1887

Abstract

The genomic island 9 (SPI-9) from Salmonella enterica serovar Typhi (S. Typhi) carries three ORFs (STY2876, STY2877, STY2878) presenting 98 % identity with a type 1 secretory apparatus (T1SS), and a single ORF (STY2875) similar to a large RTX-like protein exhibiting repeated Ig domains. BapA, the Salmonella enterica serovar Enteritidis orthologous to S. Typhi STY2875, has been associated with biofilm formation, and is described as a virulence factor in mice. Preliminary in silico analyses revealed that S. Typhi STY2875 ORF has a 600 bp deletion compared with S. Enteritidis bapA, suggesting that S. Typhi STY2875 might be non-functional. At present, SPI-9 has not been studied in S. Typhi. We found that the genes constituting SPI-9 are arranged in an operon whose promoter was up-regulated in high osmolarity and low pH in a RpoS-dependent manner. All the proteins encoded by S. Typhi SPI-9 were located at the membrane fraction, consistent with their putative role as T1SS. Furthermore, SPI-9 contributed to adherence of S. Typhi to epithelial cells when bacteria were grown under high osmolarity or low pH. Under the test conditions, S. Typhi SPI-9 did not participate in biofilm formation. SPI-9 is functional in S. Typhi and encodes an adhesin induced under conditions normally found in the intestine, such as high osmolarity. Hence, this is an example of a locus that might be designated a pseudogene by computational approaches but not by direct biological assays.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.000319
2016-08-01
2019-10-21
Loading full text...

Full text loading...

/deliver/fulltext/micro/162/8/1367.html?itemId=/content/journal/micro/10.1099/mic.0.000319&mimeType=html&fmt=ahah

