Salmonella Typhimurium Diarrhea Reveals Basic Principles of Enteropathogen Infection and Disease-Promoted DNA Exchange

Cell Host and Microbe

Volumn 21, Issue 4, 2017, Pages 443-454

  Wotzka, Sandra Y ^a   Nguyen, Bidong D ^a   Hardt, Wolf Dietrich ^a  

^a ETH ZURICH   (Switzerland)

Author keywords

antibody; epithelium; inflammasome; inflammation; microbiota; mucosa; NLRC4; phage; plasmid; secretory IgA

Indexed keywords

BACTERIAL DNA; STREPTOMYCIN;

ANTIBIOTIC RESISTANCE; BACTERIAL GROWTH; DIARRHEA; GENE TRANSFER; IMMUNITY; INTESTINE FLORA; NONHUMAN; PATHOGEN LOAD; PRIORITY JOURNAL; REVIEW; SALMONELLA ENTERICA SEROVAR TYPHIMURIUM; SPECIES COMPOSITION; VACCINATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; HORIZONTAL GENE TRANSFER; HOST PATHOGEN INTERACTION; INNATE IMMUNITY; INTERSPERSED REPEAT; INTESTINE MUCOSA; MICROBIOLOGY; PATHOGENICITY; PATHOLOGY; SALMONELLOSIS;

DIARRHEA; GENE TRANSFER, HORIZONTAL; HOST-PATHOGEN INTERACTIONS; IMMUNITY, INNATE; INTERSPERSED REPETITIVE SEQUENCES; INTESTINAL MUCOSA; SALMONELLA INFECTIONS; SALMONELLA TYPHIMURIUM;

EID: 85017374567     PISSN: 19313128     EISSN: 19346069     Source Type: Journal    
DOI: 10.1016/j.chom.2017.03.009     Document Type: Review

References (122)

1. Ackermann, M., Stecher, B., Freed, N.E., Songhet, P., Hardt, W.D., Doebeli, M., Self-destructive cooperation mediated by phenotypic noise. Nature 454 (2008), 987–990.
2. Arumugam, M., Raes, J., Pelletier, E., Le Paslier, D., Yamada, T., Mende, D.R., Fernandes, G.R., Tap, J., Bruls, T., Batto, J.M., et al., MetaHIT Consortium. Enterotypes of the human gut microbiome. Nature 473 (2011), 174–180.
3. Barthel, M., Hapfelmeier, S., Quintanilla-Martínez, L., Kremer, M., Rohde, M., Hogardt, M., Pfeffer, K., Rüssmann, H., Hardt, W.D., Pretreatment of mice with streptomycin provides a Salmonella enterica serovar Typhimurium colitis model that allows analysis of both pathogen and host. Infect. Immun. 71 (2003), 2839–2858.
4. Basler, M., Ho, B.T., Mekalanos, J.J., Tit-for-tat: type VI secretion system counterattack during bacterial cell-cell interactions. Cell 152 (2013), 884–894.
5. Behnsen, J., Jellbauer, S., Wong, C.P., Edwards, R.A., George, M.D., Ouyang, W., Raffatellu, M., The cytokine IL-22 promotes pathogen colonization by suppressing related commensal bacteria. Immunity 40 (2014), 262–273.
6. Brugiroux, S., Beutler, M., Pfann, C., Garzetti, D., Ruscheweyh, H.J., Ring, D., Diehl, M., Herp, S., Lötscher, Y., Hussain, S., et al. Genome-guided design of a defined mouse microbiota that confers colonization resistance against Salmonella enterica serovar Typhimurium. Nat. Microbiol., 2, 2016, 16215.
7. Brüssow, H., Canchaya, C., Hardt, W.D., Phages and the evolution of bacterial pathogens: from genomic rearrangements to lysogenic conversion. Microbiol. Mol. Biol. Rev. 68 (2004), 560–602.
8. Buffie, C.G., Bucci, V., Stein, R.R., McKenney, P.T., Ling, L., Gobourne, A., No, D., Liu, H., Kinnebrew, M., Viale, A., et al. Precision microbiome reconstitution restores bile acid mediated resistance to Clostridium difficile. Nature 517 (2015), 205–208.
9. Chatzidaki-Livanis, M., Geva-Zatorsky, N., Comstock, L.E., Bacteroides fragilis type VI secretion systems use novel effector and immunity proteins to antagonize human gut Bacteroidales species. Proc. Natl. Acad. Sci. USA 113 (2016), 3627–3632.
10. Chudnovskiy, A., Mortha, A., Kana, V., Kennard, A., Ramirez, J.D., Rahman, A., Remark, R., Mogno, I., Ng, R., Gnjatic, S., et al. Host-protozoan interactions protect from mucosal infections through activation of the inflammasome. Cell 167 (2016), 444–456.e14.
