Pathogenicity island excision during an infection by Salmonella enterica serovar Enteritidis is required for crossing the intestinal epithelial barrier in mice to cause systemic infection
Autoři:
Catalina Pardo-Roa aff001; Geraldyne A. Salazar aff001; Loreani Noguera aff001; Francisco J. Salazar-Echegarai aff001; Omar P. Vallejos aff001; Isidora Suazo aff001; Bárbara M. Schultz aff001; Irenice Coronado-Arrazola aff001; Alexis M. Kalergis aff001; Susan M. Bueno aff001
Působiště autorů:
Millennium Institute on Immunology and Immunotherapy, Departamento de Genética Molecular y Microbiología, Facultad de Ciencias Biológicas, Pontificia Universidad Católica de Chile, Santiago, Chile
aff001; Departamento de Endocrinología, Facultad de Medicina, Pontificia Universidad Católica de Chile, Santiago, Chile
aff002
Vyšlo v časopise:
Pathogenicity island excision during an infection by Salmonella enterica serovar Enteritidis is required for crossing the intestinal epithelial barrier in mice to cause systemic infection. PLoS Pathog 15(12): e32767. doi:10.1371/journal.ppat.1008152
Kategorie:
Research Article
doi:
https://doi.org/10.1371/journal.ppat.1008152
Souhrn
Pathogenicity island excision is a phenomenon that occurs in several Salmonella enterica serovars and other members of the family Enterobacteriaceae. ROD21 is an excisable pathogenicity island found in the chromosome of S. Enteritidis, S. Dublin and S. Typhi among others, which contain several genes encoding virulence-associated proteins. Excision of ROD21 may play a role in the ability of S. Enteritidis to cause a systemic infection in mice. Our previous studies have shown that Salmonella strains unable to excise ROD21 display a reduced ability to colonize the liver and spleen. In this work, we determined the kinetics of ROD21 excision in vivo in C57BL/6 mice and its effect on virulence. We quantified bacterial burden and excision frequency in different portions of the digestive tract and internal organs throughout the infection. We observed that the frequency of ROD21 excision was significantly increased in the bacterial population colonizing mesenteric lymph nodes at early stages of the infective cycle, before 48 hours post-infection. In contrast, excision frequency remained very low in the liver and spleen at these stages. Interestingly, excision increased drastically after 48 h post infection, when intestinal re-infection and mortality begun. Moreover, we observed that the inability to excise ROD21 had a negative effect on S. Enteritidis capacity to translocate from the intestine to deeper organs, which correlates with an abnormal transcription of invA in the S. Enteritidis strain unable to excise ROD21. These results suggest that excision of ROD21 is a genetic mechanism required by S. Enteritidis to produce a successful invasion of the intestinal epithelium, a step required to generate systemic infection in mice.
Klíčová slova:
DNA transcription – Gastrointestinal infections – Gastrointestinal tract – Gene expression – Liver – Salmonella – Salmonellosis – Spleen
Zdroje
1. Rabsch W, Andrews HL, Kingsley RA, Prager R, Tschape H, Adams LG, et al. Salmonella enterica serotype Typhimurium and its host-adapted variants. Infect Immun. 2002;70(5):2249–55. Epub 2002/04/16. doi: 10.1128/IAI.70.5.2249-2255.2002 11953356
2. Yim L, Betancor L, Martinez A, Giossa G, Bryant C, Maskell D, et al. Differential phenotypic diversity among epidemic-spanning Salmonella enterica serovar Enteritidis isolates from humans or animals. Applied and environmental microbiology. 2010;76(20):6812–20. doi: 10.1128/AEM.00497-10 20802078
3. Wilks C, Parkinson G. International Review of Salmonella Enteritidis Epidemiology and Control Policies: A Report for the Rural Industries Research and Development Corporation RIRDC Project No. DAV-146A; 2000.
4. Sanchez-Vargas FM, Abu-El-Haija MA, Gomez-Duarte OG. Salmonella infections: an update on epidemiology, management, and prevention. Travel Med Infect Dis. 2011;9(6):263–77. Epub 2011/11/29. doi: 10.1016/j.tmaid.2011.11.001 22118951.
