1887

Abstract

The genomic island 9 (SPI-9) from serovar Typhi ( 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 serovar Enteritidis orthologous to Typhi STY2875, has been associated with biofilm formation, and is described as a virulence factor in mice. Preliminary analyses revealed that Typhi STY2875 ORF has a 600 bp deletion compared with Enteritidis , suggesting that Typhi STY2875 might be non-functional. At present, SPI-9 has not been studied in 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 Typhi SPI-9 were located at the membrane fraction, consistent with their putative role as T1SS. Furthermore, SPI-9 contributed to adherence of Typhi to epithelial cells when bacteria were grown under high osmolarity or low pH. Under the test conditions, Typhi SPI-9 did not participate in biofilm formation. SPI-9 is functional in 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
2020-04-08
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 Microbiol43:85–92[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 Microbiol22:703–714[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 Chem285:40573–40580 [CrossRef][PubMed]
    [Google Scholar]
  4. Barlag B., Hensel M.. 2015; The giant adhesin SiiE of Salmonella enterica . Molecules20:1134–1150 [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. IJMM304:521–529 [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 Bacteriol189:1827–1835 [CrossRef][PubMed]
    [Google Scholar]
  8. Brenner F. W., Villar R. G., Angulo F. J., Tauxe R., Swaminathan B.. 2000; Salmonella nomenclature. J Clin Microbiol38:2465–2467[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. Genetics173:25–34 [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 Bacteriol186:3202–3213[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 Bacteriol185:553–563[PubMed][CrossRef]
    [Google Scholar]
  12. Che D., Hasan M. S., Chen B.. 2014; Identifying pathogenicity islands in bacterial pathogenomics using computational approaches. Pathogens3:36–56 [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 A97:6640–6645[CrossRef]
    [Google Scholar]
  14. Delepelaire P.. 2004; Type I secretion in gram-negative bacteria. Biochim Biophys Acta1694:149–161 [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 Bacteriol176:3825–3831[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. Gene290:153–161 [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 Microbiol10:24–29 [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 Microbiol47:103–118[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 A103:1906–1911 [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. Microbiology155:477–488 [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 Microbiol159:279–287 [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 Microbiol160:800–808 [CrossRef][PubMed]
    [Google Scholar]
  23. Galán J. E.. 2001; Salmonella interactions with host cells: type III secretion at work. Annu Rev Cell Dev Biol17:53–86 [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 Microbiol9:1834–1850 [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 Rep2:376–381 [CrossRef][PubMed]
    [Google Scholar]
  26. Hansen-Wester I., Hensel M.. 2001; Salmonella pathogenicity islands encoding type III secretion systems. Microbes Infect3:549–559 [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 Immun72:2879–2888[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 One9: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 Biol485:85–93 [CrossRef][PubMed]
    [Google Scholar]
  30. Hentschel U., Hacker J.. 2001; Pathogenicity islands: the tip of the iceberg. Microbes Infect3:545–548 [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 Biol22:29–39[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 Genet1: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 Microbiol14:139 [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 Rev33:376–393 [CrossRef][PubMed]
    [Google Scholar]
  35. Laemmli U. K.. 1970; Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature227:680–685 [CrossRef][PubMed]
    [Google Scholar]
  36. Lasa I., Penadés J. R.. 2006; Bap: a family of surface proteins involved in biofilm formation. Res Microbiol157:99–107 [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 Microbiol58:1322–1339 [CrossRef][PubMed]
    [Google Scholar]
  38. Link A. J., LaBaer J.. 2011; Trichloroacetic acid (TCA) precipitation of proteins. Cold Spring Harb Protoc2011:993–994 [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. Electrophoresis12:448–450 [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. Nature413:852–856 [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. Gene29:247–250 [CrossRef][PubMed]
    [Google Scholar]
  42. Moran N. A., Plague G. R.. 2004; Genomic changes following host restriction in bacteria. Curr Opin Genet Dev14:627–633 [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 A93:7800–7804[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. Nature413:848–852 [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 Res45:2 [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 One4:e5551 [CrossRef][PubMed]
    [Google Scholar]
  47. Rhen M., Dorman C. J.. 2005; Hierarchical gene regulators adapt Salmonella enterica to its host milieus. IJMM294:487–502 [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. Scientifica2014:532816 [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 Rev29:1021–1040 [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 Microbiol38:428–432 [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 Bacteriol180:4750–4752[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 Evol26:146–152 [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 A98:15264–15269 [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 Announc2: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 One11: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. Bioinformatics26:1608–1615 [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. Bioinformatics20:612–622 [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

Most cited this month

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