1887

Microbiology Society logo

Volume 160, Issue 7

Comprehensive overexpression analysis of cyclic-di-GMP signalling proteins in the phytopathogen reveals diverse effects on motility and virulence phenotypes Free

Abstract

Bis-(3′-5′)-cyclic dimeric guanosine monophosphate (c-di-GMP) is a ubiquitous bacterial signalling molecule produced by diguanylate cyclases of the GGDEF-domain family. Elevated c-di-GMP levels or increased GGDEF protein expression is frequently associated with the onset of sessility and biofilm formation in numerous bacterial species. Conversely, phosphodiesterase-dependent diminution of c-di-GMP levels by EAL- and HD-GYP-domain proteins is often accompanied by increased motility and virulence. In this study, we individually overexpressed 23 predicted GGDEF, EAL or HD-GYP-domain proteins encoded by the phytopathogen strain SCRI1043. MS-based detection of c-di-GMP and 5′-phosphoguanylyl-(3′-5′)-guanosine in these strains revealed that overexpression of most genes promoted modest 1–10-fold changes in cellular levels of c-di-GMP, with the exception of the GGDEF-domain proteins ECA0659 and ECA3374, which induced 1290- and 7660-fold increases, respectively. Overexpression of most EAL domain proteins increased motility, while overexpression of most GGDEF domain proteins reduced motility and increased poly-β-1,6--acetyl-glucosamine-dependent flocculation. In contrast to domain-based predictions, overexpression of the EAL protein ECA3549 or the HD-GYP protein ECA3548 increased c-di-GMP concentrations and reduced motility. Most overexpression constructs altered the levels of secreted cellulases, pectinases and proteases, confirming c-di-GMP regulation of virulence in . . However, there was no apparent correlation between virulence-factor induction and the domain class expressed or cellular c-di-GMP levels, suggesting that regulation was in response to specific effectors within the network, rather than total c-di-GMP concentration. Finally, we demonstrated that the cellular localization patterns vary considerably for GGDEF/EAL/HD-GYP proteins, indicating it is a likely factor restricting specific interactions within the c-di-GMP network.

  • Received:
  • Accepted:
  • Published Online:
Funding
This study was supported by the:
  • Biotechnology and Biological Sciences Research Council (BBSRC, UK)
  • James Hutton Institute
© Microbiology Society
Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.076828-0
2014-07-01
2024-04-27
Loading full text...

Full text loading...

/deliver/fulltext/micro/160/7/1427.html?itemId=/content/journal/micro/10.1099/mic.0.076828-0&mimeType=html&fmt=ahah