5. Eguale T, Gebreyes WA, Asrat D, Alemayehu H, Gunn JS, Engidawork E. Non-typhoidal Salmonella serotypes, antimicrobial resistance and co-infection with parasites among patients with diarrhea and other gastrointestinal complaints in Addis Ababa, Ethiopia. BMC Infect Dis. 2015;15:497. Epub 2015/11/04. doi: 10.1186/s12879-015-1235-y 26537951
6. Barthel M, Hapfelmeier S, Quintanilla-Martínez L, Kremer M, Rohde M, Hogardt M, et al. Pretreatment of mice with streptomycin provides a Salmonella enterica serovar Typhimurium colitis model that allows analysis of both pathogen and host. Infect Immun. 2003;71(5):2839–58. doi: 10.1128/IAI.71.5.2839-2858.2003 12704158
7. Palmer AD, Slauch JM. Mechanisms of Salmonella pathogenesis in animal models. Hum Ecol Risk Assess. 2017;23(8):1877–92. Epub 2017/08/24. doi: 10.1080/10807039.2017.1353903 31031557
8. Guard-Petter J, Henzler DJ, Rahman MM, Carlson RW. On-farm monitoring of mouse-invasive Salmonella enterica serovar Enteritidis and a model for its association with the production of contaminated eggs. Applied and environmental microbiology. 1997;63(4):1588–93. 9097453
9. Marin C, Martelli F, Rabie A, Davies R. Commercial Frozen Mice Used by Owners to Feed Reptiles are Highly Externally Contaminated with Salmonella Enteritidis PT8. Vector Borne Zoonotic Dis. 2018;18(9):453–7. Epub 2018/05/23. doi: 10.1089/vbz.2018.2295 29791305.
10. Guard J, Cao G, Luo Y, Baugher JD, Davison S, Yao K, et al. Genome sequence analysis of 91 Salmonella Enteritidis isolates from mice caught on poultry farms in the mid 1990s. Genomics. 2019. Epub 2019/04/08. doi: 10.1016/j.ygeno.2019.04.005 30974149.
11. Jacobsen A, Hendriksen RS, Aaresturp FM, Ussery DW, Friis C. The Salmonella enterica pan-genome. Microb Ecol. 2011;62(3):487–504. Epub 2011/06/07. doi: 10.1007/s00248-011-9880-1 21643699 mc3175032.
12. Swart AL, Hensel M. Interactions of Salmonella enterica with dendritic cells. Virulence. 2012;3(7):660–7. Epub 2012/11/15. doi: 10.4161/viru.22761 23221476
13. Monack DM. Salmonella persistence and transmission strategies. Curr Opin Microbiol. 2012;15(1):100–7. Epub 2011/12/06. doi: 10.1016/j.mib.2011.10.013 22137596.
14. Ilyas B, Tsai CN, Coombes BK. Evolution of Salmonella-Host Cell Interactions through a Dynamic Bacterial Genome. Front Cell Infect Microbiol. 2017;7:428. Epub 2017/09/29. doi: 10.3389/fcimb.2017.00428 29034217
15. Gal-Mor O, Finlay BB. Pathogenicity islands: a molecular toolbox for bacterial virulence. Cell Microbiol. 2006;8(11):1707–19. Epub 2006/08/31. doi: 10.1111/j.1462-5822.2006.00794.x 16939533.
16. Schmidt H, Hensel M. Pathogenicity Islands in Bacterial Pathogenesis. Clin Microbiol Rev. 2004;17(1):14–56. doi: 10.1128/CMR.17.1.14-56.2004 14726454
17. Blum G, Ott M, Lischewski A, Ritter A, Imrich H, Tschape H, et al. Excision of large DNA regions termed pathogenicity islands from tRNA-specific loci in the chromosome of an Escherichia coli wild-type pathogen. Infect Immun. 1994;62(2):606–14. Epub 1994/02/01. 7507897.
18. Lautner M, Schunder E, Herrmann V, Heuner K. Regulation, integrase-dependent excision, and horizontal transfer of genomic islands in Legionella pneumophila. J Bacteriol. 2013;195(7):1583–97. Epub 2013/01/29. doi: 10.1128/JB.01739-12 23354744
19. Lesic B, Bach S, Ghigo JM, Dobrindt U, Hacker J, Carniel E. Excision of the high-pathogenicity island of Yersinia pseudotuberculosis requires the combined actions of its cognate integrase and Hef, a new recombination directionality factor. Mol Microbiol. 2004;52(5):1337–48. Epub 2004/05/29. doi: 10.1111/j.1365-2958.2004.04073.x 15165237.
