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Volume 160, Issue 9

Sulfate assimilation pathway intermediate phosphoadenosine 5′-phosphosulfate acts as a signal molecule affecting production of curli fibres in Free

Abstract

The enterobacterium can utilize a variety of molecules as sulfur sources, including cysteine, sulfate, thiosulfate and organosulfonates. An intermediate of the sulfate assimilation pathway, adenosine 5′-phosphosulfate (APS), also acts as a signal molecule regulating the utilization of different sulfur sources. In this work, we show that inactivation of the gene, leading to accumulation of phosphoadenosine 5′-phosphosulfate (PAPS), also an intermediate of the sulfate assimilation pathway, results in increased surface adhesion and cell aggregation by activating the expression of the curli-encoding operon. In contrast, curli production was unaffected by the inactivation of any other gene belonging to the sulfate assimilation pathway. Overexpression of the gene downregulated transcription, further suggesting a link between intracellular PAPS levels and curli gene expression. In addition to curli components, the Flu, OmpX and Slp proteins were also found in increased amounts in the outer membrane compartment of the mutant; deletion of the corresponding genes suggested that these proteins also contribute to surface adhesion and cell surface properties in this strain. Our results indicate that, similar to APS, PAPS also acts as a signal molecule, albeit with a distinct mechanism and role: whilst APS regulates organosulfonate utilization, PAPS would couple availability of sulfur sources to remodulation of the cell surface, as part of a more global effect on cell physiology.

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2014-09-01
2024-04-26
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References

  1. Alexander D. M., St John A. C. ( 1994). Characterization of the carbon starvation-inducible and stationary phase-inducible gene slp encoding an outer membrane lipoprotein in Escherichia coli. Mol Microbiol 11:1059–1071 [View Article][PubMed]
     [Google Scholar]
  2. Barnhart M. M., Lynem J., Chapman M. R. ( 2006). GlcNAc-6P levels modulate the expression of curli fibers by Escherichia coli. J Bacteriol 188:5212–5219 [View Article][PubMed]
     [Google Scholar]
  3. Berendt U., Haverkamp T., Prior A., Schwenn J. D. ( 1995). Reaction mechanism of thioredoxin: 3′-phospho-adenylylsulfate reductase investigated by site-directed mutagenesis. Eur J Biochem 233:347–356 [View Article][PubMed]
     [Google Scholar]
  4. Blattner F. R., Plunkett G. III, Bloch C. A., Perna N. T., Burland V., Riley M., Collado-Vides J., Glasner J. D., Rode C. K. & other authors ( 1997). The complete genome sequence of Escherichia coli K-12. Science 277:1453–1462 [View Article][PubMed]
     [Google Scholar]
  5. Bougdour A., Lelong C., Geiselmann J. ( 2004). Crl, a low temperature-induced protein in Escherichia coli that binds directly to the stationary phase sigma subunit of RNA polymerase. J Biol Chem 279:19540–19550 [View Article][PubMed]
     [Google Scholar]
  6. Brombacher E., Baratto A., Dorel C., Landini P. ( 2006). Gene expression regulation by the curli activator CsgD protein: modulation of cellulose biosynthesis and control of negative determinants for microbial adhesion. J Bacteriol 188:2027–2037 [View Article][PubMed]
     [Google Scholar]
  7. Brown P. K., Dozois C. M., Nickerson C. A., Zuppardo A., Terlonge J., Curtiss R. III ( 2001). MlrA, a novel regulator of curli (AgF) and extracellular matrix synthesis by Escherichia coli and Salmonella enterica serovar Typhimurium. Mol Microbiol 41:349–363 [View Article][PubMed]
     [Google Scholar]
  8. Bykowski T., van der Ploeg J. R., Iwanicka-Nowicka R., Hryniewicz M. M. ( 2002). The switch from inorganic to organic sulphur assimilation in Escherichia coli: adenosine 5′-phosphosulphate (APS) as a signalling molecule for sulphate excess. Mol Microbiol 43:1347–1358 [View Article][PubMed]