References

  1. Aldridge P., Paul R., Goymer P., Rainey P., Jenal U. ( 2003). Role of the GGDEF regulator PleD in polar development of Caulobacter crescentus.. Mol Microbiol 47:1695–1708 [View Article][PubMed]
     [Google Scholar]
  2. Amikam D., Galperin M. Y. ( 2006). PilZ domain is part of the bacterial c-di-GMP binding protein. Bioinformatics 22:3–6 [View Article][PubMed]
     [Google Scholar]
  3. Amikam D., Steinberger O., Shkolnik T., Ben-Ishai Z. ( 1995). The novel cyclic dinucleotide 3′-5′ cyclic diguanylic acid binds to p21ras and enhances DNA synthesis but not cell replication in the Molt 4 cell line. Biochem J 311:921–927[PubMed]
     [Google Scholar]
  4. Andrade M. O., Alegria M. C., Guzzo C. R., Docena C., Pareda Rosa M. C., Ramos C. H. I., Farah C. S. ( 2006). 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 62:537–551 [View Article][PubMed]
     [Google Scholar]
  5. Arai R., Ueda H., Kitayama A., Kamiya N., Nagamune T. ( 2001). Design of the linkers which effectively separate domains of a bifunctional fusion protein. Protein Eng 14:529–532 [View Article][PubMed]
     [Google Scholar]
  6. Aravind L., Ponting C. P. ( 1997). The GAF domain: an evolutionary link between diverse phototransducing proteins. Trends Biochem Sci 22:458–459 [View Article][PubMed]
     [Google Scholar]
  7. Barends T. R. M., Hartmann E., Griese J. J., Beitlich T., Kirienko N. V., Ryjenkov D. A., Reinstein J., Shoeman R. L., Gomelsky M., Schlichting I. ( 2009). Structure and mechanism of a bacterial light-regulated cyclic nucleotide phosphodiesterase. Nature 459:1015–1018 [View Article][PubMed]
     [Google Scholar]
  8. Bell K. S., Sebaihia M., Pritchard L., Holden M. T. G., Hyman L. J., Holeva M. C., Thomson N. R., Bentley S. D., Churcher L. J. C. & other authors ( 2004). Genome sequence of the enterobacterial phytopathogen Erwinia carotovora subsp. atroseptica and characterization of virulence factors. Proc Natl Acad Sci U S A 101:11105–11110 [View Article][PubMed]
     [Google Scholar]
  9. Bellini D., Caly D. L., McCarthy Y., Bumann M., An S.-Q., Dow J. M., Ryan R. P., Walsh M. A. ( 2014). Crystal structure of an HD-GYP domain cyclic-di-GMP phosphodiesterase reveals an enzyme with a novel trinuclear catalytic iron centre. Mol Microbiol 91:26–38 [View Article][PubMed]
     [Google Scholar]
  10. Bharati B. K., Sharma I. M., Kasetty S., Kumar M., Mukherjee R., Chatterji D. ( 2012). A full-length bifunctional protein involved in c-di-GMP turnover is required for long-term survival under nutrient starvation in Mycobacterium smegmatis.. Microbiology 158:1415–1427 [View Article][PubMed]
     [Google Scholar]
  11. Chan C., Paul R., Samoray D., Amiot N. C., Giese B., Jenal U., Schirmer T. ( 2004). Structural basis of activity and allosteric control of diguanylate cyclase. Proc Natl Acad Sci U S A 101:17084–17089 [View Article][PubMed]
     [Google Scholar]
  12. 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 [View Article][PubMed]
     [Google Scholar]
  13. 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 281:32015–32024 [View Article][PubMed]
     [Google Scholar]
  14. Christensen G. D., Simpson W. A., Younger J. J., Baddour L. M., Barrett F. F., Melton D. M., Beachey E. H. ( 1985). Adherence of coagulase-negative staphylococci to plastic tissue culture plates: a quantitative model for the adherence of staphylococci to medical devices. J Clin Microbiol 22:996–1006[PubMed]
     [Google Scholar]
  15. Cooper V. J., Salmond G. P. ( 1993). Molecular analysis of the major cellulase (CelV) of Erwinia carotovora: evidence for an evolutionary “mix-and-match” of enzyme domains. Mol Gen Genet 241:341–350[PubMed]