20. Wee BA, Woolfit M, Beatson SA, Petty NK. A distinct and divergent lineage of genomic island-associated Type IV Secretion Systems in Legionella. PloS one. 2013;8(12):e82221. Epub 2013/12/21. doi: 10.1371/journal.pone.0082221 24358157
21. Murphy RA, Boyd EF. Three pathogenicity islands of Vibrio cholerae can excise from the chromosome and form circular intermediates. J Bacteriol. 2008;190(2):636–47. Epub 2007/11/13. doi: 10.1128/JB.00562-07 17993521.
22. Quiroz TS, Nieto PA, Tobar HE, Salazar-Echegarai FJ, Lizana RJ, Quezada CP, et al. Excision of an Unstable Pathogenicity Island in Salmonella enterica Serovar Enteritidis Is Induced during Infection of Phagocytic Cells. Plos One. 2011;6(10):13. doi: 10.1371/journal.pone.0026031 22039432
23. Bueno SM, Santiviago CA, Murillo AA, Fuentes JA, Trombert AN, Rodas PI, et al. Precise excision of the large pathogenicity island, SPI7, in Salmonella enterica serovar Typhi. J Bacteriol. 2004;186(10):3202–13. Epub 2004/05/06. doi: 10.1128/JB.186.10.3202-3213.2004 15126483.
24. Nieto PA, Pardo-Roa C, Salazar-Echegarai FJ, Tobar HE, Coronado-Arrazola I, Riedel CA, et al. New insights about excisable pathogenicity islands in Salmonella and their contribution to virulence. Microbes Infect. 2016;18(5):302–9. Epub 2016/03/05. doi: 10.1016/j.micinf.2016.02.001 26939722.
25. Porwollik S, Santiviago CA, Cheng P, Florea L, Jackson S, McClelland M. Differences in gene content between Salmonella enterica serovar Enteritidis isolates and comparison to closely related serovars Gallinarum and Dublin. J Bacteriol. 2005;187(18):6545–55. Epub 2005/09/15. doi: 10.1128/JB.187.18.6545-6555.2005 16159788
26. Thomson NR, Clayton DJ, Windhorst D, Vernikos G, Davidson S, Churcher C, et al. Comparative genome analysis of Salmonella Enteritidis PT4 and Salmonella Gallinarum 287/91 provides insights into evolutionary and host adaptation pathways. Genome Res. 2008;18(10):1624–37. Epub 2008/06/28. doi: 10.1101/gr.077404.108 18583645
27. Piña-Iturbe A, Ulloa-Allendes D, Pardo-Roa C, Coronado-Arrázola I, Salazar-Echegarai FJ, Sclavi B, et al. Comparative and phylogenetic analysis of a novel family of Enterobacteriaceae-associated genomic islands that share a conserved excision/integration module. Sci Rep. 2018;8(1):10292. Epub 2018/07/06. doi: 10.1038/s41598-018-28537-0 29980701
28. Salazar-Echegarai FJ, Tobar HE, Nieto PA, Riedel CA, Bueno SM. Conjugal Transfer of the Pathogenicity Island ROD21 in Salmonella enterica serovar Enteritidis Depends on Environmental Conditions. PLoS One. 2014;9(4):e90626. Epub 2014/04/08. doi: 10.1371/journal.pone.0090626 24705125.
29. Newman RM, Salunkhe P, Godzik A, Reed JC. Identification and characterization of a novel bacterial virulence factor that shares homology with mammalian Toll/interleukin-1 receptor family proteins. Infect Immun. 2006;74(1):594–601. Epub 2005/12/22. doi: 10.1128/IAI.74.1.594-601.2006 16369016.
30. Navarre WW, Porwollik S, Wang Y, McClelland M, Rosen H, Libby SJ, et al. Selective silencing of foreign DNA with low GC content by the H-NS protein in Salmonella. Science. 2006;313(5784):236–8. Epub 2006/06/10. doi: 10.1126/science.1128794 16763111.
31. Dorman CJ. H-NS-like nucleoid-associated proteins, mobile genetic elements and horizontal gene transfer in bacteria. Plasmid. 2014;75:1–11. Epub 2014/07/03. doi: 10.1016/j.plasmid.2014.06.004 24998344.
