1932

Abstract

Bacterial pathogens are increasingly antibiotic resistant, and development of clinically effective antibiotics is lagging. Curing infections increasingly requires antimicrobials that are broader spectrum, more toxic, and more expensive, and mortality attributable to antibiotic-resistant pathogens is rising. The commensal microbiota, comprising microbes that colonize the mammalian gastrointestinal tract, can provide high levels of resistance to infection, and the contributions of specific bacterial species to resistance are being discovered and characterized. Microbiota-mediated mechanisms of colonization resistance and pathogen clearance include bactericidal activity, nutrient depletion, immune activation, and manipulation of the gut's chemical environment. Current research is focusing on development of microbiota-based therapies to reduce intestinal colonization with antibiotic-resistant pathogens, with the goal of reducing pathogen transmission and systemic dissemination.

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2017-09-08
2024-06-22
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Literature Cited

  1. Abt MC, Buffie CG, Sušac B, Becattini S, Carter RA. 1.  et al. 2016. TLR-7 activation enhances IL-22-mediated colonization resistance against vancomycin-resistant Enterococcus. Sci. Transl. Med. 8:327327ra25 [Google Scholar]
  2. Abt MC, Mckenney PT, Pamer EG. 2.  2016. Clostridium difficile colitis: pathogenesis and host defence. Nat. Rev. Microbiol. 14:10609–20 [Google Scholar]
  3. Abujamel T, Cadnum JL, Jury LA, Sunkesula VCK, Kundrapu S. 3.  et al. 2013. Defining the vulnerable period for re-establishment of Clostridium difficile colonization after treatment of C. difficile infection with oral vancomycin or metronidazole. PLOS ONE 8:101–12 [Google Scholar]
  4. Alkhatib Z, Abts A, Mavaro A, Schmitt L, Smits SHJ. 4.  2012. Lantibiotics: How do producers become self-protected?. J. Biotechnol. 159:3145–54 [Google Scholar]
  5. Antunes LCM, McDonald JAK, Schroeter K, Carlucci C, Ferreira RBR. 5.  et al. 2014. Antivirulence activity of the human gut metabolome. mBio 5:4e01183–14 [Google Scholar]
  6. Atarashi K, Tanoue T, Ando M, Kamada N, Nagano Y. 6.  et al. 2015. Th17 cell induction by adhesion of microbes to intestinal epithelial cells. Cell 163:2367–80 [Google Scholar]
  7. Baden LR, Thiemke W, Skolnik A, Chambers R, Strymish J. 7.  et al. 2001. Prolonged colonization with vancomycin-resistant Enterococcus faecium in long-term care patients and the significance of “clearance. ”. Clin. Infect. Dis. 33:101654–60 [Google Scholar]
  8. Baker J, Brown K, Rajendiran E, Yip A, DeCoffe D. 8.  et al. 2012. Medicinal lavender modulates the enteric microbiota to protect against Citrobacter rodentium-induced colitis. Am. J. Physiol. Gastrointest. Liver Physiol. 303:7G825–36 [Google Scholar]
  9. Bartoloni A, Mantella A, Goldstein BP, Dei R, Benedetti M. 9.  et al. 2004. In-vitro activity of nisin against clinical isolates of Clostridium difficile. J. Chemother. 16:2119–21 [Google Scholar]
  10. Behnsen J, Jellbauer S, Wong CP, Edwards RA, George MD. 10.  et al. 2014. The cytokine IL-22 promotes pathogen colonization by suppressing related commensal bacteria. Immunity 40:2262–73 [Google Scholar]
  11. Bilinski J, Grzesiowski P, Muszyński J, Wróblewska M, Mądry K. 11.  et al. 2016. Fecal microbiota transplantation inhibits multidrug-resistant gut pathogens: preliminary report performed in an immunocompromised host. Arch. Immunol. Ther. Exp. 64:255–58 [Google Scholar]
  12. Bilinski J, Robak K, Peric Z, Marchel H, Karakulska-Prystupiuk E. 12.  et al. 2016. Impact of gut colonization by antibiotic-resistant bacteria on the outcomes of allogeneic hematopoietic stem cell transplantation: a retrospective, single-center study. Biol. Blood Marrow Transplant. 22:61087–93 [Google Scholar]
  13. Biswas B, Adhya S, Washart P, Paul B, Trostel AN. 13.  et al. 2002. Bacteriophage therapy rescues mice bacteremic from a clinical isolate of vancomycin-resistant Enterococcus. Infect. Immun. 70:1204–10 [Google Scholar]
  14. Bohnhoff M, Miller CP, Martin WR. 14.  1964. Resistance of the mouse's intestinal tract to experimental Salmonella infection. J. Exp. Med. 120:805–16 [Google Scholar]
  15. Borrero J, Chen Y, Dunny GM, Kaznessis YN. 15.  2014. Modified lactic acid bacteria detect and inhibit multiresistant enterococci. ACS Synth. Biol. 4:299–306 [Google Scholar]
  16. Brandl K, Plitas G, Mihu CN, Ubeda C, Jia T. 16.  et al. 2009. Vancomycin-resistant enterococci exploit antibiotic-induced innate immune deficits. Nature 455:7214804–7 [Google Scholar]
  17. Brandl K, Plitas G, Schnabl B, DeMatteo RP, Pamer EG. 17.  2007. Myd88-mediated signals induce the bactericidal lectin RegIIIγ and protect mice against intestinal Listeria monocytogenes infection. J. Exp. Med. 204:81891–1900 [Google Scholar]
  18. Bricker E, Garg R, Nelson R, Loza A, Novak T, Hansen J. 18.  2005. Antibiotic treatment for Clostridium difficile-associated diarrhea in adults. Cochrane Database Syst. Rev. 3:CD004610 [Google Scholar]
  19. Brown ED, Wright GD. 19.  2016. Antibacterial drug discovery in the resistance era. Nature 529:7586336–43 [Google Scholar]
