Gut inflammation can boost horizontal gene transfer between pathogenic and commensal Enterobacteriaceae

Proceedings of the National Academy of Sciences of the United States of America

Volumn 109, Issue 4, 2012, Pages 1269-1274

  Stecher, Bärbel ^a,b   Denzler, Rémy ^a   Maier, Lisa ^a   Bernet, Florian ^a   Sanders, Mandy J ^c   Pickard, Derek J ^c   Barthel, Manja ^a   Westendorf, Astrid M ^d   Krogfelt, Karen A ^e   Walker, Alan W ^c   Ackermann, Martin ^a,f   Dobrindt, Ulrich ^g,h   Thomson, Nicholas R ^c   Hardt, Wolf Dietrich ^a  

^a ETH ZURICH   (Switzerland)

^b UNIVERSITY OF MUNICH   (Germany)

^c WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

^d UNIVERSITY OF DUISBURG ESSEN   (Germany)

^e STATENS SERUM INSTITUT   (Denmark)

^f Department of Environmental Microbiology ^*  (Switzerland)

^g UNIVERSITY OF WÜRZBURG   (Germany)

^h UNIVERSITY OF MÜNSTER   (Germany)

Author keywords

Bacterial evolution; Hospital acquired infection; Mucosal immune response; Plasmid spread

Indexed keywords

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL VIRULENCE; COMMENSAL ESCHERICHIA COLI; CONTROLLED STUDY; ENTEROBACTERIACEAE; ENTEROPATHY; HORIZONTAL GENE TRANSFER; IN VIVO STUDY; INFLAMMATION; INTESTINE; MOUSE; NONHUMAN; PLASMID; PRIORITY JOURNAL; SALMONELLA TYPHIMURIUM; SALMONELLOSIS;

ANIMALS; BACTERIOCIN PLASMIDS; BASE SEQUENCE; BIOLOGICAL EVOLUTION; COLITIS; COMPUTATIONAL BIOLOGY; DNA PRIMERS; ENTEROBACTERIACEAE; ESCHERICHIA COLI; GENE TRANSFER, HORIZONTAL; MICE; MOLECULAR SEQUENCE DATA; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PHYLOGENY; RNA, RIBOSOMAL, 16S; SALMONELLA TYPHIMURIUM; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS, DNA;

BACTERIA (MICROORGANISMS); ENTEROBACTERIACEAE; ESCHERICHIA COLI; MAMMALIA; NEGIBACTERIA; SALMONELLA; SALMONELLA ENTERICA SUBSP. ENTERICA SEROVAR TYPHIMURIUM;

EID: 84856374839     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1113246109     Document Type: Article

References (46)