32. Fang FC, Rimsky S. New insights into transcriptional regulation by H-NS. Curr Opin Microbiol. 2008;11(2):113–20. Epub 2008/04/02. doi: 10.1016/j.mib.2008.02.011 18387844
33. Tobar HE, Salazar-Echegarai FJ, Nieto PA, Palavecino CE, Sebastian VP, Riedel CA, et al. Chromosomal Excision of a New Pathogenicity Island Modulates Salmonella Virulence In Vivo. Current Gene Therapy. 2013;13(4):240–9. doi: 10.2174/1566523211313040002 23746206
34. Feasey NA, Hadfield J, Keddy KH, Dallman TJ, Jacobs J, Deng X, et al. Distinct Salmonella Enteritidis lineages associated with enterocolitis in high-income settings and invasive disease in low-income settings. Nat Genet. 2016;48(10):1211–7. Epub 2016/08/22. doi: 10.1038/ng.3644 27548315
35. Silva CA, Blondel CJ, Quezada CP, Porwollik S, Andrews-Polymenis HL, Toro CS, et al. Infection of mice by Salmonella enterica serovar Enteritidis involves additional genes that are absent in the genome of serovar Typhimurium. Infect Immun. 2012;80(2):839–49. Epub 2011/11/16. doi: 10.1128/IAI.05497-11 22083712.
36. Middendorf B, Hochhut B, Leipold K, Dobrindt U, Blum-Oehler G, Hacker J. Instability of pathogenicity islands in uropathogenic Escherichia coli 536. J Bacteriol. 2004;186(10):3086–96. Epub 2004/05/06. doi: 10.1128/JB.186.10.3086-3096.2004 15126470.
37. Marcoleta AE, Berríos-Pastén C, Nuñez G, Monasterio O, Lagos R. Klebsiella pneumoniae Asparagine tDNAs Are Integration Hotspots for Different Genomic Islands Encoding Microcin E492 Production Determinants and Other Putative Virulence Factors Present in Hypervirulent Strains. Front Microbiol. 2016;7:849. Epub 2016/06/03. doi: 10.3389/fmicb.2016.00849 27375573
38. Almagro-Moreno S, Napolitano MG, Boyd EF. Excision dynamics of Vibrio pathogenicity island-2 from Vibrio cholerae: role of a recombination directionality factor VefA. BMC Microbiol. 2010;10:306. Epub 2010/12/02. doi: 10.1186/1471-2180-10-306 21118541.
39. Vanga BR, Ramakrishnan P, Butler RC, Toth IK, Ronson CW, Jacobs JM, et al. Mobilization of horizontally acquired island 2 is induced in planta in the phytopathogen Pectobacterium atrosepticum SCRI1043 and involves the putative relaxase ECA0613 and quorum sensing. Environ Microbiol. 2015;17(11):4730–44. Epub 2015/08/15. doi: 10.1111/1462-2920.13024 26271942.
40. Carpenter MR, Kalburge SS, Borowski JD, Peters MC, Colwell RR, Boyd EF. CRISPR-Cas and Contact-Dependent Secretion Systems Present on Excisable Pathogenicity Islands with Conserved Recombination Modules. J Bacteriol. 2017;199(10). Epub 2017/04/25. doi: 10.1128/JB.00842-16 28264992
41. Alvarez-Ordóñez A, Begley M, Prieto M, Messens W, López M, Bernardo A, et al. Salmonella spp. survival strategies within the host gastrointestinal tract. Microbiology. 2011;157(Pt 12):3268–81. Epub 2011/10/20. doi: 10.1099/mic.0.050351-0 22016569.
42. Alvarez-Ordóñez A, Fernández A, Bernardo A, López M. Arginine and lysine decarboxylases and the acid tolerance response of Salmonella Typhimurium. Int J Food Microbiol. 2010;136(3):278–82. Epub 2009/10/04. doi: 10.1016/j.ijfoodmicro.2009.09.024 19864032.
43. Audia JP, Webb CC, Foster JW. Breaking through the acid barrier: an orchestrated response to proton stress by enteric bacteria. Int J Med Microbiol. 2001;291(2):97–106. doi: 10.1078/1438-4221-00106 11437344.
44. Patel S, McCormick BA. Mucosal Inflammatory Response to Salmonella Typhimurium Infection. Front Immunol. 2014;5:311. Epub 2014/07/04. doi: 10.3389/fimmu.2014.00311 25071772
45. Erhardt M, Dersch P. Regulatory principles governing Salmonella and Yersinia virulence. Front Microbiol. 2015;6:949. Epub 2015/09/09. doi: 10.3389/fmicb.2015.00949 26441883
46. Alonso-Hernando A, Alonso-Calleja C, Capita R. Effects of exposure to poultry chemical decontaminants on the membrane fluidity of Listeria monocytogenes and Salmonella enterica strains. Int J Food Microbiol. 2010;137(2–3):130–6. Epub 2009/12/03. doi: 10.1016/j.ijfoodmicro.2009.11.022 20056288.
