Distinct but Spatially Overlapping Intestinal Niches for Vancomycin-Resistant Enterococcus faecium and Carbapenem-Resistant Klebsiella pneumoniae

PLoS Pathogens

Volumn 11, Issue 9, 2015, Pages 1-20

  Caballero, Silvia ^a,b   Carter, Rebecca ^a   Ke, Xu ^a   Sušac, Bože ^a   Leiner, Ingrid M ^a   Kim, Grace J ^a   Miller, Liza ^a   Ling, Lilan ^a   Manova, Katia ^a   Pamer, Eric G ^a,b  

^a MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^b Weill Cornell Graduate School of Biomedical Sciences   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMPICILLIN; ANTIINFECTIVE AGENT; CARBAPENEM DERIVATIVE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL COLONIZATION; BACTERIAL LOAD; CONFOCAL MICROSCOPY; CONTROLLED STUDY; ENTEROCOCCUS FAECIUM; FECAL MICROBIOTA TRANSPLANTATION; FECES ANALYSIS; FLUORESCENCE IN SITU HYBRIDIZATION; IMMUNOFLUORESCENCE TEST; INTESTINE FLORA; KLEBSIELLA PNEUMONIAE; MOUSE; NONHUMAN; SEQUENCE ANALYSIS; TRANSPLANTATION; VANCOMYCIN RESISTANT ENTEROCOCCUS; ANIMAL; BACTERIAL COUNT; C57BL MOUSE; COMPARATIVE STUDY; DRUG EFFECTS; ENTERITIS; FECES; FEMALE; GERMFREE ANIMAL; GRAM-POSITIVE BACTERIAL INFECTIONS; GROWTH, DEVELOPMENT AND AGING; HOST PATHOGEN INTERACTION; INTESTINE MUCOSA; ISOLATION AND PURIFICATION; KLEBSIELLA INFECTIONS; MICROBIOLOGY; ORGANISMAL INTERACTION; PATHOLOGY; PHYSIOLOGY;

AMPICILLIN; ANIMALS; ANTI-BACTERIAL AGENTS; CARBAPENEMS; COLONY COUNT, MICROBIAL; DRUG RESISTANCE, BACTERIAL; ENTERITIS; ENTEROCOCCUS FAECIUM; FECAL MICROBIOTA TRANSPLANTATION; FECES; FEMALE; GASTROINTESTINAL MICROBIOME; GRAM-POSITIVE BACTERIAL INFECTIONS; HOST-PATHOGEN INTERACTIONS; IN SITU HYBRIDIZATION, FLUORESCENCE; INTESTINAL MUCOSA; KLEBSIELLA INFECTIONS; KLEBSIELLA PNEUMONIAE; MICE, INBRED C57BL; MICROBIAL INTERACTIONS; SPECIFIC PATHOGEN-FREE ORGANISMS; VANCOMYCIN-RESISTANT ENTEROCOCCI;

EID: 84943570990     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1005132     Document Type: Article

References (51)