  20. Brugiroux S, Beutler M, Pfann C, Garzetti D, Ruscheweyh H-J. 20.  et al. 2016. Genome-guided design of a defined mouse microbiota that confers colonization resistance against Salmonella enterica serovar Typhimurium. Nat. Microbiol. 2:16215 [Google Scholar]
  21. Buffie CG, Bucci V, Stein RR, Mckenney PT, Ling L. 21.  et al. 2015. Precision microbiome restoration of bile acid-mediated resistance to Clostridium difficile. Nature 517:7533205–8 [Google Scholar]
  22. Buffie CG, Jarchum I, Equinda M, Lipuma L, Gobourne A. 22.  et al. 2012. Profound alterations of intestinal microbiota following a single dose of clindamycin results in sustained susceptibility to Clostridium difficile-induced colitis. Infect. Immun. 80:162–73 [Google Scholar]
  23. Caballero S, Carter R, Ke X, Sušac B, Leiner IM. 23.  et al. 2015. Distinct but spatially overlapping intestinal niches for vancomycin-resistant Enterococcus faecium and carbapenem-resistant Klebsiella pneumoniae. PLOS Pathog. 11:91–20 [Google Scholar]
  24. Capparelli R, Nocerino N, Iannaccone M, Ercolini D, Parlato M. 24.  et al. 2010. Bacteriophage therapy of Salmonella enterica: a fresh appraisal of bacteriophage therapy. J. Infect. Dis. 201:152–61 [Google Scholar]
  25. Carlton RM. 25.  1999. Phage therapy: past history and future prospects. Arch. Immunol. Ther. Exp. 47:5267–74 [Google Scholar]
  26. Cash HL, Whitham CV, Behrendt CL, Hooper LV. 26.  2006. Symbiotic bacteria direct expression of an intestinal bactericidal lectin. Science 313:57901126–30 [Google Scholar]
  27. 27. Cent. Dis. Control Prevent. 2013. Antibiotic resistance threats in the United States, 2013 Cent. Dis. Control Prevent Atlanta: https://www.cdc.gov/drugresistance/threat-report-2013/ [Google Scholar]
  28. Chai C, Lee KS, Oh SW. 28.  2015. Synergistic inhibition of Clostridium difficile with nisin-lysozyme combination treatment. Anaerobe 34:24–26 [Google Scholar]
  29. Chang JY, Antonopoulos DA, Kalra A, Tonelli A, Khalife WT. 29.  et al. 2008. Decreased diversity of the fecal microbiome in recurrent Clostridium difficile-associated diarrhea. J. Infect. Dis. 197:3435–38 [Google Scholar]
  30. Cornely OA, Crook DW, Esposito R, Poirier A, Somero MS. 30.  et al. 2012. Fidaxomicin versus vancomycin for infection with Clostridium difficile in Europe, Canada, and the USA: a double-blind, non-inferiority, randomised controlled trial. Lancet Infect. Dis. 12:4281–89 [Google Scholar]
  31. Costello SP, Conlon MA, Vuaran MS, Roberts-Thomson IC, Andrews JM. 31.  2015. Faecal microbiota transplant for recurrent Clostridium difficile infection using long-term frozen stool is effective: clinical efficacy and bacterial viability data. Aliment. Pharmacol. Ther. 42:81011–18 [Google Scholar]
  32. Crum-Cianflone NF, Sullivan E, Ballon-Landa G. 32.  2015. Fecal microbiota transplantation and successful resolution of multidrug-resistant-organism colonization. J. Clin. Microbiol. 53:61986–89 [Google Scholar]
  33. Cullen TW, Schofield WB, Barry NA, Putnam EE, Rundell EA. 33.  et al. 2015. Antimicrobial peptide resistance mediates resilience of prominent gut commensals during inflammation. Science 347:6218170–75 [Google Scholar]
  34. Dalmasso M, Strain R, Neve H, Franz CMAP, Cousin FJ. 34.  et al. 2016. Three new Escherichia coli phages from the human gut show promising potential for phage therapy. PLOS ONE 11:6e0156773 [Google Scholar]
  35. David LA, Maurice CF, Carmody RN, Gootenberg DB, Button JE. 35.  et al. 2014. Diet rapidly and reproducibly alters the human gut microbiome. Nature 505:7484559–63 [Google Scholar]
  36. Dawson LF, Valiente E, Donahue EH, Birchenough G, Wren BW. 36.  2011. Hypervirulent Clostridium difficile PCR-ribotypes exhibit resistance to widely used disinfectants. PLOS ONE 6:10e25754 [Google Scholar]
  37. Deriu E, Liu JZ, Pezeshki M, Edwards RA, Ochoa RJ. 37.  et al. 2013. Probiotic bacteria reduce Salmonella Typhimurium intestinal colonization by competing for iron. Cell Host Microbe 14:126–37 [Google Scholar]
  38. Dethlefsen L, Huse S, Sogin ML, Relman DA. 38.  2008. Exploring microbial diversity and taxonomy using SSU rRNA hypervariable tag sequencing. PLOS Biol 6:11e1000255 [Google Scholar]
  39. Dethlefsen L, Relman DA. 39.  2011. Incomplete recovery and individualized responses of the human distal gut microbiota to repeated antibiotic perturbation. PNAS 108:Suppl. 14554–61 [Google Scholar]
  40. Diaz-Ochoa VE, Lam D, Lee CS, Klaus S, Behnsen J. 40.  et al. 2016. Salmonella mitigates oxidative stress and thrives in the inflamed gut by evading calprotectin-mediated manganese sequestration. Cell Host Microbe 19:6814–25 [Google Scholar]
  41. Dini C, Bolla PA, de Urraza PJ. 41.  2016. Treatment of in vitro enterohemorrhagic Escherichia coli infection using phage and probiotics. J. Appl. Microbiol. 121:178–88 [Google Scholar]
  42. Dischinger J, Basi Chipalu S, Bierbaum G. 42.  2014. Lantibiotics: promising candidates for future applications in health care. Int. J. Med. Microbiol 304151–62 [Google Scholar]
  43. Donskey CJ, Hanrahan JA, Hutton RA, Rice LB. 43.  2000. Effect of parenteral antibiotic administration on the establishment of colonization with vancomycin-resistant Enterococcus faecium in the mouse gastrointestinal tract. J. Infect. Dis. 181:51830–33 [Google Scholar]