     [Google Scholar]
  16. Coulthurst S. J., Lilley K. S., Salmond G. P. C. ( 2006). Genetic and proteomic analysis of the role of LuxS in the enteric phytopathogen, Erwinia carotovora.. Mol Plant Pathol 7:31–45 [View Article][PubMed]
     [Google Scholar]
  17. Cserzö M., Wallin E., Simon I., von Heijne G., Elofsson A. ( 1997). Prediction of transmembrane α-helices in prokaryotic membrane proteins: the dense alignment surface method. Protein Eng 10:673–676 [View Article][PubMed]
     [Google Scholar]
  18. De N., Navarro M. V. A. S., Raghavan R. V., Sondermann H. ( 2009). Determinants for the activation and autoinhibition of the diguanylate cyclase response regulator WspR. J Mol Biol 393:619–633 [View Article][PubMed]
     [Google Scholar]
  19. Delepelaire P., Wandersman C. ( 1991). Characterization, localization and transmembrane organization of the three proteins PrtD, PrtE and PrtF necessary for protease secretion by the gram-negative bacterium Erwinia chrysanthemi.. Mol Microbiol 5:2427–2434 [View Article][PubMed]
     [Google Scholar]
  20. 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 23:93–104 [View Article][PubMed]
     [Google Scholar]
  21. Fineran P. C., Williamson N. R., Lilley K. S., Salmond G. P. C. ( 2007). Virulence and prodigiosin antibiotic biosynthesis in Serratia are regulated pleiotropically by the GGDEF/EAL domain protein, PigX. J Bacteriol 189:7653–7662 [View Article][PubMed]
     [Google Scholar]
  22. Galperin M. Y., Nikolskaya A. N., Koonin E. V. ( 2001). Novel domains of the prokaryotic two-component signal transduction systems. FEMS Microbiol Lett 203:11–21 [View Article][PubMed]
     [Google Scholar]
  23. Güvener Z. T., Harwood C. S. ( 2007). Subcellular location characteristics of the Pseudomonas aeruginosa GGDEF protein, WspR, indicate that it produces cyclic-di-GMP in response to growth on surfaces. Mol Microbiol 66:1459–1473[PubMed]
     [Google Scholar]
  24. Guzman L. M., Belin D., Carson M. J., Beckwith J. ( 1995). Tight regulation, modulation, and high-level expression by vectors containing the arabinose PBAD promoter. J Bacteriol 177:4121–4130[PubMed]
     [Google Scholar]
  25. Guzzo C. R., Dunger G., Salinas R. K., Farah C. S. ( 2013). Structure of the PilZ-FimXEAL-c-di-GMP complex responsible for the regulation of bacterial type IV pilus biogenesis. J Mol Biol 425:2174–2197 [View Article][PubMed]
     [Google Scholar]
  26. Hengge R. ( 2009). Principles of c-di-GMP signalling in bacteria. Nat Rev Microbiol 7:263–273 [View Article][PubMed]
     [Google Scholar]
  27. Hinsa S. M., O'Toole G. A. ( 2006). Biofilm formation by Pseudomonas fluorescens WCS365: a role for LapD. Microbiology 152:1375–1383 [View Article][PubMed]
     [Google Scholar]
  28. Hinton J. C., Sidebotham J. M., Gill D. R., Salmond G. P. ( 1989). Extracellular and periplasmic isoenzymes of pectate lyase from Erwinia carotovora subspecies carotovora belong to different gene families. Mol Microbiol 3:1785–1795 [View Article][PubMed]
     [Google Scholar]
  29. Hofmann K., Stoffel W. ( 1993). TMBASE - a database of membrane spanning protein segments. Biol Chem Hoppe Seyler 374:166
     [Google Scholar]
  30. Hou S., Freitas T., Larsen R. W., Piatibratov M., Sivozhelezov V., Yamamoto A., Meleshkevitch E. A., Zimmer M., Ordal G. W., Alam M. ( 2001). Globin-coupled sensors: a class of heme-containing sensors in Archaea and Bacteria. Proc Natl Acad Sci U S A 98:9353–9358 [View Article][PubMed]
     [Google Scholar]
