81. Morgan JL, Strumillo J, Zimmer J. Crystallographic snapshot of cellulose synthesis and membrane translocation. Nature 493(7431), 181-186 (2013).
82. Donlan RM. Biofilms: microbial life on surfaces. Emerg. Infect. Dis. 8(9), 881-890 (2002).
83. Gerstel U, Park C, Römling U. Complexregulation of csgD promoter activity by globalregulatory proteins. Mol. Microbiol. 49(3),639-654 (2003).
84. Gerstel U, Kolb A, Römling U. Regulatorycomponents at the csgD promoter-additional roles for OmpR and integrationhost factor and role of the 5′ untranslatedregion. FEMS Microbiol. Lett. 261(1),109-117 (2006).
85. Ogasawara H, Yamamoto K, Ishihama A.Role of the biofilm master regulator CsgD incross-regulation between biofilm formationand flagellar synthesis. J. Bacteriol. 193(10),2587-2597 (2011).
86. Gerstel U, Römling U. The csgD promoter, acontrol unit for biofilm formation inSalmonella Typhimurium. Res. Microbiol.154(10), 659-667 (2003).
87. Brown PK, Dozois CM, Nickerson CA,Zuppardo A, Terlonge J, Curtiss R 3rd. MlrA,a novel regulator of curli (AgF) andextracellular matrix synthesis by Escherichiacoli and Salmonella enterica serovarTyphimurium. Mol. Microbiol. 41(2),349-363 (2001).
88. Ogasawara H, Yamamoto K, Ishihama A.Regulatory role of MlrA in transcriptionactivation of csgD, the master regulator ofbiofilm formation in Escherichia coli. FEMSMicrobiol. Lett. 312(2), 160-168 (2010).
89. Ogasawara H, Shinohara S, Yamamoto K,Ishihama A. Novel regulation targets of themetal-response BasS-BasR two componentsystem of Escherichia coli. Microbiology158(Pt 6), 1482-1492 (2012).
90. Reshamwala SM, Noronha SB. Biofilmformation in Escherichia coli cra mutants isimpaired due to down-regulation of curlibiosynthesis. Arch. Microbiol. 193(10),711-722 (2011).
91. Saier MH Jr, Ramseier TM. The cataboliterepressor/activator (Cra) protein of entericbacteria. J. Bacteriol. 178(12), 3411-3417(1996).
92. Zheng D, Constantinidou C, Hobman JL,Minchin SD. Identification of the CRPregulon using in vitro and in vivotranscriptional profiling. Nucleic Acids Res.32(19), 5874-5893 (2004).
93. Brombacher E, Dorel C, Zehnder AJ, LandiniP. The curli biosynthesis regulator CsgDco-ordinates the expression of both positiveand negative determinants for biofilmformation in Escherichia coli. Microbiology149(Pt 10), 2847-2857 (2003).
94. Ogasawara H, Yamada K, Kori A, YamamotoK, Ishihama A. Regulation of the Escherichiacoli csgD promoter: interplay between fivetranscription factors. Microbiology 156(Pt 8),2470-2483 (2010).
95. Pogliano J, Lynch AS, Belin D, Lin EC,Beckwith J. Regulation of Escherichia coli cellenvelope proteins involved in protein foldingand degradation by the Cpx two componentsystem. Genes Dev. 11(9), 1169-1182 (1997).
96. Yamamoto K, Ishihama A. Characterizationof copper-inducible promoters regulated byCpxA/CpxR in Escherichia coli. Biosci.Biotechnol. Biochem. 70(7), 1688-1695(2006).
97. Jubelin G, Vianney A, Beloin C et al.CpxR/OmpR interplay regulates curli geneexpression in response to osmolarity inEscherichia coli. J. Bacteriol. 187(6),2038-2049 (2005).