11. Dethlefsen, L., McFall-Ngai, M., Relman, D.A., An ecological and evolutionary perspective on human-microbe mutualism and disease. Nature 449 (2007), 811–818.
12. Diard, M., Bakkeren, E., Cornuault, J.K., Moor, K., Hausmann, A., Sellin, M.E., Loverdo, C., Aertsen, A., Ackermann, M., De Paepe, M., et al. Inflammation boosts bacteriophage transfer between Salmonella spp. Science 355 (2017), 1211–1215.
13. Dolowschiak, T., Mueller, A.A., Pisan, L.J., Feigelman, R., Felmy, B., Sellin, M.E., Namineni, S., Nguyen, B.D., Wotzka, S.Y., Heikenwalder, M., et al. IFN-γ hinders recovery from mucosal inflammation during antibiotic therapy for Salmonella gut infection. Cell Host Microbe 20 (2016), 238–249.
14. Duerkop, B.A., Clements, C.V., Rollins, D., Rodrigues, J.L., Hooper, L.V., A composite bacteriophage alters colonization by an intestinal commensal bacterium. Proc. Natl. Acad. Sci. USA 109 (2012), 17621–17626.
15. Endt, K., Stecher, B., Chaffron, S., Slack, E., Tchitchek, N., Benecke, A., Van Maele, L., Sirard, J.C., Mueller, A.J., Heikenwalder, M., et al. The microbiota mediates pathogen clearance from the gut lumen after non-typhoidal Salmonella diarrhea. PLoS Pathog., 6, 2010, e1001097.
16. Faber, F., Tran, L., Byndloss, M.X., Lopez, C.A., Velazquez, E.M., Kerrinnes, T., Nuccio, S.P., Wangdi, T., Fiehn, O., Tsolis, R.M., Bäumler, A.J., Host-mediated sugar oxidation promotes post-antibiotic pathogen expansion. Nature 534 (2016), 697–699.
17. Faber, F., Thiennimitr, P., Spiga, L., Byndloss, M.X., Litvak, Y., Lawhon, S., Andrews-Polymenis, H.L., Winter, S.E., Bäumler, A.J., Respiration of microbiota-derived 1,2-propanediol drives Salmonella expansion during colitis. PLoS Pathog., 13, 2017, e1006129.
18. Fabich, A.J., Jones, S.A., Chowdhury, F.Z., Cernosek, A., Anderson, A., Smalley, D., McHargue, J.W., Hightower, G.A., Smith, J.T., Autieri, S.M., et al. Comparison of carbon nutrition for pathogenic and commensal Escherichia coli strains in the mouse intestine. Infect. Immun. 76 (2008), 1143–1152.
19. Felmy, B., Songhet, P., Slack, E.M., Müller, A.J., Kremer, M., Van Maele, L., Cayet, D., Heikenwalder, M., Sirard, J.C., Hardt, W.D., NADPH oxidase deficient mice develop colitis and bacteremia upon infection with normally avirulent, TTSS-1- and TTSS-2-deficient Salmonella Typhimurium. PLoS ONE, 8, 2013, e77204.
20. Ferreyra, J.A., Wu, K.J., Hryckowian, A.J., Bouley, D.M., Weimer, B.C., Sonnenburg, J.L., Gut microbiota-produced succinate promotes C. difficile infection after antibiotic treatment or motility disturbance. Cell Host Microbe 16 (2014), 770–777.
21. Fischer, M., Sipe, B., Cheng, Y.W., Phelps, E., Rogers, N., Sagi, S., Bohm, M., Xu, H., Kassam, Z., Fecal microbiota transplant in severe and severe-complicated Clostridium difficile: a promising treatment approach. Gut Microbes, 2016, 10.1080/19490976.2016.1273998 Published online December 21, 2016.
22. Forbes, S.J., Martinelli, D., Hsieh, C., Ault, J.G., Marko, M., Mannella, C.A., Mantis, N.J., Association of a protective monoclonal IgA with the O antigen of Salmonella enterica serovar Typhimurium impacts type 3 secretion and outer membrane integrity. Infect. Immun. 80 (2012), 2454–2463.
23. Freter, R., Brickner, H., Botney, M., Cleven, D., Aranki, A., Mechanisms that control bacterial populations in continuous-flow culture models of mouse large intestinal flora. Infect. Immun. 39 (1983), 676–685.
24. Gantois, I., Ducatelle, R., Pasmans, F., Haesebrouck, F., Hautefort, I., Thompson, A., Hinton, J.C., Van Immerseel, F., Butyrate specifically down-regulates salmonella pathogenicity island 1 gene expression. Appl. Environ. Microbiol. 72 (2006), 946–949.