1. Round JL, Mazmanian SK (2009) The gut microbiota shapes intestinal immune responses during health and disease. Nat Rev Immunol 9:313-323.
2. Qin J, et al.; MetaHIT Consortium (2010) A human gut microbial gene catalogue established by metagenomic sequencing. Nature 464:59-65.
3. Arumugam M, et al. (2011) Enterotypes of the human gut microbiome. Nature 470:510-512.
4. Treangen TJ, Rocha EP (2011) Horizontal transfer, not duplication, drives the expansion of protein families in prokaryotes. PLoS Genet 7:e1001284.
5. Hehemann JH, et al. (2009) Transfer of carbohydrate-active enzymes from marine bacteria to Japanese gut microbiota. (Translated from eng). Nature 464:908-912.
6. Nelson KE, et al.; Human Microbiome Jumpstart Reference Strains Consortium (2010) A catalog of reference genomes from the human microbiome. Science 328:994-999.
7. Paulsen IT, et al. (2003) Role of mobile DNA in the evolution of vancomycin-resistant Enterococcus faecalis. Science 299:2071-2074. (Pubitemid 36383734)
8. Johnson TJ, et al. (2010) Horizontal gene transfer of a ColV plasmid has resulted in a dominant avian clonal type of Salmonella enterica serovar Kentucky. PLoS ONE 5:e15524.
9. Bielaszewska M, et al. (2011) Characterisation of the Escherichia coli strain associated with an outbreak of haemolytic uraemic syndrome in Germany, 2011: A microbiological study. Lancet Infect Dis 11:671-676.
10. Tenaillon O, Skurnik D, Picard B, Denamur E (2010) The population genetics of commensal Escherichia coli. Nat Rev Microbiol 8:207-217.
11. Scott KP (2002) The role of conjugative transposons in spreading antibiotic resistance between bacteria that inhabit the gastrointestinal tract. Cell Mol Life Sci 59:2071-2082. (Pubitemid 36140280)
12. Bohnhoff M, Drake BL, Miller CP (1954) Effect of streptomycin on susceptibility of intestinal tract to experimental Salmonella infection. Proc Soc Exp Biol NY 86:132-137.
13. van der Waaij D, Berghuis-de Vries JM, Lekkerkerk Lekkerkerk-v (1971) Colonization resistance of the digestive tract in conventional and antibiotic-treated mice. J Hyg (Lond) 69:405-411.
14. Berg RD (1996) The indigenous gastrointestinal microflora. Trends Microbiol 4:430-435.
15. Licht TR, Christensen BB, Krogfelt KA, Molin S (1999) Plasmid transfer in the animal intestine and other dynamic bacterial populations: the role of community structure and environment. Microbiology 145:2615-2622. (Pubitemid 29454380)
16. Daniels JB, Call DR, Besser TE (2007) Molecular epidemiology of blaCMY-2 plasmids carried by Salmonella enterica and Escherichia coli isolates from cattle in the Pacific Northwest. Appl Environ Microbiol 73:8005-8011. (Pubitemid 350308819)
17. Smet A, et al. (2011) In situ ESBL conjugation from avian to human Escherichia coli during cefotaxime administration. J Appl Microbiol 110:541-549.
18. Moubareck C, Bourgeois N, Courvalin P, Doucet-Populaire F (2003) Multiple antibiotic resistance gene transfer from animal to human enterococci in the digestive tract of gnotobiotic mice. Antimicrob Agents Chemother 47:2993-2996. (Pubitemid 37040285)
19. Faure S, Perrin-Guyomard A, Delmas JM, Chatre P, Laurentie M (2010) Transfer of plasmid-mediated CTX-M-9 from Salmonella enterica serotype Virchow to Enterobacteriaceae in human flora-associated rats treated with cefixime. Antimicrob Agents Chemother 54:164-169.
20. Lupp C, et al. (2007) Host-mediated inflammation disrupts the intestinal microbiota and promotes the overgrowth of Enterobacteriaceae. Cell Host Microbe 2:119-129. (Pubitemid 47209521)
21. Stecher B, et al. (2007) Salmonella enterica serovar Typhimurium exploits inflammation to compete with the intestinal microbiota. (Translated from Eng). PLoS Biol 5:e244.
22. Pédron T, Sansonetti P (2008) Commensals, bacterial pathogens and intestinal inflammation: an intriguing ménage à trois. Cell Host Microbe 3:344-347. (Pubitemid 351773104)
23. Winter SE, et al. (2010) Gut inflammation provides a respiratory electron acceptor for Salmonella. Nature 467:426-429.