  44. Donskey CJ, Hoyen CK, Das SM, Farmer S, Dery M, Bonomo RA. 44.  2001. Effect of oral Bacillus coagulans administration on the density of vancomycin-resistant enterococci in the stool of colonized mice. Lett. Appl. Microbiol. 33:184–88 [Google Scholar]
  45. Donskey CJ, Hume ME, Callaway TR, Das SM, Hoyen CK, Rice LB. 45.  2001. Inhibition of vancomycin-resistant enterococci by an in vitro continuous-flow competitive exclusion culture containing human stool flora. J. Infect. Dis. 184:1624–27 [Google Scholar]
  46. Donskey CJ, Ray AJ, Hoyen CK, Fuldauer PD, Aron DC. 46.  et al. 2003. Colonization and infection with multiple nosocomial pathogens among patients colonized with vancomycin-resistant Enterococcus. Infect. Control Hosp. Epidemiol. 24:4242–45 [Google Scholar]
  47. Doron S, Hibberd PL, Goldin B, Thorpe C, McDermott L, Snydman DR. 47.  2015. Effect of Lactobacillus rhamnosus GG administration on vancomycin-resistant Enterococcus colonization in adults with comorbidities. Antimicrob. Agents Chemother. 59:84593–99 [Google Scholar]
  48. Dubberke ER, Mullane KM, Gerding DN, Lee CH, Louie TJ. 48.  et al. 2016. Clearance of vancomycin-resistant Enterococcus concomitant with administration of a microbiota-based drug targeted at recurrent Clostridium difficile infection. Open Forum Infect. Dis. 3:31–6 [Google Scholar]
  49. Dufour N, Clermont O, La Combe B, Messika J, Dion S. 49.  et al. 2016. Bacteriophage LM33_P1, a fast-acting weapon against the pandemic ST131-O25b:H4 Escherichia coli clonal complex. J. Antimicrob. Chemother. 71:3072–80 [Google Scholar]
  50. Eiseman B, Silen W, Bascom G, Kauvar A. 50.  1958. Fecal enema as an adjunct in the treatment of pseudomembranous enterocolitis. Surgery 44:5854–59 [Google Scholar]
  51. Endt K, Stecher B, Chaffron S, Slack E, Tchitchek N. 51.  et al. 2010. The microbiota mediates pathogen clearance from the gut lumen after non-typhoidal Salmonella diarrhea. PLOS Pathog 6:9e1001097 [Google Scholar]
  52. Ferreyra JA, Wu KJ, Hryckowian AJ, Bouley DM, Weimer BC, Sonnenburg JL. 52.  2014. Gut microbiota-produced succinate promotes C.difficile infection after antibiotic treatment or motility disturbance. Cell Host Microbe 16:6770–77 [Google Scholar]
  53. Field D, Quigley L, O'Connor PM, Rea MC, Daly K. 53.  et al. 2010. Studies with bioengineered Nisin peptides highlight the broad-spectrum potency of Nisin V. Microb. Biotechnol. 3:4473–86 [Google Scholar]
  54. Fitzpatrick LR, Small JS, Greene WH, Karpa KD, Farmer S, Keller D. 54.  2012. Bacillus coagulans GBI-30, 6086 limits the recurrence of Clostridium difficile-induced colitis following vancomycin withdrawal in mice. Gut Pathog. 4:113 [Google Scholar]
  55. Fitzpatrick LR, Small JS, Greene WH, Karpa KD, Keller D. 55.  2011. Bacillus coagulans GBI-30 (BC30) improves indices of Clostridium difficile-induced colitis in mice. Gut Pathog. 3:116 [Google Scholar]
  56. Fukuda S, Toh H, Hase K, Oshima K, Nakanishi Y. 56.  et al. 2011. Bifidobacteria can protect from enteropathogenic infection through production of acetate. Nature 469:7331543–47 [Google Scholar]
  57. Ge H. 57.  2000. Zhou hou bei ji fang Tianjin Sci. Technol. Tianjin, China: [Google Scholar]
  58. Gebhart D, Lok S, Clare S, Tomas M, Stares M. 58.  et al. 2015. A modified R-type bacteriocin specifically targeting Clostridium difficile prevents colonization of mice without affecting gut microbiota diversity. mBio 6:21–13 [Google Scholar]
  59. Gebhart D, Williams SR, Bishop-Lilly KA, Govoni GR, Willner KM. 59.  et al. 2012. Novel high-molecular-weight, R-type bacteriocins of Clostridium difficile. J. Bacteriol. 194:226240–47 [Google Scholar]
  60. George RH, Symonds JM, Dimock F, Brown JD, Arabi Y. 60.  et al. 1978. Identification of Clostridium difficile as a cause of pseudomembranous colitis. BMJ 16114695 [Google Scholar]
  61. Giel JL, Sorg JA, Sonenshein AL, Zhu J. 61.  2010. Metabolism of bile salts in mice influences spore germination in Clostridium difficile. PLOS ONE 5:1e8740 [Google Scholar]
  62. Gong P, Cheng M, Li X, Jiang H, Yu C. 62.  et al. 2016. Characterization of Enterococcus faecium bacteriophage IME-EFm5 and its endolysin LysEFm5. Virology 492:11–20 [Google Scholar]
  63. Gough E, Shaikh H, Manges AR. 63.  2011. Systematic review of intestinal microbiota transplantation (fecal bacteriotherapy) for recurrent Clostridium difficile infection. Clin. Infect. Dis. 53:10994–1002 [Google Scholar]
  64. Hall AJ, Curns AT, McDonald LC, Parashar UD, Lopman BA. 64.  2012. The roles of Clostridium difficile and norovirus among gastroenteritis-associated deaths in the United States, 1999–2007. Clin. Infect. Dis. 55:2216–23 [Google Scholar]
  65. Hamilton MJ, Weingarden AR, Unno T, Khoruts A, Sadowsky MJ. 65.  2013. High-throughput DNA sequence analysis reveals stable engraftment of gut microbiota following transplantation of previously frozen fecal bacteria. Gut Microbes 4:2125–35 [Google Scholar]
  66. Hentges D, Freter R. 66.  1962. In vivo and in vitro antagonism of intestinal bacteria against Shigella flexneri: I. Correlation between various tests. J. Infect. Dis. 110:30–37 [Google Scholar]