25. Gerlach, R.G., Jäckel, D., Stecher, B., Wagner, C., Lupas, A., Hardt, W.D., Hensel, M., Salmonella pathogenicity island 4 encodes a giant non-fimbrial adhesin and the cognate type 1 secretion system. Cell. Microbiol. 9 (2007), 1834–1850.
26. Giannella, R.A., Broitman, S.A., Zamcheck, N., Gastric acid barrier to ingested microorganisms in man: studies in vivo and in vitro. Gut 13 (1972), 251–256.
27. Gilmore, M.S., Rauch, M., Ramsey, M.M., Himes, P.R., Varahan, S., Manson, J.M., Lebreton, F., Hancock, L.E., Pheromone killing of multidrug-resistant Enterococcus faecalis V583 by native commensal strains. Proc. Natl. Acad. Sci. USA 112 (2015), 7273–7278.
28. Godinez, I., Haneda, T., Raffatellu, M., George, M.D., Paixão, T.A., Rolán, H.G., Santos, R.L., Dandekar, S., Tsolis, R.M., Bäumler, A.J., T cells help to amplify inflammatory responses induced by Salmonella enterica serotype Typhimurium in the intestinal mucosa. Infect. Immun. 76 (2008), 2008–2017.
29. Hachani, A., Allsopp, L.P., Oduko, Y., Filloux, A., The VgrG proteins are “à la carte” delivery systems for bacterial type VI effectors. J. Biol. Chem. 289 (2014), 17872–17884.
30. Hapfelmeier, S., Hardt, W.D., A mouse model for S. typhimurium-induced enterocolitis. Trends Microbiol. 13 (2005), 497–503.
31. Hapfelmeier, S., Ehrbar, K., Stecher, B., Barthel, M., Kremer, M., Hardt, W.D., 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 (2004), 795–809.
32. Hapfelmeier, S., Stecher, B., Barthel, M., Kremer, M., Müller, A.J., Heikenwalder, M., Stallmach, T., Hensel, M., Pfeffer, K., Akira, S., Hardt, W.D., 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 (2005), 1675–1685.
33. Hapfelmeier, S., Müller, A.J., Stecher, B., Kaiser, P., Barthel, M., Endt, K., Eberhard, M., Robbiani, R., Jacobi, C.A., Heikenwalder, M., et al. Microbe sampling by mucosal dendritic cells is a discrete, MyD88-independent step in DeltainvG S. Typhimurium colitis. J. Exp. Med. 205 (2008), 437–450.
34. Hardt, W.D., Chen, L.M., Schuebel, K.E., Bustelo, X.R., Galán, J.E., S. typhimurium encodes an activator of Rho GTPases that induces membrane ruffling and nuclear responses in host cells. Cell 93 (1998), 815–826.
35. Harrington, L., Srikanth, C.V., Antony, R., Shi, H.N., Cherayil, B.J., A role for natural killer cells in intestinal inflammation caused by infection with Salmonella enterica serovar Typhimurium. FEMS Immunol. Med. Microbiol. 51 (2007), 372–380.
36. Ho, B.T., Dong, T.G., Mekalanos, J.J., A view to a kill: the bacterial type VI secretion system. Cell Host Microbe 15 (2014), 9–21.
37. Hu, B., Elinav, E., Huber, S., Booth, C.J., Strowig, T., Jin, C., Eisenbarth, S.C., Flavell, R.A., Inflammation-induced tumorigenesis in the colon is regulated by caspase-1 and NLRC4. Proc. Natl. Acad. Sci. USA 107 (2010), 21635–21640.
38. Human Microbiome Project Consortium. Structure, function and diversity of the healthy human microbiome. Nature 486 (2012), 207–214.
39. Jellbauer, S., Perez Lopez, A., Behnsen, J., Gao, N., Nguyen, T., Murphy, C., Edwards, R.A., Raffatellu, M., Beneficial effects of sodium phenylbutyrate administration during infection with Salmonella enterica serovar Typhimurium. Infect. Immun. 84 (2016), 2639–2652.
40. Jones, S.A., Gibson, T., Maltby, R.C., Chowdhury, F.Z., Stewart, V., Cohen, P.S., Conway, T., Anaerobic respiration of Escherichia coli in the mouse intestine. Infect. Immun. 79 (2011), 4218–4226.
41. Kaiser, P., Diard, M., Stecher, B., Hardt, W.D., The streptomycin mouse model for Salmonella diarrhea: functional analysis of the microbiota, the pathogen's virulence factors, and the host's mucosal immune response. Immunol. Rev. 245 (2012), 56–83.
42. Kaiser, P., Slack, E., Grant, A.J., Hardt, W.D., Regoes, R.R., Lymph node colonization dynamics after oral Salmonella Typhimurium infection in mice. PLoS Pathog., 9, 2013, e1003532.