     [Google Scholar]
  9. Carzaniga T., Antoniani D., Dehò G., Briani F., Landini P. ( 2012). The RNA processing enzyme polynucleotide phosphorylase negatively controls biofilm formation by repressing poly-N-acetylglucosamine (PNAG) production in Escherichia coli C. BMC Microbiol 12:270 [View Article][PubMed]
     [Google Scholar]
  10. Comunian C., Rusconi F., De Palma A., Brunetti P., Catalucci D., Mauri P. L. ( 2011). A comparative MudPIT analysis identifies different expression profiles in heart compartments. Proteomics 11:2320–2328 [View Article][PubMed]
     [Google Scholar]
  11. Cookson A. L., Cooley W. A., Woodward M. J. ( 2002). The role of type 1 and curli fimbriae of Shiga toxin-producing Escherichia coli in adherence to abiotic surfaces. Int J Med Microbiol 292:195–205 [View Article][PubMed]
     [Google Scholar]
  12. Danese P. N., Pratt L. A., Dove S. L., Kolter R. ( 2000). The outer membrane protein, antigen 43, mediates cell-to-cell interactions within Escherichia coli biofilms. Mol Microbiol 37:424–432 [View Article][PubMed]
     [Google Scholar]
  13. Datsenko K. A., Wanner B. L. ( 2000). One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci U S A 97:6640–6645 [View Article][PubMed]
     [Google Scholar]
  14. Domka J., Lee J., Bansal T., Wood T. K. ( 2007). Temporal gene-expression in Escherichia coli K-12 biofilms. Environ Microbiol 9:332–346 [View Article][PubMed]
     [Google Scholar]
  15. Dorel C., Vidal O., Prigent-Combaret C., Vallet I., Lejeune P. ( 1999). Involvement of the Cpx signal transduction pathway of E. coli in biofilm formation. FEMS Microbiol Lett 178:169–175 [View Article][PubMed]
     [Google Scholar]
  16. DuBois M., Gilles K. A., Hamilton J. K., Rebers P. A., Smith F. ( 1956). Colorimetric method for determination of sugars and related substances. Anal Chem 28:350–356 [View Article]
     [Google Scholar]
  17. Garavaglia M., Rossi E., Landini P. ( 2012). The pyrimidine nucleotide biosynthetic pathway modulates production of biofilm determinants in Escherichia coli.. PLoS ONE 7:e31252 [View Article][PubMed]
     [Google Scholar]
  18. Gerstel U., Römling U. ( 2001). Oxygen tension and nutrient starvation are major signals that regulate agfD promoter activity and expression of the multicellular morphotype in Salmonella typhimurium. Environ Microbiol 3:638–648 [View Article][PubMed]
     [Google Scholar]
  19. Gerstel U., Römling U. ( 2003). The csgD promoter, a control unit for biofilm formation in Salmonella typhimurium. Res Microbiol 154:659–667 [View Article][PubMed]
     [Google Scholar]
  20. Gerstel U., Park C., Römling U. ( 2003). Complex regulation of csgD promoter activity by global regulatory proteins. Mol Microbiol 49:639–654 [View Article][PubMed]
     [Google Scholar]
  21. Gualdi L., Tagliabue L., Landini P. ( 2007). Biofilm formation-gene expression relay system in Escherichia coli: modulation of sigmaS-dependent gene expression by the CsgD regulatory protein via sigmaS protein stabilization. J Bacteriol 189:8034–8043 [View Article][PubMed]
     [Google Scholar]
  22. Hammar M., Arnqvist A., Bian Z., Olsén A., Normark S. ( 1995). Expression of two csg operons is required for production of fibronectin- and Congo red-binding curli polymers in Escherichia coli K-12. Mol Microbiol 18:661–670 [View Article][PubMed]
     [Google Scholar]
  23. Harrington B. J., Raper K. B. ( 1968). Use of a fluorescent brightener to demonstrate cellulose in the cellular slime molds. Appl Microbiol 16:106–113[PubMed]
     [Google Scholar]
  24. Hung D. L., Raivio T. L., Jones C. H., Silhavy T. J., Hultgren S. J. ( 2001). Cpx signaling pathway monitors biogenesis and affects assembly and expression of P pili. EMBO J 20:1508–1518 [View Article][PubMed]
     [Google Scholar]
  25. Imperi F., Tiburzi F., Fimia G. M., Visca P. ( 2010). Transcriptional control of the pvdS iron starvation sigma factor gene by the master regulator of sulfur metabolism CysB in Pseudomonas aeruginosa. Environ Microbiol 12:1630–1642[PubMed]