  67. Hirsch BE, Saraiya N, Poeth K, Schwartz RM, Epstein ME, Honig G. 67.  2015. Effectiveness of fecal-derived microbiota transfer using orally administered capsules for recurrent Clostridium difficile infection. BMC Infect. Dis. 15:191 [Google Scholar]
  68. Holler E, Butzhammer P, Schmid K, Hundsrucker C, Koestler J. 68.  et al. 2014. Metagenomic analysis of the stool microbiome in patients receiving allogeneic stem cell transplantation: Loss of diversity is associated with use of systemic antibiotics and more pronounced in gastrointestinal graft-versus-host disease. Biol. Blood Marrow Transplant. 20:5640–45 [Google Scholar]
  69. Hume ME, Poole TL, Pultz NJ, Hanrahan JA, Donskey CJ. 69.  2004. Inhibition of vancomycin-resistant Enterococcus by continuous-flow cultures of human stool microflora with and without anaerobic gas supplementation. Curr. Microbiol. 48:5364–67 [Google Scholar]
  70. Iancu C, Grainger A, Field D, Cotter PD, Hill C, Ross RP. 70.  2012. Comparison of the potency of the lipid II targeting antimicrobials nisin, lacticin 3147 and vancomycin against gram-positive bacteria. Probiotics Antimicrob. Proteins 4:2108–15 [Google Scholar]
  71. Iredell J, Brown J, Tagg K. 71.  2016. Antibiotic resistance in Enterobacteriaceae: Mechanisms and clinical implications. BMJ 352:h6420 [Google Scholar]
  72. Jellbauer S, Perez Lopez A, Behnsen J, Gao N, Nguyen T. 72.  et al. 2016. Beneficial effects of sodium phenylbutyrate administration during infection with Salmonella enterica serovar Typhimurium. Infect. Immun. 84:2639–52 [Google Scholar]
  73. Johnson-Henry KC, Pinnell LJ, Waskow AM, Irrazabal T, Martin A. 73.  et al. 2014. Short-chain fructo-oligosaccharide and inulin modulate inflammatory responses and microbial communities in Caco2-bbe cells and in a mouse model of intestinal injury. J. Nutr. 144:111725–33 [Google Scholar]
  74. Jump RLP, Polinkovsky A, Hurless K, Sitzlar B, Eckart K. 74.  et al. 2014. Metabolomics analysis identifies intestinal microbiota-derived biomarkers of colonization resistance in clindamycin-treated mice. PLOS ONE 9:7e101267 [Google Scholar]
  75. Kabbani TA, Pallav K, Dowd SE, Villafuerte-Galvez J, Vanga RR. 75.  et al. 2017. Prospective randomized controlled study on the effects of Saccharomyces boulardii CNCM I-745 and amoxicillin-clavulanate or the combination on the gut microbiota of healthy volunteers. Gut Microbes 8:117–32 [Google Scholar]
  76. Khalifa L, Brosh Y, Gelman D, Coppenhagen-Glazer S, Beyth S. 76.  et al. 2015. Targeting Enterococcus faecalis biofilms with phage therapy. Appl. Environ. Microbiol. 81:82696–705 [Google Scholar]
  77. Khan MJ, Gerasimidis K, Edwards CA, Shaikh MG. 77.  2016. Role of gut microbiota in the aetiology of obesity: proposed mechanisms and review of the literature. J. Obes. 2016:1–27 [Google Scholar]
  78. Khanna S, Pardi DS, Kelly CR, Kraft CS, Dhere T. 78.  et al. 2016. A novel microbiome therapeutic increases gut microbial diversity and prevents recurrent Clostridium difficile infection. J. Infect. Dis. 214:jiv766 [Google Scholar]
  79. Kinnebrew MA, Lee YJ, Jenq RR, Lipuma L, Littmann ER. 79.  et al. 2014. Early Clostridium difficile infection during allogeneic hematopoietic stem cell transplantation. PLOS ONE 9:31–9 [Google Scholar]
  80. Kinnebrew MA, Ubeda C, Zenewicz LA, Smith N, Richard A, Pamer EG. 80.  2011. Bacterial flagellin stimulates TLR5-dependent defense against vancomycin-resistant Enterococcus infection. J. Infect. Dis. 201:4534–43 [Google Scholar]
  81. Koenigsknecht MJ, Theriot CM, Bergin IL, Schumacher CA, Schloss PD, Young VB. 81.  2015. Dynamics and establishment of Clostridium difficile infection in the murine gastrointestinal tract. Infect. Immun. 83:3934–41 [Google Scholar]
  82. Kommineni S, Bretl DJ, Lam V, Chakraborty R, Hayward M. 82.  et al. 2015. Bacteriocin production augments niche competition by enterococci in the mammalian gastrointestinal tract. Nature 526:7575719–22 [Google Scholar]
  83. Koon HW, Su B, Xu C, Mussatto CC, Tran DH-N. 83.  et al. 2016. Probiotic Saccharomyces boulardii CNCM I-745 prevents outbreak-associated Clostridium difficile-associated cecal inflammation in hamsters. Am. J. Physiol. Gastrointest. Liver Physiol. 311:G610–23 [Google Scholar]
  84. Kumar A, Henderson A, Forster GM, Goodyear AW, Weir TL. 84.  et al. 2012. Dietary rice bran promotes resistance to Salmonella enterica serovar Typhimurium colonization in mice. BMC Microbiol 12:171 [Google Scholar]
  85. Kurushima J, Ike Y, Tomita H. 85.  2016. Partial diversity generates effector immunity specificity of the Bac41-like bacteriocins of Enterococcus faecalis clinical strains. J. Bacteriol. 198:2379–90 [Google Scholar]
  86. Lawley TD, Clare S, Deakin LJ, Goulding D, Yen JL. 86.  et al. 2010. Use of purified Clostridium difficile spores to facilitate evaluation of health care disinfection regimens. Appl. Environ. Microbiol. 76:206895–900 [Google Scholar]
  87. Lawley TD, Clare S, Walker AW, Stares MD, Connor TR. 87.  et al. 2012. Targeted restoration of the intestinal microbiota with a simple, defined bacteriotherapy resolves relapsing Clostridium difficile disease in mice. PLOS Pathog 8:10e1002995 [Google Scholar]