References

  1. Altier C. . ( 2005;). Genetic and environmental control of salmonella invasion. . J Microbiol 43: 85–92.[PubMed]
    [Google Scholar]
  2. Bajaj V. , Lucas R. L. , Hwang C. , Lee C. A. . ( 1996;). Co-ordinate regulation of Salmonella typhimurium invasion genes by environmental and regulatory factors is mediated by control of hilA expression. . Mol Microbiol 22: 703–714.[PubMed] [CrossRef]
    [Google Scholar]
  3. Bakkes P. J. , Jenewein S. , Smits S. H. , Holland I. B. , Schmitt L. . ( 2010;). The rate of folding dictates substrate secretion by the Escherichia coli hemolysin type 1 secretion system. . J Biol Chem 285: 40573–40580. [CrossRef] [PubMed]
    [Google Scholar]
  4. Barlag B. , Hensel M. . ( 2015;). The giant adhesin SiiE of Salmonella enterica . . Molecules 20: 1134–1150. [CrossRef] [PubMed]
    [Google Scholar]
  5. Barrow P. A. , Duchet-Suchaux M. . ( 1997;). Salmonella carriage and the carrier state. . Pages 241–250 in Salmonella and Salmonellosis,’97 Proceedings. France:: Zoopôle;.
    [Google Scholar]
  6. Bielaszewska M. , Aldick T. , Bauwens A. , Karch H. . ( 2014;). Hemolysin of enterohemorrhagic Escherichia coli: structure, transport, biological activity and putative role in virulence. . IJMM 304: 521–529. [CrossRef] [PubMed]
    [Google Scholar]
  7. Boardman B. K. , Meehan B. M. , Fullner Satchell K. J. . ( 2007;). Growth phase regulation of Vibrio cholerae RTX toxin export. . J Bacteriol 189: 1827–1835. [CrossRef] [PubMed]
    [Google Scholar]
  8. Brenner F. W. , Villar R. G. , Angulo F. J. , Tauxe R. , Swaminathan B. . ( 2000;). Salmonella nomenclature. . J Clin Microbiol 38: 2465–2467.[PubMed]
    [Google Scholar]
  9. Bucarey S. A. , Villagra N. A. , Fuentes J. A. , Mora G. C. . ( 2006;). The cotranscribed Salmonella enterica sv. Typhi t sx and impX genes encode opposing nucleoside-specific import and export proteins. . Genetics 173: 25–34. [CrossRef] [PubMed]
    [Google Scholar]
  10. Bueno S. M. , Santiviago C. A. , Murillo A. A. , Fuentes J. A. , Trombert A. N. , Rodas P. I. , Youderian P. , Mora G. C. . ( 2004;). Precise excision of the large pathogenicity island, SPI7, in Salmonella enterica serovar Typhi. . J Bacteriol 186: 3202–3213.[PubMed] [CrossRef]
    [Google Scholar]
  11. Chan K. , Baker S. , Kim C. C. , Detweiler C. S. , Dougan G. , Falkow S. . ( 2003;). Genomic comparison of Salmonella enterica serovars and Salmonella bongori by use of an S. enterica serovar typhimurium DNA microarray. . J Bacteriol 185: 553–563.[PubMed] [CrossRef]
    [Google Scholar]
  12. Che D. , Hasan M. S. , Chen B. . ( 2014;). Identifying pathogenicity islands in bacterial pathogenomics using computational approaches. . Pathogens 3: 36–56. [CrossRef] [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 Acad Sci U S A 97: 6640–6645.[CrossRef]
    [Google Scholar]
  14. Delepelaire P. . ( 2004;). Type I secretion in gram-negative bacteria. . Biochim Biophys Acta 1694: 149–161. [CrossRef] [PubMed]
    [Google Scholar]
  15. Dinh T. , Paulsen I. T. , Saier M. H., Jr. . ( 1994;). A family of extracytoplasmic proteins that allow transport of large molecules across the outer membranes of gram-negative bacteria. . J Bacteriol 176: 3825–3831.[PubMed]
    [Google Scholar]
  16. Ellermeier C. D. , Janakiraman A. , Slauch J. M. . ( 2002;). Construction of targeted single copy lac fusions using lambda Red and FLP-mediated site-specific recombination in bacteria. . Gene 290: 153–161. [CrossRef] [PubMed]
    [Google Scholar]
  17. Ellermeier J. R. , Slauch J. M. . ( 2007;). Adaptation to the host environment: regulation of the SPI1 type III secretion system in Salmonella enterica serovar Typhimurium. . Curr Opin Microbiol 10: 24–29. [CrossRef] [PubMed]
    [Google Scholar]
  18. Eriksson S. , Lucchini S. , Thompson A. , Rhen M. , Hinton J. C. . ( 2003;). Unravelling the biology of macrophage infection by gene expression profiling of intracellular Salmonella enterica . . Mol Microbiol 47: 103–118.[PubMed] [CrossRef]
    [Google Scholar]
  19. Faucher S. P. , Porwollik S. , Dozois C. M. , McClelland M. , Daigle F. . ( 2006;). Transcriptome of Salmonella enterica serovar Typhi within macrophages revealed through the selective capture of transcribed sequences. . Proc Natl Acad Sci U S A 103: 1906–1911. [CrossRef] [PubMed]
    [Google Scholar]
  20. Faucher S. P. , Forest C. , Béland M. , Daigle F. . ( 2009;). A novel PhoP-regulated locus encoding the cytolysin ClyA and the secreted invasin TaiA of Salmonella enterica serovar Typhi is involved in virulence. . Microbiology 155: 477–488. [CrossRef] [PubMed]