43. Knodler, L.A., Vallance, B.A., Celli, J., Winfree, S., Hansen, B., Montero, M., Steele-Mortimer, O., Dissemination of invasive Salmonella via bacterial-induced extrusion of mucosal epithelia. Proc. Natl. Acad. Sci. USA 107 (2010), 17733–17738.
44. Knodler, L.A., Crowley, S.M., Sham, H.P., Yang, H., Wrande, M., Ma, C., Ernst, R.K., Steele-Mortimer, O., Celli, J., Vallance, B.A., Noncanonical inflammasome activation of caspase-4/caspase-11 mediates epithelial defenses against enteric bacterial pathogens. Cell Host Microbe 16 (2014), 249–256.
45. Lagkouvardos, I., Pukall, R., Abt, B., Foesel, B.U., Meier-Kolthoff, J.P., Kumar, N., Bresciani, A., Martínez, I., Just, S., Ziegler, C., et al. The Mouse Intestinal Bacterial Collection (miBC) provides host-specific insight into cultured diversity and functional potential of the gut microbiota. Nat. Microbiol., 1, 2016, 16131.
46. Lam, L.H., Monack, D.M., Intraspecies competition for niches in the distal gut dictate transmission during persistent Salmonella infection. PLoS Pathog., 10, 2014, e1004527.
47. Lara-Tejero, M., Sutterwala, F.S., Ogura, Y., Grant, E.P., Bertin, J., Coyle, A.J., Flavell, R.A., Galán, J.E., Role of the caspase-1 inflammasome in Salmonella typhimurium pathogenesis. J. Exp. Med. 203 (2006), 1407–1412.
48. Lawhon, S.D., Maurer, R., Suyemoto, M., Altier, C., Intestinal short-chain fatty acids alter Salmonella typhimurium invasion gene expression and virulence through BarA/SirA. Mol. Microbiol. 46 (2002), 1451–1464.
49. Lawley, T.D., Bouley, D.M., Hoy, Y.E., Gerke, C., Relman, D.A., Monack, D.M., Host transmission of Salmonella enterica serovar Typhimurium is controlled by virulence factors and indigenous intestinal microbiota. Infect. Immun. 76 (2008), 403–416.
50. Li, H., Limenitakis, J.P., Fuhrer, T., Geuking, M.B., Lawson, M.A., Wyss, M., Brugiroux, S., Keller, I., Macpherson, J.A., Rupp, S., et al. The outer mucus layer hosts a distinct intestinal microbial niche. Nat. Commun., 6, 2015, 8292.
51. Lupp, C., Robertson, M.L., Wickham, M.E., Sekirov, I., Champion, O.L., Gaynor, E.C., Finlay, B.B., Host-mediated inflammation disrupts the intestinal microbiota and promotes the overgrowth of Enterobacteriaceae. Cell Host Microbe 2 (2007), 119–129.
52. Maier, R.J., Use of molecular hydrogen as an energy substrate by human pathogenic bacteria. Biochem. Soc. Trans. 33 (2005), 83–85.
53. Maier, R.J., Olczak, A., Maier, S., Soni, S., Gunn, J., Respiratory hydrogen use by Salmonella enterica serovar Typhimurium is essential for virulence. Infect. Immun. 72 (2004), 6294–6299.
54. Maier, L., Vyas, R., Cordova, C.D., Lindsay, H., Schmidt, T.S., Brugiroux, S., Periaswamy, B., Bauer, R., Sturm, A., Schreiber, F., et al. Microbiota-derived hydrogen fuels Salmonella typhimurium invasion of the gut ecosystem. Cell Host Microbe 14 (2013), 641–651.
55. Maier, L., Barthel, M., Stecher, B., Maier, R.J., Gunn, J.S., Hardt, W.D., Salmonella Typhimurium strain ATCC14028 requires H2-hydrogenases for growth in the gut, but not at systemic sites. PLoS ONE, 9, 2014, e110187.
56. Maier, L., Diard, M., Sellin, M.E., Chouffane, E.S., Trautwein-Weidner, K., Periaswamy, B., Slack, E., Dolowschiak, T., Stecher, B., Loverdo, C., et al. Granulocytes impose a tight bottleneck upon the gut luminal pathogen population during Salmonella typhimurium colitis. PLoS Pathog., 10, 2014, e1004557.
57. Maltez, V.I., Tubbs, A.L., Cook, K.D., Aachoui, Y., Falcone, E.L., Holland, S.M., Whitmire, J.K., Miao, E.A., Inflammasomes coordinate pyroptosis and natural killer cell cytotoxicity to clear infection by a ubiquitous environmental bacterium. Immunity 43 (2015), 987–997.
58. McNorton, M.M., Maier, R.J., Roles of H2 uptake hydrogenases in Shigella flexneri acid tolerance. Microbiology 158 (2012), 2204–2212.