98. Shimada T, Katayama Y, Kawakita S et al.A novel regulator RcdA of the csgD geneencoding the master regulator of biofilmformation in Escherichia coli. Microbiologyopen1(4), 381-394 (2012).
99. Ogasawara H, Hasegawa A, Kanda E, MikiT, Yamamoto K, Ishihama A. GenomicSELEX search for target promoters under thecontrol of the PhoQP-RstBA signal relaycascade. J. Bacteriol. 189(13), 4791-4799(2007).
100. Shimada T, Fujita N, Maeda M, Ishihama A.Systematic search for the Cra-bindingpromoters using genomic SELEX system.Genes Cells 10(9), 907-918 (2005).
101. Chen HD, Jewett MW, Groisman EA.An allele of an ancestral transcription factordependent on a horizontally acquired geneproduct. PLoS Genet. 8(12), e1003060(2012).
102. Allen JH, Utley M, Van Den Bosch H et al.A functional cra gene is required forSalmonella enterica serovar Typhimuriumvirulence in BALB/c mice. Infect. Immun.68(6), 3772-3775 (2000).
103. Wolfe AJ, Chang DE, Walker JD et al.Evidence that acetyl phosphate functions asa global signal during biofilm development.Mol. Microbiol. 48(4), 977-988 (2003).
104. Monteiro C, Papenfort K, Hentrich K et al.Hfq and Hfq-dependent small RNAs aremajor contributors to multicellulardevelopment in Salmonella enterica serovarTyphimurium. RNA Biol. 9(4), 489-502(2012).
105. Brown L, Elliott T. Efficient translation of theRpoS sigma factor in SalmonellaTyphimurium requires host factor I, anRNA-binding protein encoded by the hfqgene. J. Bacteriol. 178(13), 3763-3770 (1996).
106. Sittka A, Lucchini S, Papenfort K et al. Deepsequencing analysis of small noncoding RNAand mRNA targets of the global posttranscriptionalregulator, Hfq. PLoS Genet.4(8), e1000163 (2008).
107. Papenfort K, Said N, Welsink T, Lucchini S,Hinton JC, Vogel J. Specific and pleiotropicpatterns of mRNA regulation by ArcZ, aconserved, Hfq-dependent small RNA. Mol.Microbiol. 74(1), 139-158 (2009).
108. De Lay N, Gottesman S. A complex networkof small non-coding RNAs regulate motilityin Escherichia coli. Mol Microbiol. . 86(3),524-538 (2012).
109. Latasa C, Garcia B, Echeverz M et al.Salmonella biofilm development depends onthe phosphorylation status of RcsB.J. Bacteriol. 194(14), 3708-3722 (2012).
110. Holmqvist E, Reimegard J, Sterk M,Grantcharova N, Römling U, Wagner EG.Two antisense RNAs target the transcriptionalregulator CsgD to inhibit curli synthesis.EMBO J. 29(11), 1840-1850 (2010).
111. Mika F, Busse S, Possling A et al. Targeting ofcsgD by the small regulatory RNA RprAlinks stationary phase, biofilm formation and cell envelope stress in Escherichia coli. Mol. Microbiol. 84(1), 51-65 (2012).
112. Bordeau V, Felden B. Curli synthesis andbiofilm formation in enteric bacteria arecontrolled by a dynamic small RNA modulemade up of a pseudoknot assisted by an RNAchaperone. Nucleic Acids Res. 42(7),4682-4696 (2014).
113. Jorgensen MG, Nielsen JS, Boysen A, FranchT, Moller-Jensen J, Valentin-Hansen P. Smallregulatory RNAs control the multi-cellularadhesive lifestyle of Escherichia coli. Mol.Microbiol. 84(1), 36-50 (2012).
114. Sato K, Hamada M, Asai K, Mituyama T.CENTROIDFOLD: a web server for RNAsecondary structure prediction. Nucleic AcidsRes. 37(Web Server issue), W277-W280(2009).