  31. Huang B., Whitchurch C. B., Mattick J. S. ( 2003). FimX, a multidomain protein connecting environmental signals to twitching motility in Pseudomonas aeruginosa.. J Bacteriol 185:7068–7076 [View Article][PubMed]
     [Google Scholar]
  32. Itoh Y., Rice J. D., Goller C., Pannuri A., Taylor J., Meisner J., Beveridge T. J., Preston J. F. III, Romeo T. ( 2008). Roles of pgaABCD genes in synthesis, modification, and export of the Escherichia coli biofilm adhesin poly-β-1,6-N-acetyl-d-glucosamine. J Bacteriol 190:3670–3680 [View Article][PubMed]
     [Google Scholar]
  33. Jones L. J., Carballido-López R., Errington J. ( 2001). Control of cell shape in bacteria: helical, actin-like filaments in Bacillus subtilis.. Cell 104:913–922 [View Article][PubMed]
     [Google Scholar]
  34. Kotaka M., Dutta S., Lee H. C., Lim M. J. M., Wong Y., Rao F., Mitchell E. P., Liang Z. X., Lescar J. ( 2009). Expression, purification and preliminary crystallographic analysis of Pseudomonas aeruginosa RocR protein. Acta Crystallogr Sect F Struct Biol Cryst Commun 65:1035–1038 [View Article][PubMed]
     [Google Scholar]
  35. Krogh A., Larsson B., von Heijne G., Sonnhammer E. L. ( 2001). Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J Mol Biol 305:567–580 [View Article][PubMed]
     [Google Scholar]
  36. Kruse T., Bork-Jensen J., Gerdes K. ( 2005). The morphogenetic MreBCD proteins of Escherichia coli form an essential membrane-bound complex. Mol Microbiol 55:78–89 [View Article][PubMed]
     [Google Scholar]
  37. Kulasekara B. R., Kamischke C., Kulasekara H. D., Christen M., Wiggins P. A., Miller S. I. ( 2013). c-di-GMP heterogeneity is generated by the chemotaxis machinery to regulate flagellar motility. Elife 2:e01402 [View Article][PubMed]
     [Google Scholar]
  38. Levet-Paulo M., Lazzaroni J.-C., Gilbert C., Atlan D., Doublet P., Vianney A. ( 2011). The atypical two-component sensor kinase Lpl0330 from Legionella pneumophila controls the bifunctional diguanylate cyclase-phosphodiesterase Lpl0329 to modulate bis-(3′-5′)-cyclic dimeric GMP synthesis. J Biol Chem 286:31136–31144 [View Article][PubMed]
     [Google Scholar]
  39. Lovering A. L., Capeness M. J., Lambert C., Hobley L., Sockett R. E. ( 2011). The structure of an unconventional HD-GYP protein from Bdellovibrio reveals the roles of conserved residues in this class of cyclic-di-GMP phosphodiesterases. MBio 2:e00163-11 [View Article][PubMed]
     [Google Scholar]
  40. Marchler-Bauer A., Lu S., Anderson J. B., Chitsaz F., Derbyshire M. K., DeWeese-Scott C., Fong J. H., Geer L. Y., Geer R. C. & other authors ( 2011). CDD: a conserved domain database for the functional annotation of proteins. Nucleic Acids Res 39:DatabaseD225–D229 [View Article][PubMed]
     [Google Scholar]
  41. McCarthy Y., Ryan R. P., O’Donovan K., He Y.-Q., Jiang B.-L., Feng J.-X., Tang J.-L., Dow J. M. ( 2008). The role of PilZ domain proteins in the virulence of Xanthomonas campestris pv. campestris.. Mol Plant Pathol 9:819–824 [View Article][PubMed]
     [Google Scholar]
  42. Mills E., Pultz I. S., Kulasekara H. D., Miller S. I. ( 2011). The bacterial second messenger c-di-GMP: mechanisms of signalling. Cell Microbiol 13:1122–1129 [View Article][PubMed]
     [Google Scholar]
  43. Minasov G., Padavattan S., Shuvalova L., Brunzelle J. S., Miller D. J., Baslé A., Massa C., Collart F. R., Schirmer T., Anderson W. F. ( 2009). Crystal structures of YkuI and its complex with second messenger cyclic Di-GMP suggest catalytic mechanism of phosphodiester bond cleavage by EAL domains. J Biol Chem 284:13174–13184 [View Article][PubMed]
     [Google Scholar]