  88. Le Lay C, Dridi L, Bergeron MG, Ouellette M, Fliss I. 88.  2016. Nisin is an effective inhibitor of Clostridium difficile vegetative cells and spore germination. J. Med. Microbiol 652169–75 [Google Scholar]
  89. Le Lay C, Fernandez B, Hammami R, Ouellette M, Fliss I. 89.  2015. On Lactococcus lactis UL719 competitivity and nisin (nisaplin®) capacity to inhibit Clostridium difficile in a model of human colon. Front. Microbiol. 6:1020 [Google Scholar]
  90. Leatham MP, Banerjee S, Autieri SM, Mercado-Lubo R, Conway T, Cohen PS. 90.  2009. Precolonized human commensal Escherichia coli strains serve as a barrier to E. coli O157:H7 growth in the streptomycin-treated mouse intestine. Infect. Immun. 77:72876–86 [Google Scholar]
  91. Leclercq R, Derlot E, Duval J, Courvalin P. 91.  1988. Plasmid-mediated resistance to vancomycin and teicoplanin in Enterococcus faecium. N. Engl. J. Med. 319:3157–61 [Google Scholar]
  92. Lederberg J, McCray A. 92.  2001. ’Ome sweet ’omics—a genealogical treasury of words. The Scientist 15:78 [Google Scholar]
  93. Lee CH, Steiner T, Petrof EO, Smieja M, Roscoe D. 93.  et al. 2016. Frozen versus fresh fecal microbiota transplantation and clinical resolution of diarrhea in patients with recurrent Clostridium difficile infection: a randomized clinical trial. JAMA 315:2142–49 [Google Scholar]
  94. Leewenhoek A. 94.  1684. An abstract of a letter from Mr. Anthony Leewenhoek at Delft, dated Sep. 17, 1683: containing some microscopical observations, about animals in the scurf of the teeth, the substance call'd worms in the nose, the cuticula consisting of scales. Philos. Trans. R. Soc. 14:568–74 https://dx.doi.org/10.1098/rstl.1684.0030 [Crossref] [Google Scholar]
  95. Lessa FC, Mu Y, Bamberg WM, Beldavs ZG, Dumyati GK. 95.  et al. 2015. Burden of Clostridium difficile infection in the United States. N. Engl. J. Med. 372:9825–34 [Google Scholar]
  96. Lewis BB, Buffie CG, Carter RA, Leiner I, Toussaint NC. 96.  et al. 2015. Loss of microbiota-mediated colonization resistance to Clostridium difficile infection with oral vancomycin compared with metronidazole. J. Infect. Dis. 212:101656–65 [Google Scholar]
  97. Liu JZ, Jellbauer S, Poe AJ, Ton V, Pesciaroli M. 97.  et al. 2012. Zinc sequestration by the neutrophil protein calprotectin enhances Salmonella growth in the inflamed gut. Cell Host Microbe 11:3227–39 [Google Scholar]
  98. Louie TJ, Cannon K, Byrne B, Emery J, Ward L. 98.  et al. 2012. Fidaxomicin preserves the intestinal microbiome during and after treatment of Clostridium difficile infection (CDI) and reduces both toxin reexpression and recurrence of CDI. Clin. Infect. Dis. 55:Suppl. 2132–42 [Google Scholar]
  99. Louie TJ, Miller MA, Mullane KMK, Weiss K, Lentnek A. 99.  et al. 2011. Fidaxomicin versus vancomycin for Clostridium difficile infection. N. Engl. J. Med. 364:5422–31 [Google Scholar]
  100. Macfarlane S, Macfarlane GT. 100.  2003. Regulation of short-chain fatty acid production. Proc. Nutr. Soc. 62:67–72 [Google Scholar]
  101. Mai V, Ukhanova M, Reinhard MK, Li M, Sulakvelidze A. 101.  2015. Bacteriophage administration significantly reduces Shigella colonization and shedding by Shigella-challenged mice without deleterious side effects and distortions in the gut microbiota. Bacteriophage 5:4e1088124 [Google Scholar]
  102. Maltby R, Leatham-Jensen MP, Gibson T, Cohen PS, Conway T. 102.  2013. Nutritional basis for colonization resistance by human commensal Escherichiacoli strains HS and Nissle 1917 against E. coli O157:H7 in the mouse intestine. PLOS ONE 8:1e53957 [Google Scholar]
  103. Manley KJ, Fraenkel MB, Mayall BC, Power DA. 103.  2007. Probiotic treatment of vancomycin-resistant enterococci: a randomised controlled trial. Med. J. Aust 1869454–57 [Google Scholar]
  104. Marin JJG, Macias RIR, Briz O, Banales JM, Monte MJ. 104.  2015. Bile acids in physiology, pathology and pharmacology. Curr. Drug Metab. 17:14–29 [Google Scholar]
  105. Maura D, Galtier M, Le Bouguénec C, Debarbieux L. 105.  2012. Virulent bacteriophages can target O104:H4 enteroaggregative Escherichia coli in the mouse intestine. Antimicrob. Agents Chemother. 56:126235–42 [Google Scholar]
  106. Millette M, Cornut G, Dupont C, Shareck F, Archambault D, Lacroix M. 106.  2008. Capacity of human nisin- and pediocin-producing lactic acid bacteria to reduce intestinal colonization by vancomycin-resistant enterococci. Appl. Environ. Microbiol. 74:71997–2003 [Google Scholar]
  107. Miyazaki S, Fujikawa T, Kobayashi I, Matsumoto T, Tateda K, Yamaguchi K. 107.  2001. Development of systemic bacteraemia after oral inoculation of vancomycin-resistant enterococci in mice. J. Med. Microbiol 508695–701 [Google Scholar]
  108. Ng KM, Ferreyra JA, Higginbottom SK, Lynch JB, Kashyap PC. 108.  et al. 2014. Microbiota-liberated host sugars facilitate post-antibiotic expansion of enteric pathogens. Nature 502:746996–99 [Google Scholar]
  109. Ongey EL, Neubauer P. 109.  2016. Lanthipeptides: chemical synthesis versus in vivo biosynthesis as tools for pharmaceutical production. Microb. Cell Factories 15:197 [Google Scholar]
  110. Orenstein R, Dubberke E, Hardi R, Ray A, Mullane K. 110.  et al. 2016. Safety and durability of RBX2660 (microbiota suspension) for recurrent Clostridium difficile infection: results of the punch CD study. Clin. Infect. Dis. 62:5596–602 [Google Scholar]