115. De Keersmaecker SC, Varszegi C, van BoxelN et al. Chemical synthesis of (S)-4,5-dihydroxy-2,3-pentanedione, a bacterialsignal molecule precursor, and validation ofits activity in Salmonella Typhimurium.J. Biol. Chem. 280(20), 19563-19568 (2005).
116. Udekwu KI, Darfeuille F, Vogel J, ReimegardJ, Holmqvist E, Wagner EG. Hfq-dependentregulation of OmpA synthesis is mediated byan antisense RNA. Genes Dev. 19(19),2355-2366 (2005).
117. Rasmussen AA, Eriksen M, Gilany K et al. Regulation of ompA mRNA stability: the role of a small regulatory RNA in growth phase-dependent control. Mol. Microbiol. 58(5), 1421-1429 (2005).
118. Coornaert A, Lu A, Mandin P, Springer M, Gottesman S, Guillier M. MicA sRNA links the PhoP regulon to cell envelope stress. Mol. Microbiol. 76(2), 467-479 (2010).
119. Kint G, De Coster D, Marchal K, Vanderleyden J, De Keersmaecker SC. The small regulatory RNA molecule MicA is involved in Salmonella enterica serovar Typhimurium biofilm formation. BMC Microbiol. 10, 276 (2010).
120. Boehm A, Vogel J. The csgD mRNA as a hub for signal integration via multiple small RNAs. Mol. Microbiol. 84(1), 1-5 (2012).
121. Mika F, Hengge R. Small Regulatory RNAs in the Control of Motility and Biofilm Formation in E. coli and Salmonella. Int. J. Mol. Sci. 14(3), 4560-4579 (2013).
122. Van Puyvelde S, Steenackers HP, Vanderleyden J. Small RNAs regulating biofilm formation and outer membrane homeostasis. RNA Biol. 10(2), 185-191 (2013).
123. Cabeza ML, Aguirre A, Soncini FC, Vescovi EG. Induction of RpoS degradation by the two component system regulator RstA in Salmonella enterica. J. Bacteriol. 189(20), 7335-7342 (2007).
124. Lawhon SD, Frye JG, Suyemoto M, Porwollik S, Mcclelland M, Altier C. Global regulation by CsrA in Salmonella Typhimurium. Mol. Microbiol. 48(6), 1633-1645 (2003).
125. Edwards AN, Patterson-Fortin LM, Vakulskas CA et al. Circuitry linking the Csr and stringent response global regulatory systems. Mol. Microbiol. 80(6), 1561-1580 (2011).
126. Babitzke P, Romeo T. CsrB sRNA family: sequestration of RNA-binding regulatory proteins. Curr. Opin. Microbiol. 10(2), 156-163 (2007).
127. Lapouge K, Schubert M, Allain FH, Haas D. Gac/Rsm signal transduction pathway of gamma-proteobacteria: from RNA recognition to regulation of social behaviour. Mol. Microbiol. 67(2), 241-253 (2008).
128. Lucchetti-Miganeh C, Burrowes E, Baysse C, Ermel G. The post-transcriptional regulator CsrA plays a central role in the adaptation of bacterial pathogens to different stages of infection in animal hosts. Microbiology 154(Pt 1), 16-29 (2008).
129. Romeo T, Vakulskas CA, Babitzke P. Post-transcriptional regulation on a global scale: form and function of Csr/Rsm systems. Environ. Microbiol. 15(2), 313-324 (2013).
130. Liu MY, Gui G, Wei B et al. The RNA molecule CsrB binds to the global regulatory protein CsrA and antagonizes its activity in Escherichia coli. J. Biol. Chem. 272(28), 17502-17510 (1997).
131. Suzuki K, Wang X, Weilbacher T et al. Regulatory circuitry of the CsrA/CsrB and BarA/UvrY systems of Escherichia coli. J. Bacteriol. 184(18), 5130-5140 (2002).