     [Google Scholar]
  26. Jackson D. W., Simecka J. W., Romeo T. ( 2002). Catabolite repression of Escherichia coli biofilm formation. J Bacteriol 184:3406–3410 [View Article][PubMed]
     [Google Scholar]
  27. Kader A., Simm R., Gerstel U., Morr M., Römling U. ( 2006). Hierarchical involvement of various GGDEF domain proteins in rdar morphotype development of Salmonella enterica serovar Typhimurium. Mol Microbiol 60:602–616 [View Article][PubMed]
     [Google Scholar]
  28. Kredich N. M. ( 1992). The molecular basis for positive regulation of cys promoters in Salmonella typhimurium and Escherichia coli. Mol Microbiol 6:2747–2753 [View Article][PubMed]
     [Google Scholar]
  29. Liu C., Martin E., Leyh T. S. ( 1994). GTPase activation of ATP sulfurylase: the mechanism. Biochemistry 33:2042–2047 [View Article][PubMed]
     [Google Scholar]
  30. Mauri P., Dehò G. ( 2008). A proteomic approach to the analysis of RNA degradosome composition in Escherichia coli. Methods Enzymol 447:99–117 [View Article][PubMed]
     [Google Scholar]
  31. Mauri P., Scarpa A., Nascimbeni A. C., Benazzi L., Parmagnani E., Mafficini A., Della Peruta M., Bassi C., Miyazaki K., Sorio C. ( 2005). Identification of proteins released by pancreatic cancer cells by multidimensional protein identification technology: a strategy for identification of novel cancer markers. FASEB J 19:1125–1127[PubMed]
     [Google Scholar]
  32. McManus H. R., Dove S. L. ( 2011). The CgrA and CgrC proteins form a complex that positively regulates cupA fimbrial gene expression in Pseudomonas aeruginosa. J Bacteriol 193:6152–6161 [View Article][PubMed]
     [Google Scholar]
  33. Mechold U., Ogryzko V., Ngo S., Danchin A. ( 2006). Oligoribonuclease is a common downstream target of lithium-induced pAp accumulation in Escherichia coli and human cells. Nucleic Acids Res 34:2364–2373 [View Article][PubMed]
     [Google Scholar]
  34. Mecsas J., Welch R., Erickson J. W., Gross C. A. ( 1995). Identification and characterization of an outer membrane protein, OmpX, in Escherichia coli that is homologous to a family of outer membrane proteins including Ail of Yersinia enterocolitica. J Bacteriol 177:799–804[PubMed]
     [Google Scholar]
  35. Mika F., Hengge R. ( 2013). Small regulatory RNAs in the control of motility and biofilm formation in E. coli and Salmonella. Int J Mol Sci 14:4560–4579 [View Article][PubMed]
     [Google Scholar]
  36. Mikkelsen H., Sivaneson M., Filloux A. ( 2011). Key two-component regulatory systems that control biofilm formation in Pseudomonas aeruginosa. Environ Microbiol 13:1666–1681 [View Article][PubMed]
     [Google Scholar]
  37. Neidhardt F. C., Bloch P. L., Smith D. F. ( 1974). Culture medium for enterobacteria. J Bacteriol 119:736–747[PubMed]
     [Google Scholar]
  38. Otto K., Hermansson M. ( 2004). Inactivation of ompX causes increased interactions of type 1 fimbriated Escherichia coli with abiotic surfaces. J Bacteriol 186:226–234 [View Article][PubMed]
     [Google Scholar]
  39. Palma C.-A., Samorì P., Cecchini M. ( 2010). Atomistic simulations of 2D bicomponent self-assembly: from molecular recognition to self-healing. J Am Chem Soc 132:17880–17885 [View Article][PubMed]
     [Google Scholar]
  40. Plumbridge J. A. ( 1991). Repression and induction of the nag regulon of Escherichia coli K-12: the roles of nagC and nagA in maintenance of the uninduced state. Mol Microbiol 5:2053–2062 [View Article][PubMed]
     [Google Scholar]
  41. Pratt L. A., Silhavy T. J. ( 1998). Crl stimulates RpoS activity during stationary phase. Mol Microbiol 29:1225–1236 [View Article][PubMed]
     [Google Scholar]
  42. Prigent-Combaret C., Prensier G., Le Thi T. T., Vidal O., Lejeune P., Dorel C. ( 2000). Developmental pathway for biofilm formation in curli-producing Escherichia coli strains: role of flagella, curli and colanic acid. Environ Microbiol 2:450–464 [View Article][PubMed]