  111. Pallav K, Dowd SE, Villafuerte J, Yang X, Kabbani T. 111.  et al. 2014. Effects of polysaccharopeptide from Trametes versicolor and amoxicillin on the gut microbiome of healthy volunteers: a randomized clinical trial. Gut Microbes 5:4458–67 [Google Scholar]
  112. Pamer EG. 112.  2014. Fecal microbiota transplantation: effectiveness, complexities, and lingering concerns. Mucosal Immunol 7:2210–14 [Google Scholar]
  113. Pamer EG. 113.  2016. Resurrecting the intestinal microbiota to combat antibiotic-resistant pathogens. Science 352:6285535–38 [Google Scholar]
  114. Parasion S, Kwiatek M, Mizak L, Gryko R, Bartoszcze M, Kocik J. 114.  2012. Isolation and characterization of a novel bacteriophage φ4D lytic against Enterococcus faecalis strains. Curr. Microbiol. 65:3284–89 [Google Scholar]
  115. Pedicord VA, Lockhart AAK, Rangan KJ, Craig JW, Loschko J. 115.  et al. 2016. Exploiting a host-commensal interaction to promote intestinal barrier function and enteric pathogen tolerance. Sci. Immunol. 1:3eaai7732 [Google Scholar]
  116. Petrof EO, Gloor GB, Vanner SJ, Weese SJ, Carter D. 116.  et al. 2013. Stool substitute transplant therapy for the eradication of Clostridium difficile infection: “repoopulating” the gut. Microbiome 1:13 [Google Scholar]
  117. Pham TAN, Clare S, Goulding D, Arasteh JM, Stares MD. 117.  et al. 2014. Epithelial IL-22RA1-mediated fucosylation promotes intestinal colonization resistance to an opportunistic pathogen. Cell Host Microbe 16:4504–16 [Google Scholar]
  118. Pickard JM, Maurice CF, Kinnebrew MA, Abt MC, Schenten D. 118.  et al. 2014. Rapid fucosylation of intestinal epithelium sustains host-commensal symbiosis in sickness. Nature 514:7524638–41 [Google Scholar]
  119. Proença D, Leandro C, Garcia M, Pimentel M, São-José C. 119.  2015. EC300: A phage-based, bacteriolysin-like protein with enhanced antibacterial activity against Enterococcus faecalis. Appl. Microbiol. Biotechnol. 99:125137–49 [Google Scholar]
  120. Pultz NJ, Stiefel U, Subramanyan S, Helfand MS, Donskey CJ. 120.  2005. Mechanisms by which anaerobic microbiota inhibit the establishment in mice of intestinal colonization by vancomycin-resistant Enterococcus. J. Infect. Dis. 191:6949–56 [Google Scholar]
  121. Raibaud P, Ducluzeau R, Muller M, Sacquet E. 121.  1974. Le taurocholate de sodium, facteur de germination in vitro et in vivo. Ann. Microbiol. 125B:3381–91 [Google Scholar]
  122. Rangan KJ, Pedicord V, Lu Y, Shaham S, Mucida D, Hang HC. 122.  2016. A bacterial secreted peptidoglycan hydrolase enhances host resistance to intestinal pathogens. Science 353:63061434–37 [Google Scholar]
  123. Rea MC, Clayton E, O'Connor PM, Shanahan F, Kiely B. 123.  et al. 2007. Antimicrobial activity of lacticin 3147 against clinical Clostridium difficile strains. J. Med. Microbiol 567940–46 [Google Scholar]
  124. Rea MC, Sit CS, Clayton E, O'Connor PM, Whittal RM. 124.  et al. 2010. Thuricin CD, a posttranslationally modified bacteriocin with a narrow spectrum of activity against Clostridium difficile. PNAS 107:209352–57 [Google Scholar]
  125. Reeves AE, Koenigsknecht MJ, Bergin IL, Young VB. 125.  2012. Suppression of Clostridium difficile in the gastrointestinal tracts of germfree mice inoculated with a murine isolate from the family Lachnospiraceae. Infect. Immun. 80:113786–94 [Google Scholar]
  126. Rivera-Chavez F, Zhang LF, Faber F, Lopez CA, Byndloss MX. 126.  et al. 2016. Depletion of butyrate-producing clostridia from the gut microbiota drives an aerobic luminal expansion of Salmonella. Cell Host Microbe 19:4443–54 [Google Scholar]
  127. Rodriguez-Palacios A, LeJeune JT. 127.  2011. Moist-heat resistance, spore aging, and superdormancy in Clostridium difficile. Appl. Environ. Microbiol. 77:93085–91 [Google Scholar]
  128. Rosser EC, Mauri C. 128.  2016. A clinical update on the significance of the gut microbiota in systemic autoimmunity. J. Autoimmun. 74:85–93 [Google Scholar]
  129. Sarker SA, Brüssow H. 129.  2016. From bench to bed and back again: phage therapy of childhood Escherichia coli diarrhea. Ann. N. Y. Acad. Sci. 1372:42–52 [Google Scholar]
  130. Sarker SA, Sultana S, Reuteler G, Moine D, Descombes P. 130.  et al. 2015. Oral phage therapy of acute bacterial diarrhea with two coliphage preparations: a randomized trial in children from Bangladesh. EBioMedicine 4:124–37 [Google Scholar]
  131. Schnell N, Entian KD, Schneider U, Götz F, Zähner H. 131.  et al. 1988. Prepeptide sequence of epidermin, a ribosomally synthesized antibiotic with four sulphide-rings. Nature 333:6170276–78 [Google Scholar]
  132. Schroeder BO, Bäckhed F. 132.  2016. Signals from the gut microbiota to distant organs in physiology and disease. Nat. Med. 22:101079–89 [Google Scholar]
  133. Schubert AM, Rogers MAM, Ring C, Mogle J, Petrosino JP. 133.  et al. 2014. Microbiome data distinguish patients with Clostridium difficile infection and non-C. difficile-associated diarrhea from healthy controls. mBio 5:3e01021–14 [Google Scholar]
  134. Seekatz AM, Aas J, Gessert CE, Rubin TA, Saman DM. 134.  et al. 2014. Recovery of the gut microbiome following fecal microbiota transplantation. mBio 5:3e00893–14 [Google Scholar]