24. Darfeuille-Michaud A, et al. (2004) High prevalence of adherent-invasive Escherichia coli associated with ileal mucosa in Crohn's disease. Gastroenterology 127:412-421. (Pubitemid 39091889)
25. Barthel M, et al. (2003) Pretreatment of mice with streptomycin provides a Salmonella enterica serovar Typhimurium colitis model that allows analysis of both pathogen and host. Infect Immun 71:2839-2858. (Pubitemid 36519898)
26. Stecher B, et al. (2010) Like will to like: abundances of closely related species can predict susceptibility to intestinal colonization by pathogenic and commensal bacteria. PLoS Pathog 6:e1000711.
27. Brzuszkiewicz E, et al. (2006) How to become a uropathogen: comparative genomic analysis of extraintestinal pathogenic Escherichia coli strains. Proc Natl Acad Sci USA 103:12879-12884. (Pubitemid 44298655)
28. Welch RA, et al. (2002) Extensive mosaic structure revealed by the complete genome sequence of uropathogenic Escherichia coli. Proc Natl Acad Sci USA 99:17020-17024. (Pubitemid 36034091)
29. Kim SR, Komano T (1997) The plasmid R64 thin pilus identified as a type IV pilus. J Bacteriol 179:3594-3603.
30. Komano T, Yoshida T, Narahara K, Furuya N (2000) The transfer region of IncI1 plasmid R64: Similarities between R64 tra and legionella icm/dot genes. Mol Microbiol 35:1348-1359. (Pubitemid 30175511)
31. Sampei G, et al. (2010) Complete genome sequence of the incompatibility group I1 plasmid R64. Plasmid 64:92-103.
32. Komano T, Kubo A, Nisioka T (1987) Shufflon: Multi-inversion of four contiguous DNA segments of plasmid R64 creates seven different open reading frames. Nucleic Acids Res 15:1165-1172.
33. Cascales E, et al. (2007) Colicin biology. Microbiol Mol Biol Rev 71:158-229. (Pubitemid 46456687)
34. Kerr B, Riley MA, Feldman MW, Bohannan BJ (2002) Local dispersal promotes biodiversity in a real-life game of rock-paper-scissors. Nature 418:171-174. (Pubitemid 34773769)
35. Sonnenborn U, Schulze J (2009) The non-pathogenic Escherichia coli strain Nissle 1917 - features of a versatile probiotic. Microb Ecol Health Dis 21:122-158.
36. Hapfelmeier S, et al. (2005) The Salmonella pathogenicity island (SPI)-2 and SPI-1 type III secretion systems allow Salmonella serovar typhimurium to trigger colitis via MyD88-dependent and MyD88-independent mechanisms. J Immunol 174:1675-1685.
37. Dewhirst FE, et al. (1999) Phylogeny of the defined murine microbiota: Altered Schaedler flora. Appl Environ Microbiol 65:3287-3292. (Pubitemid 29398945)
38. Stecher B, Hardt WD (2010) Mechanisms controlling pathogen colonization of the gut. Curr Opin Microbiol 14:82-91.
39. Pfeifer Y, Cullik A, Witte W (2010) Resistance to cephalosporins and carbapenems in Gram-negative bacterial pathogens. Int J Med Microbiol 300:371-379.
40. Bergstrom CT, Lipsitch M, Levin BR (2000) Natural selection, infectious transfer and the existence conditions for bacterial plasmids. Genetics 155:1505-1519. (Pubitemid 30626375)
41. Dionisio F, Matic I, Radman M, Rodrigues OR, Taddei F (2002) Plasmids spread very fast in heterogeneous bacterial communities. Genetics 162:1525-1532. (Pubitemid 36114643)
42. Hapfelmeier S, et al. (2004) Role of the Salmonella pathogenicity island 1 effector proteins SipA, SopB, SopE, and SopE2 in Salmonella enterica subspecies 1 serovar Typhimurium colitis in streptomycin-pretreated mice. Infect Immun 72:795-809. (Pubitemid 38166658)
43. Clermont O, Bonacorsi S, Bingen E (2000) Rapid and simple determination of the Escherichia coli phylogenetic group. Appl Environ Microbiol 66:4555-4558.
44. Westendorf AM, et al. (2006) Autoimmune-mediated intestinal inflammation-impact and regulation of antigen-specific CD8+ T cells. Gastroenterology 131:510-524. (Pubitemid 44142451)
45. Stecher B, et al. (2008) Motility allows S. Typhimurium to benefit from the mucosal defence. Cell Microbiol 10:1166-1180. (Pubitemid 351524280)
46. Wang RF, Kushner SR (1991) Construction of versatile low-copy-number vectors for cloning, sequencing and gene expression in Escherichia coli. Gene 100:195-199.