59. Michetti, P., Mahan, M.J., Slauch, J.M., Mekalanos, J.J., Neutra, M.R., Monoclonal secretory immunoglobulin A protects mice against oral challenge with the invasive pathogen Salmonella typhimurium. Infect. Immun. 60 (1992), 1786–1792.
60. Michetti, P., Porta, N., Mahan, M.J., Slauch, J.M., Mekalanos, J.J., Blum, A.L., Kraehenbuhl, J.P., Neutra, M.R., Monoclonal immunoglobulin A prevents adherence and invasion of polarized epithelial cell monolayers by Salmonella typhimurium. Gastroenterology 107 (1994), 915–923.
61. Miki, T., Hardt, W.D., Outer membrane permeabilization is an essential step in the killing of gram-negative bacteria by the lectin RegIIIβ. PLoS ONE, 8, 2013, e69901.
62. Miki, T., Holst, O., Hardt, W.D., The bactericidal activity of the C-type lectin RegIIIβ against Gram-negative bacteria involves binding to lipid A. J. Biol. Chem. 287 (2012), 34844–34855.
63. Miki, T., Goto, R., Fujimoto, M., Okada, N., Hardt, W.D., The bactericidal lectin RegIIIβ prolongs gut colonization and enteropathy in the streptomycin mouse model for Salmonella diarrhea. Cell Host Microbe 21 (2017), 195–207.
64. Mirold, S., Rabsch, W., Rohde, M., Stender, S., Tschäpe, H., Rüssmann, H., Igwe, E., Hardt, W.D., Isolation of a temperate bacteriophage encoding the type III effector protein SopE from an epidemic Salmonella typhimurium strain. Proc. Natl. Acad. Sci. USA 96 (1999), 9845–9850.
65. Moor, K., Wotzka, S.Y., Toska, A., Diard, M., Hapfelmeier, S., Slack, E., Peracetic acid treatment generates potent inactivated oral vaccines from a broad range of culturable bacterial species. Front. Immunol., 7, 2016, 34.
66. Moor, K., Diard, M., Sellin, M.E., Felmy, B., Wotzka, S.Y., Toska, A., Bakkeren, E., Arnoldini, M., Bansept, F., Dal Co, A., et al. High-avidity IgA protects the intestine by enchaining growing bacteria. Nature, 2017, 10.1038/nature22058 Published online April 12, 2017.
67. Müller, A.J., Hoffmann, C., Galle, M., Van Den Broeke, A., Heikenwalder, M., Falter, L., Misselwitz, B., Kremer, M., Beyaert, R., Hardt, W.D., The S. Typhimurium effector SopE induces caspase-1 activation in stromal cells to initiate gut inflammation. Cell Host Microbe 6 (2009), 125–136.
68. Müller, A.J., Kaiser, P., Dittmar, K.E., Weber, T.C., Haueter, S., Endt, K., Songhet, P., Zellweger, C., Kremer, M., Fehling, H.J., Hardt, W.D., Salmonella gut invasion involves TTSS-2-dependent epithelial traversal, basolateral exit, and uptake by epithelium-sampling lamina propria phagocytes. Cell Host Microbe 11 (2012), 19–32.
69. Müller, A.A., Dolowschiak, T., Sellin, M.E., Felmy, B., Verbree, C., Gadient, S., Westermann, A.J., Vogel, J., LeibundGut-Landmann, S., Hardt, W.D., An NK cell perforin response elicited via IL-18 controls mucosal inflammation kinetics during Salmonella gut infection. PLoS Pathog., 12, 2016, e1005723.
70. Nedialkova, L.P., Denzler, R., Koeppel, M.B., Diehl, M., Ring, D., Wille, T., Gerlach, R.G., Stecher, B., Inflammation fuels colicin Ib-dependent competition of Salmonella serovar Typhimurium and E. coli in enterobacterial blooms. PLoS Pathog., 10, 2014, e1003844.
71. Nedialkova, L.P., Sidstedt, M., Koeppel, M.B., Spriewald, S., Ring, D., Gerlach, R.G., Bossi, L., Stecher, B., Temperate phages promote colicin-dependent fitness of Salmonella enterica serovar Typhimurium. Environ. Microbiol. 18 (2016), 1591–1603.
72. Ng, K.M., Ferreyra, J.A., Higginbottom, S.K., Lynch, J.B., Kashyap, P.C., Gopinath, S., Naidu, N., Choudhury, B., Weimer, B.C., Monack, D.M., Sonnenburg, J.L., Microbiota-liberated host sugars facilitate post-antibiotic expansion of enteric pathogens. Nature 502 (2013), 96–99.