132. Jonas K, Melefors, O. The Escherichia coli CsrB and CsrC small RNAs are strongly induced during growth in nutrient-poor medium. FEMS Microbiol. Lett. 297(1), 80-86 (2009).
133. Suzuki K, Babitzke P, Kushner SR, Romeo T. Identification of a novel regulatory protein (CsrD) that targets the global regulatory RNAs CsrB and CsrC for degradation by RNase E. Genes Dev. 20(18), 2605-2617 (2006).
134. Jonas K, Edwards AN, Ahmad I, Romeo T, Römling U, Melefors Ö. Complex regulatory network encompassing the Csr, c-di-GMP and motility systems of Salmonella Typhimurium. Environ. Microbiol. 12(2), 524-540 (2010).
135. Jonas K, Edwards AN, Simm R, Romeo T, Römling U, Melefors Ö. The RNA binding protein CsrA controls cyclic di-GMP metabolism by directly regulating the expression of GGDEF proteins. Mol. Microbiol. 70(1), 236-257 (2008).
136. Sterzenbach T, Nguyen KT, Nuccio SP et al. A novel CsrA titration mechanism regulates fimbrial gene expression in Salmonella Typhimurium. EMBO J. 32(21), 2872-2883 (2013).
137. Monteiro C, Fang X, Ahmad I, Gomelsky M, Römling U. Regulation of biofilm components in Salmonella enterica serovar Typhimurium by lytic transglycosylases involved in cell wall turnover. J. Bacteriol. 193(23), 6443-6451 (2011).
138. Lindquist S, Weston-Hafer K, Schmidt H et al. AmpG, a signal transducer in chromosomal beta-lactamase induction. Mol. Microbiol. 9(4), 703-715 (1993).
139. Jacobs C, Frere JM, Normark S. Cytosolic intermediates for cell wall biosynthesis and degradation control inducible beta-lactam resistance in gram-negative bacteria. Cell 88(6), 823-832 (1997).
140. Jacobs C, Huang LJ, Bartowsky E, Normark S, Park JT. Bacterial cell wall recycling provides cytosolic muropeptides as effectors for beta-lactamase induction. EMBO J. 13(19), 4684-4694 (1994).
141. Denoncin K, Collet JF. Disulfide bond formation in the bacterial periplasm: major achievements and challenges ahead. Antioxid. Redox Signal. 19(1), 63-71 (2013).
142. Heras B, Totsika M, Jarrott R et al. Structural and functional characterization of three DsbA paralogues from Salmonella enterica serovar Typhimurium. J. Biol. Chem. 285(24), 18423-18432 (2010).
143. Anwar N, Rouf SF, Römling U, Rhen M et al. Modulation of biofilm-formation in Salmonella enterica serovar Typhimurium by the periplasmic DsbA/DsbB oxidoreductase system requires the GGDEF-EAL domain protein STM3615. PLoS ONE 9(8), e106095 (2014).
144. Hufnagel DA, DePas WH, Chapman MR. The disulfide bonding system suppresses CsgD-independent cellulose production in Escherichia coli. J. Bacteriol. 196(21), 3690-3699 (2014).
145. Römling U, Galperin MY, Gomelsky M. Cyclic di-GMP: the first 25 years of a universal bacterial second messenger. Microbiol. Mol. Biol. Rev. 77(1), 1-52 (2013).
146. Paul R, Weiser S, Amiot NC et al. Cell cycle-dependent dynamic localization of a bacterial response regulator with a novel di-guanylate cyclase output domain. Genes Dev. 18(6), 715-727 (2004).
147. Hickman JW, Tifrea DF, Harwood CS. A chemosensory system that regulates biofilm formation through modulation of cyclic diguanylate levels. Proc. Natl Acad. Sci. USA 102(40), 14422-14427 (2005).