  44. Navarro M. V. A. S., De N., Bae N., Wang Q., Sondermann H. ( 2009). Structural analysis of the GGDEF-EAL domain-containing c-di-GMP receptor FimX. Structure 17:1104–1116 [View Article][PubMed]
     [Google Scholar]
  45. Newell P. D., Monds R. D., O'Toole G. A. ( 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 [View Article][PubMed]
     [Google Scholar]
  46. Paul R., Abel S., Wassmann P., Beck A., Heerklotz H., Jenal U. ( 2007). Activation of the diguanylate cyclase PleD by phosphorylation-mediated dimerization. J Biol Chem 282:29170–29177 [View Article][PubMed]
     [Google Scholar]
  47. Pérez-Mendoza D., Coulthurst S. J., Humphris S., Campbell E., Welch M., Toth I. K., Salmond G. P. C. ( 2011a). 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 82:719–733 [View Article][PubMed]
     [Google Scholar]
  48. Pérez-Mendoza D., Coulthurst S. J., Sanjuán J., Salmond G. P. C. ( 2011b). N-Acetylglucosamine-dependent biofilm formation in Pectobacterium atrosepticum is cryptic and activated by elevated c-di-GMP levels. Microbiology 157:3340–3348 [View Article][PubMed]
     [Google Scholar]
  49. Pratt J. T., Tamayo R., Tischler A. D., Camilli A. ( 2007). PilZ domain proteins bind cyclic diguanylate and regulate diverse processes in Vibrio cholerae.. J Biol Chem 282:12860–12870 [View Article][PubMed]
     [Google Scholar]
  50. Rao F., Yang Y., Qi Y., Liang Z.-X. ( 2008). Catalytic mechanism of cyclic di-GMP-specific phosphodiesterase: a study of the EAL domain-containing RocR from Pseudomonas aeruginosa.. J Bacteriol 190:3622–3631 [View Article][PubMed]
     [Google Scholar]
  51. Rao F., Qi Y., Chong H. S., Kotaka M., Li B., Li J., Lescar J., Tang K., Liang Z.-X. ( 2009). The functional role of a conserved loop in EAL domain-based cyclic di-GMP-specific phosphodiesterase. J Bacteriol 191:4722–4731 [View Article][PubMed]
     [Google Scholar]
  52. Reeves P. J., Whitcombe D., Wharam S., Gibson M., Allison G., Bunce N., Barallon R., Douglas P., Mulholland V. & other authors ( 1993). Molecular cloning and characterization of 13 out genes from Erwinia carotovora subspecies carotovora: genes encoding members of a general secretion pathway (GSP) widespread in gram-negative bacteria. Mol Microbiol 8:443–456 [View Article][PubMed]
     [Google Scholar]
  53. Robert-Paganin J., Nonin-Lecomte S., Réty S. ( 2012). Crystal structure of an EAL domain in complex with reaction product 5′-pGpG. PLoS ONE 7:e52424 [View Article][PubMed]
     [Google Scholar]
  54. Ross P., Weinhouse H., Aloni Y., Michaeli D., Weinberger-Ohana P., Mayer R., Braun S., de Vroom E., van der Marel G. A. & other authors ( 1987). Regulation of cellulose synthesis in Acetobacter xylinum by cyclic diguanylic acid. Nature 325:279–281 [View Article][PubMed]
     [Google Scholar]
  55. Ryan R. P., Fouhy Y., Lucey J. F., Crossman L. C., Spiro S., He Y.-W., Zhang L.-H., Heeb S., Cámara M. & other authors ( 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 [View Article][PubMed]
     [Google Scholar]
  56. Ryan R. P., McCarthy Y., Andrade M., Farah C. S., Armitage J. P., Dow J. M. ( 2010). Cell-cell signal-dependent dynamic interactions between HD-GYP and GGDEF domain proteins mediate virulence in Xanthomonas campestris.. Proc Natl Acad Sci U S A 107:5989–5994 [View Article][PubMed]
     [Google Scholar]
  57. Ryjenkov D. A., Simm R., Römling 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 [View Article][PubMed]
     [Google Scholar]
  58. Schmidt A. J., Ryjenkov D. A., 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 [View Article][PubMed]
     [Google Scholar]