  135. Seekatz AM, Rao K, Santhosh K, Young VB. 135.  2016. Dynamics of the fecal microbiome in patients with recurrent and nonrecurrent Clostridium difficile infection. Genome Med 8:147 [Google Scholar]
  136. Seo SU, Kamada N, Munoz-Planillo R, Kim YG, Kim D. 136.  et al. 2015. Distinct commensals induce interleukin-1β via NLRP3 inflammasome in inflammatory monocytes to promote intestinal inflammation in response to injury. Immunity 42:4744–55 [Google Scholar]
  137. Shankar V, Hamilton MJ, Khoruts A, Kilburn A, Unno T. 137.  et al. 2014. Species and genus level resolution analysis of gut microbiota in Clostridium difficile patients following fecal microbiota transplantation. Microbiome 2:113 [Google Scholar]
  138. Song Y, Garg S, Girotra M, Maddox C, Von Rosenvinge EC. 138.  et al. 2013. Microbiota dynamics in patients treated with fecal microbiota transplantation for recurrent Clostridium difficile infection. PLOS ONE 8:111–11 [Google Scholar]
  139. Sonnenburg JL, Chen CTL, Gordon JI. 139.  2006. Genomic and metabolic studies of the impact of probiotics on a model gut symbiont and host. PLOS Biol 4:122213–26 [Google Scholar]
  140. Spees AM, Wangdi T, Lopez CA, Kingsbury DD, Xavier MN. 140.  et al. 2013. Streptomycin-induced inflammation enhances Escherichia coli gut colonization through nitrate respiration. mBio 4:4e00430–13 [Google Scholar]
  141. Spinler JK, Brown A, Ross CL, Boonma P, Conner ME, Savidge TC. 141.  2016. Administration of probiotic kefir to mice with Clostridium difficile infection exacerbates disease. Anaerobe 40:54–57 [Google Scholar]
  142. Stein RR, Bucci V, Toussaint NC, Buffie CG, Rätsch G. 142.  et al. 2013. Ecological modeling from time-series inference: insight into dynamics and stability of intestinal microbiota. PLOS Comput. Biol. 9:1231–36 [Google Scholar]
  143. Stiefel U, Nerandzic MM, Pultz MJ, Donskeya CJ. 143.  2014. Gastrointestinal colonization with a cephalosporinase-producing Bacteroides species preserves colonization resistance against vancomycin-resistant Enterococcus and Clostridium difficile in cephalosporin-treated mice. Antimicrob. Agents Chemother. 58:84535–42 [Google Scholar]
  144. Surawicz CM, McFarland LV, Greenberg RN, Rubin M, Fekety R. 144.  et al. 2000. The search for a better treatment for recurrent Clostridium difficile disease: use of high-dose vancomycin combined with Saccharomyces boulardii. Clin. Infect. Dis. 31:41012–17 [Google Scholar]
  145. Szachta P, Ignyś I, Cichy W. 145.  2011. An evaluation of the ability of the probiotic strain Lactobacillus rhamnosus GG to eliminate the gastrointestinal carrier state of vancomycin-resistant enterococci in colonized children. J. Clin. Gastroenterol. 45:10872–77 [Google Scholar]
  146. Taur Y, Xavier JB, Lipuma L, Ubeda C, Goldberg J. 146.  et al. 2012. Intestinal domination and the risk of bacteremia in patients undergoing allogeneic hematopoietic stem cell transplantation. Clin. Infect. Dis. 55:7905–14 [Google Scholar]
  147. Theriot CM, Bowman AA, Young VB. 147.  2015. Antibiotic-induced alterations of the gut microbiota alter secondary bile acid production and allow for Clostridium difficile spore germination and outgrowth in the large intestine. mSphere 1:1e00045–15 [Google Scholar]
  148. Theriot CM, Koenigsknecht MJ, Carlson PE Jr., Hatton GE, Nelson AM. 148.  et al. 2014. Antibiotic-induced shifts in the mouse gut microbiome and metabolome increase susceptibility to Clostridium difficile infection. Nat. Commun. 5:3114 [Google Scholar]
  149. Tian H, Ding C, Gong J, Wei Y, McFarland LV, Li N. 149.  2015. Freeze-dried, capsulized fecal microbiota transplantation for relapsing Clostridium difficile infection. J. Clin. Gastroenterol. 49:6537–38 [Google Scholar]
  150. Tvede M, Rask-Madsen J. 150.  1989. Bacteriotherapy for chronic relapsing Clostridium difficile diarrhoea in six patients. Lancet 333:86481156–60 [Google Scholar]
  151. Tvede M, Tinggaard M, Helms M. 151.  2015. Rectal bacteriotherapy for recurrent Clostridium difficile-associated diarrhoea: results from a case series of 55 patients in Denmark 2000–2012. Clin. Microbiol. Infect. 21:148–53 [Google Scholar]
  152. Ubeda C, Bucci V, Caballero S, Djukovic A, Toussaint NC. 152.  et al. 2013. Intestinal microbiota containing Barnesiella species cures vancomycin-resistant Enterococcus faecium colonization. Infect. Immun 81:3965–73 [Google Scholar]
  153. Ubeda C, Taur Y, Jenq RR, Equinda MJ, Son T. 153.  et al. 2010. Vancomycin-resistant Enterococcus domination of intestinal microbiota is enabled by antibiotic treatment and precedes bloodstream infection in humans. J. Clin. Investig. 120:124332–41 [Google Scholar]
  154. Uchiyama J, Takemura I, Satoh M, Kato S-I, Ujihara T. 154.  et al. 2011. Improved adsorption of an Enterococcus faecalis bacteriophage φEF24C with a spontaneous point mutation. PLOS ONE 6:10e26648 [Google Scholar]
  155. Uttley AH, Collins CH, Naidoo J, George RC. 155.  1988. Vancomycin-resistant enterococci. Lancet 1:8575–7657–58 [Google Scholar]
  156. van der Donk WA, Nair SK. 156.  2014. Structure and mechanism of lanthipeptide biosynthetic enzymes. Curr. Opin. Struct. Biol. 29:58–66 [Google Scholar]