148. Ryjenkov DA, Tarutina M, Moskvin OV, Gomelsky M. Cyclic diguanylate is a ubiquitous signaling molecule in bacteria: insights into biochemistry of the GGDEF protein domain. J. Bacteriol. 187(5), 1792-1798 (2005).
149. 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. 280(35), 30829-30837 (2005).
150. Schmidt AJ, Ryjenkov DA, Gomelsky M. The ubiquitous protein domain EAL is a cyclic diguanylate-specific phosphodiesterase: enzymatically active and inactive EAL domains. J. Bacteriol. 187(14), 4774-4781 (2005).
151. Tamayo R, Tischler AD, Camilli A. The EAL domain protein VieA is a cyclic diguanylate phosphodiesterase. J. Biol. Chem. 280(39), 33324-33330 (2005).
152. Ryan RP, Fouhy Y, Lucey JF et al. Cell-cell signaling in Xanthomonas campestris involves an HD-GYP domain protein that functions in cyclic di-GMP turnover. Proc. Natl Acad. Sci. USA 103(17), 6712-6717 (2006).
153. Römling U. Characterization of the rdar morphotype, a multicellular behaviour in Enterobacteriaceae. Cell. Mol. Life Sci. 62(11), 1234-1246 (2005).
154. Ahmad I, Lamprokostopoulou A, Le Guyon S et al. Complex c-di-GMP signaling networks mediate transition between virulence properties and biofilm formation in Salmonella enterica serovar Typhimurium. PLoS ONE 6(12), e28351 (2011).
155. Simm R, Lusch A, Kader A, Andersson M, Römling U. Role of EAL-containing proteins in multicellular behavior of Salmonella enterica serovar Typhimurium. J. Bacteriol. 189(9), 3613-3623 (2007).
156. 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. 60(3), 602-616 (2006).
157. Simm R, Morr M, Remminghorst U, Andersson M, Römling U. 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(1), 53-58 (2009).
158. Solano C, Garcia B, Latasa C et al. Genetic reductionist approach for dissecting individual roles of GGDEF proteins within the c-di-GMP signaling network in Salmonella. Proc. Natl Acad. Sci. USA 106(19), 7997-8002 (2009).
159. Garcia B, Latasa C, Solano C, Garcia-Del Portillo F, Gamazo C, Lasa I. Role of the GGDEF protein family in Salmonella cellulose biosynthesis and biofilm formation. Mol. Microbiol. 54(1), 264-277 (2004).
160. Le Guyon S, Simm R, Rhen M, Römling U. Dissecting the c-di-GMP signaling network regulating motility in Salmonella enterica serovar Typhimurium. Environ. Microbiol. doi:10.1111/1462-2920.12580 (2014) (Epub ahead of print).
161. Ahmad I, Wigren E, Le Guyon S et al. The EAL-like protein STM1697 regulates virulence phenotypes, motility and biofilm formation in Salmonella Typhimurium. Mol. Microbiol. 90(6), 1216-1232 (2013).
162. Hisert KB, Maccoss M, Shiloh MU 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. 56(5), 1234-1245 (2005).
163. Wozniak CE, Lee C, Hughes KT. T-POP array identifies EcnR and PefI-SrgD as novel regulators of flagellar gene expression. J. Bacteriol. 191(5), 1498-1508 (2009).
164. Zheng Y, Sambou T, Bogomolnaya LM, Cirillo JD, Mcclelland M, Andrews-Polymenis H. The EAL domain containing protein STM2215 (rtn) is needed during Salmonella infection and has cyclic di-GMP phosphodiesterase activity. Mol. Microbiol. 89(3), 403-419 (2013).
165. Santiviago CA, Reynolds MM, Porwollik S et al. Analysis of pools of targeted Salmonella deletion mutants identifies novel genes affecting fitness during competitive infection in mice. PLoS Pathog. 5(7), e1000477 (2009).
166. Weber H, Pesavento C, Possling A, Tischendorf G, Hengge R. Cyclic-di-GMP-mediated signalling within the sigma network of Escherichia coli. Mol. Microbiol. 62(4), 1014-1034 (2006).