  59. Simm R., Morr M., Remminghorst U., Andersson M., Römling 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 [View Article][PubMed]
     [Google Scholar]
  60. Smith T. G., Hoover T. R. ( 2009). Deciphering bacterial flagellar gene regulatory networks in the genomic era. Adv Appl Microbiol 67:257–295 [View Article][PubMed]
     [Google Scholar]
  61. Smith K. D., Shanahan C. A., Moore E. L., Simon A. C., Strobel S. A. ( 2011). Structural basis of differential ligand recognition by two classes of bis-(3′-5′)-cyclic dimeric guanosine monophosphate-binding riboswitches. Proc Natl Acad Sci U S A 108:7757–7762 [View Article][PubMed]
     [Google Scholar]
  62. Solano C., García B., Latasa C., Toledo-Arana A., Zorraquino V., Valle J., Casals J., Pedroso E., Lasa I. ( 2009). Genetic reductionist approach for dissecting individual roles of GGDEF proteins within the c-di-GMP signaling network in Salmonella. Proc Natl Acad Sci U S A 106:7997–8002 [View Article][PubMed]
     [Google Scholar]
  63. 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]
  64. Sondermann H., Shikuma N. J., Yildiz F. H. ( 2012). You’ve come a long way: c-di-GMP signaling. Curr Opin Microbiol 15:140–146 [View Article][PubMed]
     [Google Scholar]
  65. Sourjik V., Berg H. C. ( 2000). Localization of components of the chemotaxis machinery of Escherichia coli using fluorescent protein fusions. Mol Microbiol 37:740–751 [View Article][PubMed]
     [Google Scholar]
  66. Sudarsan N., Lee E. R., Weinberg Z., Moy R. H., Kim J. N., Link K. H., Breaker R. R. ( 2008). Riboswitches in eubacteria sense the second messenger cyclic di-GMP. Science 321:411–413 [View Article][PubMed]
     [Google Scholar]
  67. Tagliabue L., Antoniani D., Maciag A., Bocci P., Raffaelli N., Landini P. ( 2010). 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]
  68. Tchigvintsev A., Xu X., Singer A., Chang C., Brown G., Proudfoot M., Cui H., Flick R., Anderson W. F. & other authors ( 2010). Structural insight into the mechanism of c-di-GMP hydrolysis by EAL domain phosphodiesterases. J Mol Biol 402:524–538 [View Article][PubMed]
     [Google Scholar]
  69. Tuckerman J. R., Gonzalez G., Sousa E. H. S., Wan X., Saito J. A., Alam M., Gilles-Gonzalez M.-A. ( 2009). An oxygen-sensing diguanylate cyclase and phosphodiesterase couple for c-di-GMP control. Biochemistry 48:9764–9774 [View Article][PubMed]
     [Google Scholar]
  70. Wolfe A. J., Visick K. L. ( 2008). Get the message out: cyclic-Di-GMP regulates multiple levels of flagellum-based motility. J Bacteriol 190:463–475 [View Article][PubMed]
     [Google Scholar]
  71. Yi X., Yamazaki A., Biddle E., Zeng Q., Yang C.-H. ( 2010). Genetic analysis of two phosphodiesterases reveals cyclic diguanylate regulation of virulence factors in Dickeya dadantii.. Mol Microbiol 77:787–800 [View Article][PubMed]
     [Google Scholar]
  72. Zorraquino V., García B., Latasa C., Echeverz M., Toledo-Arana A., Valle J., Lasa I., Solano C. ( 2013). Coordinated cyclic-di-GMP repression of Salmonella motility through YcgR and cellulose. J Bacteriol 195:417–428 [View Article][PubMed]
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.076828-0
Loading
Comprehensive overexpression analysis of cyclic-di-GMP signalling proteins in the phytopathogen Pectobacterium atrosepticum reveals diverse effects on motility and virulence phenotypes
Microbiology 160, 1427 (2014); https://doi.org/10.1099/mic.0.076828-0
/content/journal/micro/10.1099/mic.0.076828-0
/content/journal/micro/10.1099/mic.0.076828-0
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF

Most cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error