73. Niess, J.H., Brand, S., Gu, X., Landsman, L., Jung, S., McCormick, B.A., Vyas, J.M., Boes, M., Ploegh, H.L., Fox, J.G., et al. CX3CR1-mediated dendritic cell access to the intestinal lumen and bacterial clearance. Science 307 (2005), 254–258.
74. Nikitas, G., Deschamps, C., Disson, O., Niault, T., Cossart, P., Lecuit, M., Transcytosis of Listeria monocytogenes across the intestinal barrier upon specific targeting of goblet cell accessible E-cadherin. J. Exp. Med. 208 (2011), 2263–2277.
75. Nordlander, S., Pott, J., Maloy, K.J., NLRC4 expression in intestinal epithelial cells mediates protection against an enteric pathogen. Mucosal Immunol. 7 (2014), 775–785.
76. Pabst, O., New concepts in the generation and functions of IgA. Nat. Rev. Immunol. 12 (2012), 821–832.
77. Pelludat, C., Mirold, S., Hardt, W.D., The SopEPhi phage integrates into the ssrA gene of Salmonella enterica serovar Typhimurium A36 and is closely related to the Fels-2 prophage. J. Bacteriol. 185 (2003), 5182–5191.
78. Petrovska, L., Mather, A.E., AbuOun, M., Branchu, P., Harris, S.R., Connor, T., Hopkins, K.L., Underwood, A., Lettini, A.A., Page, A., et al. Microevolution of monophasic Salmonella Typhimurium during epidemic, United Kingdom, 2005-2010. Emerg. Infect. Dis. 22 (2016), 617–624.
79. Pukatzki, S., Ma, A.T., Sturtevant, D., Krastins, B., Sarracino, D., Nelson, W.C., Heidelberg, J.F., Mekalanos, J.J., Identification of a conserved bacterial protein secretion system in Vibrio cholerae using the Dictyostelium host model system. Proc. Natl. Acad. Sci. USA 103 (2006), 1528–1533.
80. Qin, J., Li, R., Raes, J., Arumugam, M., Burgdorf, K.S., Manichanh, C., Nielsen, T., Pons, N., Levenez, F., Yamada, T., et al., MetaHIT Consortium. A human gut microbial gene catalogue established by metagenomic sequencing. Nature 464 (2010), 59–65.
81. Raffatellu, M., George, M.D., Akiyama, Y., Hornsby, M.J., Nuccio, S.P., Paixao, T.A., Butler, B.P., Chu, H., Santos, R.L., Berger, T., et al. Lipocalin-2 resistance confers an advantage to Salmonella enterica serotype Typhimurium for growth and survival in the inflamed intestine. Cell Host Microbe 5 (2009), 476–486.
82. Raupach, B., Peuschel, S.K., Monack, D.M., Zychlinsky, A., Caspase-1-mediated activation of interleukin-1beta (IL-1beta) and IL-18 contributes to innate immune defenses against Salmonella enterica serovar Typhimurium infection. Infect. Immun. 74 (2006), 4922–4926.
83. Rebuffat, S., Microcins in action: amazing defence strategies of Enterobacteria. Biochem. Soc. Trans. 40 (2012), 1456–1462.
84. Rhee, S.J., Walker, W.A., Cherayil, B.J., Developmentally regulated intestinal expression of IFN-gamma and its target genes and the age-specific response to enteric Salmonella infection. J. Immunol. 175 (2005), 1127–1136.
85. Rivera-Chávez, F., Bäumler, A.J., The pyromaniac inside you: Salmonella metabolism in the host gut. Annu. Rev. Microbiol. 69 (2015), 31–48.
86. Rivera-Chávez, F., Winter, S.E., Lopez, C.A., Xavier, M.N., Winter, M.G., Nuccio, S.P., Russell, J.M., Laughlin, R.C., Lawhon, S.D., Sterzenbach, T., et al. Salmonella uses energy taxis to benefit from intestinal inflammation. PLoS Pathog., 9, 2013, e1003267.
87. Rupnik, M., Wilcox, M.H., Gerding, D.N., Clostridium difficile infection: new developments in epidemiology and pathogenesis. Nat. Rev. Microbiol. 7 (2009), 526–536.
88. Salyers, A.A., Gene transfer in the mammalian intestinal tract. Curr. Opin. Biotechnol. 4 (1993), 294–298.
89. Sana, T.G., Flaugnatti, N., Lugo, K.A., Lam, L.H., Jacobson, A., Baylot, V., Durand, E., Journet, L., Cascales, E., Monack, D.M., Salmonella Typhimurium utilizes a T6SS-mediated antibacterial weapon to establish in the host gut. Proc. Natl. Acad. Sci. USA 113 (2016), E5044–E5051.