167. Krasteva PV, Fong JC, Shikuma NJ et al. Vibrio cholerae VpsT regulates matrix production and motility by directly sensing cyclic di-GMP. Science 327(5967), 866-868 (2010).
168. Omadjela O, Narahari A, Strumillo J et al. BcsA and BcsB form the catalytically active core of bacterial cellulose synthase sufficient for in vitro cellulose synthesis. Proc. Natl Acad. Sci. USA 110(44), 17856-17861 (2013).
169. Benach J, Swaminathan SS, Tamayo R et al. The structural basis of cyclic diguanylate signal transduction by PilZ domains. EMBO J. 26(24), 5153-5166 (2007).
170. 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 38(1), 128-139 (2010).
171. Pultz IS, Christen M, Kulasekara HD, Kennard A, Kulasekara B, Miller SI. The response threshold of Salmonella PilZ domain proteins is determined by their binding affinities for c-di-GMP. Mol. Microbiol. 86(6), 1424-1440 (2012).
172. Zorraquino V, Garcia B, Latasa C et al. Coordinated cyclic-di-GMP repression of Salmonella motility through YcgR and cellulose. J. Bacteriol. 195(3), 417-428 (2013).
173. Fang X, Ahmad I, Blanka A et al. GIL, a new c-di-GMP binding protein domain involved in cellulose synthesis regulation in Enterobacteriaceae. Mol. Microbiol. doi:10.1111/mmi.12672 (2014) (Epub ahead of print).
174. Wada T, Morizane T, Abo T, Tominaga A, Inoue-Tanaka K, Kutsukake K. EAL domain protein YdiV acts as an anti-FlhD4C2 factor responsible for nutritional control of the flagellar regulon in Salmonella enterica Serovar Typhimurium. J. Bacteriol. 193(7), 1600-1611 (2011).
175. Takaya A, Erhardt M, Karata K, Winterberg K, Yamamoto T, Hughes KT. YdiV: a dual function protein that targets FlhDC for ClpXP-dependent degradation by promoting release of DNA-bound FlhDC complex. Mol. Microbiol. 83(6), 1268-1284 (2012).
176. Dudin O, Geiselmann J, Ogasawara H, Ishihama A, Lacour S. Repression of flagellar genes in exponential phase by CsgD and CpxR, two crucial modulators of Escherichia coli biofilm formation. J. Bacteriol. 196(3), 707-715 (2014).
177. Galan JE. Salmonella interactions with host cells: type III secretion at work. Annu. Rev. Cell Dev. Biol. 17, 53-86 (2001).
178. Ehrbar K, Mirold S, Friebel A, Stender S, Hardt WD. Characterization of effector proteins translocated via the SPI1 type III secretion system of Salmonella Typhimurium. Int. J. Med. Microbiol. 291(6-7), 479-485 (2002).
179. Hanisch J, Ehinger J, Ladwein M et al. Molecular dissection of Salmonella-induced membrane ruffling versus invasion. Cell. Microbiol. 12(1), 84-98 (2010).
180. Tukel C, Nishimori JH, Wilson RP et al. Toll-like receptors 1 and 2 cooperatively mediate immune responses to curli, a common amyloid from enterobacterial biofilms. Cell. Microbiol. 12(10), 1495-1505 (2010).
181. Wang X, Rochon M, Lamprokostopoulou A, Lünsdorf H, Nimtz M, Römling U. Impact of biofilm matrix components on interaction of commensal Escherichia coli with the gastrointestinal cell line HT-29. Cell. Mol. Life Sci. 63(19-20), 2352-2363 (2006).
182. Steenackers H, Hermans K, Vanderleyden J, De Keersmaecker S. Salmonella Biofilms: an overview on occurrence, regulation and eradication. Food Res. Int. 45, 502-531 (2012).