     [Google Scholar]
  43. Prigent-Combaret C., Brombacher E., Vidal O., Ambert A., Lejeune P., Landini P., Dorel C. ( 2001). Complex regulatory network controls initial adhesion and biofilm formation in Escherichia coli via regulation of the csgD gene. J Bacteriol 183:7213–7223 [View Article][PubMed]
     [Google Scholar]
  44. Quan J. A., Schneider B. L., Paulsen I. T., Yamada M., Kredich N. M., Saier M. H. Jr ( 2002). Regulation of carbon utilization by sulfur availability in Escherichia coli and Salmonella typhimurium. Microbiology 148:123–131[PubMed]
     [Google Scholar]
  45. R Development Core Team ( 2013). r: A Language and Environment for Statistical Computing Vienna: R Foundation for Stistical Computing;
     [Google Scholar]
  46. Ren D., Zuo R., González Barrios A. F., Bedzyk L. A., Eldridge G. R., Pasmore M. E., Wood T. K. ( 2005). Differential gene expression for investigation of Escherichia coli biofilm inhibition by plant extract ursolic acid. Appl Environ Microbiol 71:4022–4034 [View Article][PubMed]
     [Google Scholar]
  47. Romeo T. ( 1998). Global regulation by the small RNA-binding protein CsrA and the non-coding RNA molecule CsrB. Mol Microbiol 29:1321–1330 [View Article][PubMed]
     [Google Scholar]
  48. Romeo T., Gong M., Liu M. Y., Brun-Zinkernagel A. M. ( 1993). Identification and molecular characterization of csrA, a pleiotropic gene from Escherichia coli that affects glycogen biosynthesis, gluconeogenesis, cell size, and surface properties. J Bacteriol 175:4744–4755[PubMed]
     [Google Scholar]
  49. Römling U., Sierralta W. D., Eriksson K., Normark S. ( 1998a). Multicellular and aggregative behaviour of Salmonella typhimurium strains is controlled by mutations in the agfD promoter. Mol Microbiol 28:249–264 [View Article][PubMed]
     [Google Scholar]
  50. Römling U., Bian Z., Hammar M., Sierralta W. D., Normark S. ( 1998b). Curli fibers are highly conserved between Salmonella typhimurium and Escherichia coli with respect to operon structure and regulation. J Bacteriol 180:722–731[PubMed]
     [Google Scholar]
  51. Römling U., Rohde M., Olsén A., Normark S., Reinköster J. ( 2000). AgfD, the checkpoint of multicellular and aggregative behaviour in Salmonella typhimurium regulates at least two independent pathways. Mol Microbiol 36:10–23 [View Article][PubMed]
     [Google Scholar]
  52. Schneider B., Xu Y. W., Janin J., Véron M., Deville-Bonne D. ( 1998). 3′-Phosphorylated nucleotides are tight binding inhibitors of nucleoside diphosphate kinase activity. J Biol Chem 273:28773–28778 [View Article][PubMed]
     [Google Scholar]
  53. Shimada T., Makinoshima H., Ogawa Y., Miki T., Maeda M., Ishihama A. ( 2004). Classification and strength measurement of stationary-phase promoters by use of a newly developed promoter cloning vector. J Bacteriol 186:7112–7122 [View Article][PubMed]
     [Google Scholar]
  54. Siculella L., Damiano F., di Summa R., Tredici S. M., Alduina R., Gnoni G. V., Alifano P. ( 2010). Guanosine 5′-diphosphate 3′-diphosphate (ppGpp) as a negative modulator of polynucleotide phosphorylase activity in a ‘rare’ actinomycete. Mol Microbiol 77:716–729 [View Article][PubMed]
     [Google Scholar]
  55. Sohanpal B. K., El-Labany S., Lahooti M., Plumbridge J. A., Blomfield I. C. ( 2004). Integrated regulatory responses of fimB to N-acetylneuraminic (sialic) acid and GlcNAc in Escherichia coli K-12. Proc Natl Acad Sci U S A 101:16322–16327 [View Article][PubMed]
     [Google Scholar]
  56. Sommerfeldt N., Possling A., Becker G., Pesavento C., Tschowri N., Hengge R. ( 2009). Gene expression patterns and differential input into curli fimbriae regulation of all GGDEF/EAL domain proteins in Escherichia coli. Microbiology 155:1318–1331 [View Article][PubMed]
     [Google Scholar]
  57. Soo V. W. C., Wood T. K. ( 2013). Antitoxin MqsA represses curli formation through the master biofilm regulator CsgD. Sci Rep 3:3186 [View Article][PubMed]
     [Google Scholar]