90. Sassone-Corsi, M., Chairatana, P., Zheng, T., Perez-Lopez, A., Edwards, R.A., George, M.D., Nolan, E.M., Raffatellu, M., Siderophore-based immunization strategy to inhibit growth of enteric pathogens. Proc. Natl. Acad. Sci. USA 113 (2016), 13462–13467.
91. Sassone-Corsi, M., Nuccio, S.P., Liu, H., Hernandez, D., Vu, C.T., Takahashi, A.A., Edwards, R.A., Raffatellu, M., Microcins mediate competition among Enterobacteriaceae in the inflamed gut. Nature 540 (2016), 280–283.
92. Schloissnig, S., Arumugam, M., Sunagawa, S., Mitreva, M., Tap, J., Zhu, A., Waller, A., Mende, D.R., Kultima, J.R., Martin, J., et al. Genomic variation landscape of the human gut microbiome. Nature 493 (2013), 45–50.
93. Schmitt, C.K., Ikeda, J.S., Darnell, S.C., Watson, P.R., Bispham, J., Wallis, T.S., Weinstein, D.L., Metcalf, E.S., O'Brien, A.D., Absence of all components of the flagellar export and synthesis machinery differentially alters virulence of Salmonella enterica serovar Typhimurium in models of typhoid fever, survival in macrophages, tissue culture invasiveness, and calf enterocolitis. Infect. Immun. 69 (2001), 5619–5625.
94. Scott, K.P., The role of conjugative transposons in spreading antibiotic resistance between bacteria that inhabit the gastrointestinal tract. Cell. Mol. Life Sci. 59 (2002), 2071–2082.
95. Sellin, M.E., Müller, A.A., Felmy, B., Dolowschiak, T., Diard, M., Tardivel, A., Maslowski, K.M., Hardt, W.D., Epithelium-intrinsic NAIP/NLRC4 inflammasome drives infected enterocyte expulsion to restrict Salmonella replication in the intestinal mucosa. Cell Host Microbe 16 (2014), 237–248.
96. Sellin, M.E., Maslowski, K.M., Maloy, K.J., Hardt, W.D., Inflammasomes of the intestinal epithelium. Trends Immunol. 36 (2015), 442–450.
97. Simonsen, J., Mølbak, K., Falkenhorst, G., Krogfelt, K.A., Linneberg, A., Teunis, P.F., Estimation of incidences of infectious diseases based on antibody measurements. Stat. Med. 28 (2009), 1882–1895.
98. Solaymani-Mohammadi, S., Lakhdari, O., Minev, I., Shenouda, S., Frey, B.F., Billeskov, R., Singer, S.M., Berzofsky, J.A., Eckmann, L., Kagnoff, M.F., Lack of the programmed death-1 receptor renders host susceptible to enteric microbial infection through impairing the production of the mucosal natural killer cell effector molecules. J. Leukoc. Biol. 99 (2016), 475–482.
99. Sommer, F., Bäckhed, F., The gut microbiota—masters of host development and physiology. Nat. Rev. Microbiol. 11 (2013), 227–238.
100. Songhet, P., Barthel, M., Stecher, B., Müller, A.J., Kremer, M., Hansson, G.C., Hardt, W.D., Stromal IFN-γR-signaling modulates goblet cell function during Salmonella Typhimurium infection. PLoS ONE, 6, 2011, e22459.
101. Sonnenburg, J.L., Xu, J., Leip, D.D., Chen, C.H., Westover, B.P., Weatherford, J., Buhler, J.D., Gordon, J.I., Glycan foraging in vivo by an intestine-adapted bacterial symbiont. Science 307 (2005), 1955–1959.
102. Stecher, B., The roles of inflammation, nutrient availability and the commensal microbiota in enteric pathogen infection. Microbiol. Spectr., 3, 2015, 10.1128/microbiolspec.MBP-0008-2014.
103. Stecher, B., Hardt, W.D., The role of microbiota in infectious disease. Trends Microbiol. 16 (2008), 107–114.
104. Stecher, B., Hardt, W.D., Mechanisms controlling pathogen colonization of the gut. Curr. Opin. Microbiol. 14 (2011), 82–91.
105. Stecher, B., Hapfelmeier, S., Müller, C., Kremer, M., Stallmach, T., Hardt, W.D., Flagella and chemotaxis are required for efficient induction of Salmonella enterica serovar Typhimurium colitis in streptomycin-pretreated mice. Infect. Immun. 72 (2004), 4138–4150.
106. Stecher, B., Robbiani, R., Walker, A.W., Westendorf, A.M., Barthel, M., Kremer, M., Chaffron, S., Macpherson, A.J., Buer, J., Parkhill, J., et al. Salmonella enterica serovar typhimurium exploits inflammation to compete with the intestinal microbiota. PLoS Biol. 5 (2007), 2177–2189.