47. Wei Y, Miller CG. Characterization of a group of anaerobically induced, fnr-dependent genes of Salmonella Typhimurium. J Bacteriol. 1999;181(19):6092–7. 10498722
48. Sevcík M, Sebková A, Volf J, Rychlík I. Transcription of arcA and rpoS during growth of Salmonella Typhimurium under aerobic and microaerobic conditions. Microbiology. 2001;147(Pt 3):701–8. doi: 10.1099/00221287-147-3-701 11238977.
49. Gart EV, Suchodolski JS, Welsh TH, Alaniz RC, Randel RD, Lawhon SD. Salmonella Typhimurium and Multidirectional Communication in the Gut. Front Microbiol. 2016;7:1827. Epub 2016/11/22. doi: 10.3389/fmicb.2016.01827 27920756
50. Navarre WW, Halsey TA, Walthers D, Frye J, McClelland M, Potter JL, et al. Co-regulation of Salmonella enterica genes required for virulence and resistance to antimicrobial peptides by SlyA and PhoP/PhoQ. Mol Microbiol. 2005;56(2):492–508. Epub 2005/04/09. doi: 10.1111/j.1365-2958.2005.04553.x 15813739.
51. Groisman EA. The pleiotropic two-component regulatory system PhoP-PhoQ. J Bacteriol. 2001;183(6):1835–42. Epub 2001/02/27. doi: 10.1128/JB.183.6.1835-1842.2001 11222580
52. Hacker J, Blum-Oehler G, Muhldorfer I, Tschape H. Pathogenicity islands of virulent bacteria: structure, function and impact on microbial evolution. Mol Microbiol. 1997;23(6):1089–97. Epub 1997/03/01. doi: 10.1046/j.1365-2958.1997.3101672.x 9106201.
53. Galán JE, Ginocchio C, Costeas P. Molecular and functional characterization of the Salmonella invasion gene invA: homology of InvA to members of a new protein family. J Bacteriol. 1992;174(13):4338–49. doi: 10.1128/jb.174.13.4338-4349.1992 1624429
54. Rüssmann H, Kubori T, Sauer J, Galán JE. Molecular and functional analysis of the type III secretion signal of the Salmonella enterica InvJ protein. Mol Microbiol. 2002;46(3):769–79. doi: 10.1046/j.1365-2958.2002.03196.x 12410834.
55. Scolari VF, Sclavi B, Cosentino Lagomarsino M. The nucleoid as a smart polymer. Front Microbiol. 2015;6:424. Epub 2015/05/26. doi: 10.3389/fmicb.2015.00424 26005440
56. Ali SS, Soo J, Rao C, Leung AS, Ngai DH, Ensminger AW, et al. Silencing by H-NS potentiated the evolution of Salmonella. PLoS Pathog. 2014;10(11):e1004500. Epub 2014/11/07. doi: 10.1371/journal.ppat.1004500 25375226
57. Galán JE, Curtiss R. Expression of Salmonella Typhimurium genes required for invasion is regulated by changes in DNA supercoiling. Infect Immun. 1990;58(6):1879–85. 2160435
58. Neale HC, Jackson RW, Preston GM, Arnold DL. Supercoiling of an excised genomic island represses effector gene expression to prevent activation of host resistance. Mol Microbiol. 2018;110(3):444–54. Epub 2018/10/03. doi: 10.1111/mmi.14111 30152900
59. Godfrey SA, Lovell HC, Mansfield JW, Corry DS, Jackson RW, Arnold DL. The stealth episome: suppression of gene expression on the excised genomic island PPHGI-1 from Pseudomonas syringae pv. phaseolicola. PLoS Pathog. 2011;7(3):e1002010. Epub 2011/04/13. doi: 10.1371/journal.ppat.1002010 21483484
60. Datsenko KA, Wanner BL. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci U S A. 2000;97(12):6640–5. Epub 2000/06/01. doi: 10.1073/pnas.120163297 10829079
61. Lee C, Kim J, Shin SG, Hwang S. Absolute and relative QPCR quantification of plasmid copy number in Escherichia coli. J Biotechnol. 2006;123(3):273–80. Epub 2006/01/04. doi: 10.1016/j.jbiotec.2005.11.014 16388869.
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