  157. van der Waaij D, Berghuis JM, Lekkerkerk JE. 157.  1972. Colonization resistance of the digestive tract of mice during systemic antibiotic treatment. J. Hyg. 70:4605–10 [Google Scholar]
  158. van Nood E, Vrieze A, Nieuwdorp M, Fuentes S, Zoetendal EG. 158.  et al. 2013. Duodenal infusion of donor feces for recurrent Clostridium difficile. N. Engl. J. Med. 368:5407–15 [Google Scholar]
  159. Vong L, Pinnell LJ, Määttänen P, Yeung CW, Lurz E, Sherman PM. 159.  2015. Selective enrichment of commensal gut bacteria protects against Citrobacter rodentium-induced colitis. Am. J. Physiol. Gastrointest. Liver Physiol. 309:G181–92 [Google Scholar]
  160. Wang J, Zhang L, Teng K, Sun S, Sun Z, Zhong J. 160.  2014. Cerecidins, novel lantibiotics from Bacillus cereus with potent antimicrobial activity. Appl. Environ. Microbiol. 80:82633–43 [Google Scholar]
  161. Wang Y, Wang W, Lv Y, Zheng W, Mi Z. 161.  et al. 2014. Characterization and complete genome sequence analysis of novel bacteriophage IME-EFm1 infecting Enterococcus faecium. J. Gen. Virol. 952014:2565–75 [Google Scholar]
  162. Weingarden A, González A, Vázquez-Baeza Y, Weiss S, Humphry G. 162.  et al. 2015. Dynamic changes in short- and long-term bacterial composition following fecal microbiota transplantation for recurrent Clostridium difficile infection. Microbiome 3:10 [Google Scholar]
  163. Weingarden AR, Dosa PI, DeWinter E, Steer CJ, Shaughnessy MK. 163.  et al. 2016. Changes in colonic bile acid composition following fecal microbiota transplantation are sufficient to control Clostridium difficile germination and growth. PLOS ONE 11:11–16 [Google Scholar]
  164. Weinstock DM, Conlon M, Iovino C, Aubrey T, Gudiol C. 164.  et al. 2007. Colonization, bloodstream infection, and mortality caused by vancomycin-resistant Enterococcus early after allogeneic hematopoietic stem cell transplant. Biol. Blood Marrow Transplant. 13:5615–21 [Google Scholar]
  165. 165. White House Off. Sci. Technol. Policy. 2016. Announcing the National Microbiome Initiative Fact Sheet, White House Off. Sci. Technol. Policy Washington, DC: https://obamawhitehouse.archives.gov/the-press-office/2016/05/12/fact-sheet-announcing-national-microbiome-initiative [Google Scholar]
  166. Wiegersma N, Jansen G, van der Waaij D. 166.  1982. Effect of twelve antimicrobial drugs on the colonization resistance of the digestive tract of mice and on endogenous potentially pathogenic bacteria. J. Hyg. 88:2221–30 [Google Scholar]
  167. Wilson KH. 167.  1983. Efficiency of various bile salt preparations for stimulation of Clostridium difficile spore germination. J. Clin. Microbiol. 18:41017–19 [Google Scholar]
  168. Wilson KH, Kennedy MJ, Fekety FR. 168.  1982. Use of sodium taurocholate to enhance spore recovery on a medium selective for Clostridium difficile. J. Clin. Microbiol. 15:3443–46 [Google Scholar]
  169. Winter SE, Winter MG, Xavier MN, Thiennimitr P, Poon V. 169.  et al. 2013. Host-derived nitrate boosts growth of E. coli in the inflamed gut. Science 339:6120708–11 [Google Scholar]
  170. Wlodarska M, Willing BP, Bravo DM, Finlay BB. 170.  2015. Phytonutrient diet supplementation promotes beneficial Clostridia species and intestinal mucus secretion resulting in protection against enteric infection. Sci. Rep. 5:9253 [Google Scholar]
  171. Wlodarska M, Willing BP, Keeney KM, Menendez A, Bergstrom KS. 171.  et al. 2011. Antibiotic treatment alters the colonic mucus layer and predisposes the host to exacerbated Citrobacter rodentium-induced colitis. Infect. Immun. 79:41536–45 [Google Scholar]
  172. 172. World Health Organ. 2014. Antimicrobial Resistance: Global Report on Surveillance 2014 Geneva: WHO Press http://www.who.int/drugresistance/documents/surveillancereport/en/ [Google Scholar]
  173. 173. World Health Organ. 2016. Antimicrobial resistance Fact Sheet, World Health Organ Geneva: http://www.who.int/mediacentre/factsheets/fs194/en/ [Google Scholar]
  174. Yamamoto M, Matsumoto S. 174.  2016. Gut microbiota and colorectal cancer. Genes Environ 38:11–18 [Google Scholar]
  175. Youngster I, Russell GH, Pindar C, Ziv-Baran T, Sauk J, Hohmann EL. 175.  2014. Oral, capsulized, frozen fecal microbiota transplantation for relapsing Clostridium difficile infection. JAMA 312:171772–78 [Google Scholar]
  176. Youngster I, Sauk J, Pindar C, Wilson RG, Kaplan JL. 176.  et al. 2014. Fecal microbiota transplant for relapsing Clostridium difficile infection using a frozen inoculum from unrelated donors: a randomized, open-label, controlled pilot study. Clin. Infect. Dis. 58:111515–22 [Google Scholar]
  177. Zeng MY, Cisalpino D, Varadarajan S, Hellman J, Warren HS. 177.  et al. 2016. Gut microbiota-induced immunoglobulin G controls systemic infection by symbiotic bacteria and pathogens. Immunity 44:3647–58 [Google Scholar]
  178. Zhang W, Mi Z, Yin X, Fan H, An X. 178.  et al. 2013. Characterization of Enterococcus faecalis phage IME-EF1 and its endolysin. PLOS ONE 8:11e80435 [Google Scholar]
  179. Zirakzadeh A, Patel R. 179.  2006. Vancomycin-resistant enterococci: colonization, infection, detection, and treatment. Mayo Clin. Proc. 81:4529–36 [Google Scholar]
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