107. Stecher, B., Barthel, M., Schlumberger, M.C., Haberli, L., Rabsch, W., Kremer, M., Hardt, W.D., Motility allows S. Typhimurium to benefit from the mucosal defence. Cell. Microbiol. 10 (2008), 1166–1180.
108. Stecher, B., Chaffron, S., Käppeli, R., Hapfelmeier, S., Freedrich, S., Weber, T.C., Kirundi, J., Suar, M., McCoy, K.D., von Mering, C., et al. Like will to like: abundances of closely related species can predict susceptibility to intestinal colonization by pathogenic and commensal bacteria. PLoS Pathog., 6, 2010, e1000711.
109. Stecher, B., Denzler, R., Maier, L., Bernet, F., Sanders, M.J., Pickard, D.J., Barthel, M., Westendorf, A.M., Krogfelt, K.A., Walker, A.W., et al. Gut inflammation can boost horizontal gene transfer between pathogenic and commensal Enterobacteriaceae. Proc. Natl. Acad. Sci. USA 109 (2012), 1269–1274.
110. Stecher, B., Berry, D., Loy, A., Colonization resistance and microbial ecophysiology: using gnotobiotic mouse models and single-cell technology to explore the intestinal jungle. FEMS Microbiol. Rev. 37 (2013), 793–829.
111. Stecher, B., Maier, L., Hardt, W.D., ‘Blooming’ in the gut: how dysbiosis might contribute to pathogen evolution. Nat. Rev. Microbiol. 11 (2013), 277–284.
112. Stelter, C., Käppeli, R., König, C., Krah, A., Hardt, W.D., Stecher, B., Bumann, D., Salmonella-induced mucosal lectin RegIIIβ kills competing gut microbiota. PLoS ONE, 6, 2011, e20749.
113. Studer, N., Desharnais, L., Beutler, M., Brugiroux, S., Terrazos, M.A., Menin, L., Schürch, C.M., McCoy, K.D., Kuehne, S.A., Minton, N.P., et al. Functional intestinal bile acid 7α-dehydroxylation by Clostridium scindens associated with protection from Clostridium difficile infection in a gnotobiotic mouse model. Front. Cell. Infect. Microbiol., 6, 2016, 191.
114. Tsolis, R.M., Xavier, M.N., Santos, R.L., Bäumler, A.J., How to become a top model: impact of animal experimentation on human Salmonella disease research. Infect. Immun. 79 (2011), 1806–1814.
115. Uchimura, Y., Wyss, M., Brugiroux, S., Limenitakis, J.P., Stecher, B., McCoy, K.D., Macpherson, A.J., Complete genome sequences of 12 species of stable defined moderately diverse mouse microbiota 2. Genome Announc., 4, 2016, 10.1128/genomeA.00951-16.
116. Weingarden, A.R., Chen, C., Bobr, A., Yao, D., Lu, Y., Nelson, V.M., Sadowsky, M.J., Khoruts, A., Microbiota transplantation restores normal fecal bile acid composition in recurrent Clostridium difficile infection. Am. J. Physiol. Gastrointest. Liver Physiol. 306 (2014), G310–G319.
117. Wexler, A.G., Bao, Y., Whitney, J.C., Bobay, L.M., Xavier, J.B., Schofield, W.B., Barry, N.A., Russell, A.B., Tran, B.Q., Goo, Y.A., et al. Human symbionts inject and neutralize antibacterial toxins to persist in the gut. Proc. Natl. Acad. Sci. USA 113 (2016), 3639–3644.
118. WHO and FAO. Risk Assessments for Salmonella in Eggs and Broiler Chickens: Interpretative Summary. 2002, World Health Organization.
119. Winter, S.E., Thiennimitr, P., Winter, M.G., Butler, B.P., Huseby, D.L., Crawford, R.W., Russell, J.M., Bevins, C.L., Adams, L.G., Tsolis, R.M., et al. Gut inflammation provides a respiratory electron acceptor for Salmonella. Nature 467 (2010), 426–429.
120. Yang, S.C., Lin, C.H., Sung, C.T., Fang, J.Y., Antibacterial activities of bacteriocins: application in foods and pharmaceuticals. Front. Microbiol., 5, 2014, 241.
121. Youngster, I., Russell, G.H., Pindar, C., Ziv-Baran, T., Sauk, J., Hohmann, E.L., Oral, capsulized, frozen fecal microbiota transplantation for relapsing Clostridium difficile infection. JAMA 312 (2014), 1772–1778.
122. Zhang, K., Dupont, A., Torow, N., Gohde, F., Leschner, S., Lienenklaus, S., Weiss, S., Brinkmann, M.M., Kühnel, M., Hensel, M., et al. Age-dependent enterocyte invasion and microcolony formation by Salmonella. PLoS Pathog., 10, 2014, e1004385.