    [Google Scholar]
  21. Fuentes J. A. , Villagra N. , Castillo-Ruiz M. , Mora G. C. . ( 2008;). The Salmonella Typhi hlyE gene plays a role in invasion of cultured epithelial cells and its functional transfer to S. Typhimurium promotes deep organ infection in mice. . Res Microbiol 159: 279–287. [CrossRef] [PubMed]
    [Google Scholar]
  22. Fuentes J. A. , Jofré M. R. , Villagra N. A. , Mora G. C. . ( 2009;). RpoS- and Crp-dependent transcriptional control of Salmonella Typhi taiA and hlyE genes: role of environmental conditions. . Res Microbiol 160: 800–808. [CrossRef] [PubMed]
    [Google Scholar]
  23. Galán J. E. . ( 2001;). Salmonella interactions with host cells: type III secretion at work. . Annu Rev Cell Dev Biol 17: 53–86. [CrossRef] [PubMed]
    [Google Scholar]
  24. Gerlach R. G. , Jäckel D. , Stecher B. , Wagner C. , Lupas A. , Hardt W. D. , Hensel M. . ( 2007;). Salmonella Pathogenicity Island 4 encodes a giant non-fimbrial adhesin and the cognate type 1 secretion system. . Cell Microbiol 9: 1834–1850. [CrossRef] [PubMed]
    [Google Scholar]
  25. Hacker J. , Carniel E. . ( 2001;). Ecological fitness, genomic islands and bacterial pathogenicity. A Darwinian view of the evolution of microbes. . EMBO Rep 2: 376–381. [CrossRef] [PubMed]
    [Google Scholar]
  26. Hansen-Wester I. , Hensel M. . ( 2001;). Salmonella pathogenicity islands encoding type III secretion systems. . Microbes Infect 3: 549–559. [CrossRef] [PubMed]
    [Google Scholar]
  27. Hansen-Wester I. , Chakravortty D. , Hensel M. . ( 2004;). Functional transfer of Salmonella pathogenicity island 2 to Salmonella bongori and Escherichia coli . . Infect Immun 72: 2879–2888.[PubMed] [CrossRef]
    [Google Scholar]
  28. Hayward M. R. , AbuOun M. , La Ragione R. M. , Tchórzewska M. A. , Cooley W. A. , Everest D. J. , Petrovska L. , Jansen V. A. , Woodward M. J. . ( 2014;). SPI-23 of S. Derby: role in adherence and invasion of porcine tissues. . PLoS One 9: e107857. [CrossRef] [PubMed]
    [Google Scholar]
  29. Hengge-Aronis R. . ( 2000;). A role for the sigma S subunit of RNA polymerase in the regulation of bacterial virulence. . Adv Exp Med Biol 485: 85–93. [CrossRef] [PubMed]
    [Google Scholar]
  30. Hentschel U. , Hacker J. . ( 2001;). Pathogenicity islands: the tip of the iceberg. . Microbes Infect 3: 545–548. [CrossRef] [PubMed]
    [Google Scholar]
  31. Holland I. B. , Schmitt L. , Young J. . ( 2005;). Type 1 protein secretion in bacteria, the ABC-transporter dependent pathway (review). . Mol Membr Biol 22: 29–39.[PubMed] [CrossRef]
    [Google Scholar]
  32. Hsiao W. W. , Ung K. , Aeschliman D. , Bryan J. , Finlay B. B. , Brinkman F. S. . ( 2005;). Evidence of a large novel gene pool associated with prokaryotic genomic islands. . PLoS Genet 1: e62. [CrossRef] [PubMed]
    [Google Scholar]
  33. Jofré M. R. , Rodríguez L. M. , Villagra N. A. , Hidalgo A. A. , Mora G. C. , Fuentes J. A. . ( 2014;). RpoS integrates CRP, Fis, and PhoP signaling pathways to control Salmonella Typhi hlyE expression. . BMC Microbiol 14: 139. [CrossRef] [PubMed]
    [Google Scholar]
  34. Juhas M. , van der Meer J. R. , Gaillard M. , Harding R. M. , Hood D. W. , Crook D. W. . ( 2009;). Genomic islands: tools of bacterial horizontal gene transfer and evolution. . FEMS Microbiol Rev 33: 376–393. [CrossRef] [PubMed]
    [Google Scholar]
  35. Laemmli U. K. . ( 1970;). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. . Nature 227: 680–685. [CrossRef] [PubMed]
    [Google Scholar]
  36. Lasa I. , Penadés J. R. . ( 2006;). Bap: a family of surface proteins involved in biofilm formation. . Res Microbiol 157: 99–107. [CrossRef] [PubMed]
    [Google Scholar]
  37. Latasa C. , Roux A. , Toledo-Arana A. , Ghigo J. M. , Gamazo C. , Penadés J. R. , Lasa I. . ( 2005;). BapA, a large secreted protein required for biofilm formation and host colonization of Salmonella enterica serovar Enteritidis. . Mol Microbiol 58: 1322–1339. [CrossRef] [PubMed]
    [Google Scholar]
  38. Link A. J. , LaBaer J. . ( 2011;). Trichloroacetic acid (TCA) precipitation of proteins. . Cold Spring Harb Protoc 2011: 993–994. [CrossRef] [PubMed]
    [Google Scholar]
  39. Lobos S. R. , Mora G. C. . ( 1991;). Alteration in the electrophoretic mobility of OmpC due to variations in the ammonium persulfate concentration in sodium dodecyl sulfate-polyacrylamide gel electrophoresis. . Electrophoresis 12: 448–450. [CrossRef] [PubMed]
    [Google Scholar]
  40. McClelland M. , Sanderson K. E. , Spieth J. , Clifton S. W. , Latreille P. , Courtney L. , Porwollik S. , Ali J. , Dante M. et al. ( 2001;). Complete genome sequence of Salmonella enterica serovar Typhimurium LT2. . Nature 413: 852–856. [CrossRef] [PubMed]