  58. Sturgill G., Toutain C. M., Komperda J., O’Toole G. A., Rather P. N. ( 2004). Role of CysE in production of an extracellular signaling molecule in Providencia stuartii and Escherichia coli: loss of CysE enhances biofilm formation in Escherichia coli. J Bacteriol 186:7610–7617 [View Article][PubMed]
     [Google Scholar]
  59. Tagliabue L., Maciag A., Antoniani D., Landini P. ( 2010a). The yddV-dos operon controls biofilm formation through the regulation of genes encoding curli fibers’ subunits in aerobically growing Escherichia coli. FEMS Immunol Med Microbiol 59:477–484[PubMed]
     [Google Scholar]
  60. Tagliabue L., Antoniani D., Maciag A., Bocci P., Raffaelli N., Landini P. ( 2010b). The diguanylate cyclase YddV controls production of the exopolysaccharide poly-N-acetylglucosamine (PNAG) through regulation of the PNAG biosynthetic pgaABCD operon. Microbiology 156:2901–2911 [View Article][PubMed]
     [Google Scholar]
  61. Tamayo R., Pratt J. T., Camilli A. ( 2007). Roles of cyclic diguanylate in the regulation of bacterial pathogenesis. Annu Rev Microbiol 61:131–148 [View Article][PubMed]
     [Google Scholar]
  62. Teather R. M., Wood P. J. ( 1982). Use of Congo red–polysaccharide interactions in enumeration and characterization of cellulolytic bacteria from the bovine rumen. Appl Environ Microbiol 43:777–780[PubMed]
     [Google Scholar]
  63. Toledano M. B., Kumar C., Le Moan N., Spector D., Tacnet F. ( 2007). The system biology of thiol redox system in Escherichia coli and yeast: differential functions in oxidative stress, iron metabolism and DNA synthesis. FEBS Lett 581:3598–3607 [View Article][PubMed]
     [Google Scholar]
  64. Tuckerman J. R., Gonzalez G., Gilles-Gonzalez M.-A. ( 2011). Cyclic di-GMP activation of polynucleotide phosphorylase signal-dependent RNA processing. J Mol Biol 407:633–639 [View Article][PubMed]
     [Google Scholar]
  65. Uhlich G. A., Chen C.-Y., Cottrell B. J., Nguyen L.-H. ( 2014). Growth media and temperature effects on biofilm formation by serotype O157 : H7 and non-O157 Shiga toxin-producing Escherichia coli. FEMS Microbiol Lett 354:133–141 [View Article][PubMed]
     [Google Scholar]
  66. Ulett G. C., Webb R. I., Schembri M. A. ( 2006). Antigen-43-mediated autoaggregation impairs motility in Escherichia coli. Microbiology 152:2101–2110 [View Article][PubMed]
     [Google Scholar]
  67. van der Ploeg J. R., Eichhorn E., Leisinger T. ( 2001). Sulfonate-sulfur metabolism and its regulation in Escherichia coli. Arch Microbiol 176:1–8 [View Article][PubMed]
     [Google Scholar]
  68. Vidal O., Longin R., Prigent-Combaret C., Dorel C., Hooreman M., Lejeune P. ( 1998). Isolation of an Escherichia coli K-12 mutant strain able to form biofilms on inert surfaces: involvement of a new ompR allele that increases curli expression. J Bacteriol 180:2442–2449[PubMed]
     [Google Scholar]
  69. Vogt J., Schulz G. E. ( 1999). The structure of the outer membrane protein OmpX from Escherichia coli reveals possible mechanisms of virulence. Structure 7:1301–1309 [View Article][PubMed]
     [Google Scholar]
  70. Weber H., Pesavento C., Possling A., Tischendorf G., Hengge R. ( 2006). Cyclic-di-GMP-mediated signalling within the sigma network of Escherichia coli. Mol Microbiol 62:1014–1034 [View Article][PubMed]
     [Google Scholar]
  71. Zheng D., Constantinidou C., Hobman J. L., Minchin S. D. ( 2004). Identification of the CRP regulon using in vitro and in vivo transcriptional profiling. Nucleic Acids Res 32:5874–5893 [View Article][PubMed]
     [Google Scholar]
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Sulfate assimilation pathway intermediate phosphoadenosine 5′-phosphosulfate acts as a signal molecule affecting production of curli fibres in Escherichia coli
Microbiology 160, 1832 (2014); https://doi.org/10.1099/mic.0.079699-0
/content/journal/micro/10.1099/mic.0.079699-0
/content/journal/micro/10.1099/mic.0.079699-0
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