    [Google Scholar]
  41. Miller F. D. , Hershberger C. L. . ( 1984;). A quantitative beta-galactosidase alpha-complementation assay for fusion proteins containing human insulin B-chain peptides. . Gene 29: 247–250. [CrossRef] [PubMed]
    [Google Scholar]
  42. Moran N. A. , Plague G. R. . ( 2004;). Genomic changes following host restriction in bacteria. . Curr Opin Genet Dev 14: 627–633. [CrossRef] [PubMed]
    [Google Scholar]
  43. Ochman H. , Soncini F. C. , Solomon F. , Groisman E. A. . ( 1996;). Identification of a pathogenicity island required for Salmonella survival in host cells. . Proc Natl Acad Sci U S A 93: 7800–7804.[PubMed] [CrossRef]
    [Google Scholar]
  44. Parkhill J. , Dougan G. , James K. D. , Thomson N. R. , Pickard D. , Wain J. , Churcher C. , Mungall K. L. , Bentley S. D. et al. ( 2001;). Complete genome sequence of a multiple drug resistant Salmonella enterica serovar Typhi CT18. . Nature 413: 848–852. [CrossRef] [PubMed]
    [Google Scholar]
  45. Pezoa D. , Blondel C. J. , Silva C. A. , Yang H. J. , Andrews-Polymenis H. , Santiviago C. A. , Contreras I. . ( 2014;). Only one of the two type VI secretion systems encoded in the Salmonella enterica serotype Dublin genome is involved in colonization of the avian and murine hosts. . Vet Res 45: 2. [CrossRef] [PubMed]
    [Google Scholar]
  46. Retamal P. , Castillo-Ruiz M. , Mora G. C. . ( 2009;). Characterization of MgtC, a virulence factor of Salmonella enterica Serovar Typhi. . PLoS One 4: e5551. [CrossRef] [PubMed]
    [Google Scholar]
  47. Rhen M. , Dorman C. J. . ( 2005;). Hierarchical gene regulators adapt Salmonella enterica to its host milieus. . IJMM 294: 487–502. [CrossRef] [PubMed]
    [Google Scholar]
  48. Ronald P. C. . ( 2014;). The Role of RaxST, a Prokaryotic Sulfotransferase, and RaxABC, a Putative Type I Secretion System, in Activation of the Rice XA21-Mediated Immune Response. . Scientifica 2014: 532816. [CrossRef] [PubMed]
    [Google Scholar]
  49. Rychlik I. , Barrow P. A. . ( 2005;). Salmonella stress management and its relevance to behaviour during intestinal colonisation and infection. . FEMS Microbiol Rev 29: 1021–1040. [CrossRef] [PubMed]
    [Google Scholar]
  50. Stepanović S. , Cirković I. , Ranin L. , Svabić-Vlahović M. . ( 2004;). Biofilm formation by Salmonella spp. and Listeria monocytogenes on plastic surface. . Lett Appl Microbiol 38: 428–432. [CrossRef] [PubMed]
    [Google Scholar]
  51. Toro C. S. , Mora G. C. , Figueroa-Bossi N. . ( 1998;). Gene transfer between related bacteria by electrotransformation: mapping Salmonella typhi genes in Salmonella typhimurium . . J Bacteriol 180: 4750–4752.[PubMed]
    [Google Scholar]
  52. Urrutia I. M. , Fuentes J. A. , Valenzuela L. M. , Ortega A. P. , Hidalgo A. A. , Mora G. C. . ( 2014;). Salmonella Typhi shdA: pseudogene or allelic variant?. Infect Genet Evol 26: 146–152. [CrossRef] [PubMed]
    [Google Scholar]
  53. Uzzau S. , Figueroa-Bossi N. , Rubino S. , Bossi L. . ( 2001;). Epitope tagging of chromosomal genes in Salmonella . . Proc Natl Acad Sci U S A 98: 15264–15269. [CrossRef] [PubMed]
    [Google Scholar]
  54. Valenzuela C. , Ugalde J. A. , Mora G. C. , Alvarez S. , Contreras I. , Santiviago C. A. . ( 2014;). Draft genome sequence of Salmonella enterica serovar Typhi strain STH2370. . Genome Announc 2: e00104–14. [CrossRef] [PubMed]
    [Google Scholar]
  55. Wang K. C. , Huang C. H. , Huang C. J. , Fang S. B. . ( 2016;). Impacts of Salmonella enterica serovar typhimurium and its speG gene on the transcriptomes of in vitro M cells and Caco-2 cells. . PLoS One 11: e0153444. [CrossRef] [PubMed]
    [Google Scholar]
  56. Yu N. Y. , Wagner J. R. , Laird M. R. , Melli G. , Rey S. , Lo R. , Dao P. , Sahinalp S. C. , Ester M. et al. ( 2010;). PSORTb 3.0: improved protein subcellular localization prediction with refined localization subcategories and predictive capabilities for all prokaryotes. . Bioinformatics 26: 1608–1615. [CrossRef] [PubMed]
    [Google Scholar]
  57. Zhang R. , Zhang C. T. . ( 2004;). A systematic method to identify genomic islands and its applications in analyzing the genomes of Corynebacterium glutamicum and Vibrio vulnificus CMCP6 chromosome I. . Bioinformatics 20: 612–622. [CrossRef] [PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.000319
Loading
/content/journal/micro/10.1099/mic.0.000319
Loading

Data & Media loading...

Supplements

Supplementary File 1



PDF
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