1. Magill SS, Edwards JR, Bamberg W, Beldavs ZG, Dumyati G, Kainer MA, et al. Multistate point-prevalence survey of health care-associated infections. N Engl J Med 2014, Mar 27;370(13):1198–208. doi: 10.1056/NEJMoa1306801 24670166
2. Arias CA, Murray BE, Emergence and management of drug-resistant enterococcal infections. Expert Rev Anti Infect Ther 2008, Oct;6(5):637–55. doi: 10.1586/14787210.6.5.637 18847403
3. Gupta N, Limbago BM, Patel JB, Kallen AJ, Carbapenem-resistant enterobacteriaceae: Epidemiology and prevention. Clin Infect Dis 2011, Jul 1;53(1):60–7. doi: 10.1093/cid/cir202 21653305
4. Safdar N, Maki DG, The commonality of risk factors for nosocomial colonization and infection with antimicrobial-resistant staphylococcus aureus, enterococcus, gram-negative bacilli, clostridium difficile, and candida. Ann Intern Med 2002, Jun 4;136(11):834–44. 12044132
5. Donskey CJ, The role of the intestinal tract as a reservoir and source for transmission of nosocomial pathogens. Clin Infect Dis 2004, Jul 15;39(2):219–26. 15307031
6. Blot S, Depuydt P, Vogelaers D, Decruyenaere J, De Waele J, Hoste E, et al. Colonization status and appropriate antibiotic therapy for nosocomial bacteremia caused by antibiotic-resistant gram-negative bacteria in an intensive care unit. Infect Control Hosp Epidemiol 2005, Jun;26(6):575–9. 16018434
7. Ubeda C, Taur Y, Jenq RR, Equinda MJ, Son T, Samstein M, et al. Vancomycin-resistant enterococcus domination of intestinal microbiota is enabled by antibiotic treatment in mice and precedes bloodstream invasion in humans. J Clin Invest 2010, Dec;120(12):4332–41. doi: 10.1172/JCI43918 21099116
8. Taur Y, Xavier JB, Lipuma L, Ubeda C, Goldberg J, Gobourne A, et al. Intestinal domination and the risk of bacteremia in patients undergoing allogeneic hematopoietic stem cell transplantation. Clin Infect Dis 2012, Oct;55(7):905–14. doi: 10.1093/cid/cis580 22718773
9. van der Waaij D, Berghuis-de Vries JM, Lekkerkerk Lekkerkerk-v. Colonization resistance of the digestive tract in conventional and antibiotic-treated mice. J Hyg (Lond) 1971, Sep;69(3):405–11.
10. Buffie CG, Pamer EG, Microbiota-mediated colonization resistance against intestinal pathogens. Nat Rev Immunol 2013, Nov;13(11):790–801. doi: 10.1038/nri3535 24096337
11. Ubeda C, Bucci V, Caballero S, Djukovic A, Toussaint NC, Equinda M, et al. Intestinal microbiota containing barnesiella species cures vancomycin-resistant enterococcus faecium colonization. Infect Immun 2013, Mar;81(3):965–73. doi: 10.1128/IAI.01197-12 23319552
12. Favre-Bonté S, Licht TR, Forestier C, Krogfelt KA, Klebsiella pneumoniae capsule expression is necessary for colonization of large intestines of streptomycin-treated mice. Infect Immun 1999, Nov;67(11):6152–6. 10531279
13. Perez F, Pultz MJ, Endimiani A, Bonomo RA, Donskey CJ, Effect of antibiotic treatment on establishment and elimination of intestinal colonization by kpc-producing klebsiella pneumoniae in mice. Antimicrob Agents Chemother 2011, Jun;55(6):2585–9. doi: 10.1128/AAC.00891-10 21422202
14. Brandl K, Plitas G, Mihu CN, Ubeda C, Jia T, Fleisher M, et al. Vancomycin-resistant enterococci exploit antibiotic-induced innate immune deficits. Nature 2008, Oct 9;455(7214):804–7. doi: 10.1038/nature07250 18724361
15. Bergstrom KS, Kissoon-Singh V, Gibson DL, Ma C, Montero M, Sham HP, et al. Muc2 protects against lethal infectious colitis by disassociating pathogenic and commensal bacteria from the colonic mucosa. PLoS Pathog 2010, May;6(5):e1000902. doi: 10.1371/journal.ppat.1000902 20485566
16. Kinnebrew MA, Ubeda C, Zenewicz LA, Smith N, Flavell RA, Pamer EG, Bacterial flagellin stimulates toll-like receptor 5-dependent defense against vancomycin-resistant enterococcus infection. J Infect Dis 2010, Feb 15;201(4):534–43. doi: 10.1086/650203 20064069
17. Vaishnava S, Yamamoto M, Severson KM, Ruhn KA, Yu X, Koren O, et al. The antibacterial lectin regiiigamma promotes the spatial segregation of microbiota and host in the intestine. Science 2011, Oct 14;334(6053):255–8. doi: 10.1126/science.1209791 21998396
18. Wlodarska M, Willing B, Keeney KM, Menendez A, Bergstrom KS, Gill N, et al. Antibiotic treatment alters the colonic mucus layer and predisposes the host to exacerbated citrobacter rodentium-induced colitis. Infect Immun 2011, Apr;79(4):1536–45. doi: 10.1128/IAI.01104-10 21321077
19. Sonnenburg JL, Chen CT, Gordon JI, Genomic and metabolic studies of the impact of probiotics on a model gut symbiont and host. PLoS Biol 2006, Nov;4(12):e413. 17132046
20. Flint HJ, Scott KP, Duncan SH, Louis P, Forano E, Microbial degradation of complex carbohydrates in the gut. Gut Microbes 2012;3(4):289–306. 22572875
21. Kamada N, Kim YG, Sham HP, Vallance BA, Puente JL, Martens EC, Núñez G, Regulated virulence controls the ability of a pathogen to compete with the gut microbiota. Science 2012, Jun 8;336(6086):1325–9. doi: 10.1126/science.1222195 22582016
22. Lee SM, Donaldson GP, Mikulski Z, Boyajian S, Ley K, Mazmanian SK, Bacterial colonization factors control specificity and stability of the gut microbiota. Nature 2013, Sep 19;501(7467):426–9. doi: 10.1038/nature12447 23955152
23. Ng KM, Ferreyra JA, Higginbottom SK, Lynch JB, Kashyap PC, Gopinath S, et al. Microbiota-liberated host sugars facilitate post-antibiotic expansion of enteric pathogens. Nature 2013, Oct 3;502(7469):96–9. doi: 10.1038/nature12503 23995682
24. van Nood E, Vrieze A, Nieuwdorp M, Fuentes S, Zoetendal EG, de Vos WM, et al. Duodenal infusion of donor feces for recurrent clostridium difficile. N Engl J Med 2013, Jan 31;368(5):407–15. doi: 10.1056/NEJMoa1205037 23323867
25. Johansson ME, Phillipson M, Petersson J, Velcich A, Holm L, Hansson GC, The inner of the two muc2 mucin-dependent mucus layers in colon is devoid of bacteria. Proc Natl Acad Sci U S A 2008, Sep 30;105(39):15064–9. doi: 10.1073/pnas.0803124105 18806221
26. Caballero S, Pamer EG, Microbiota-mediated inflammation and antimicrobial defense in the intestine. Annu Rev Immunol 2015, Mar 21;33:227–56. doi: 10.1146/annurev-immunol-032713-120238 25581310
27. McGuckin MA, Lindén SK, Sutton P, Florin TH, Mucin dynamics and enteric pathogens. Nat Rev Microbiol 2011, Apr;9(4):265–78. doi: 10.1038/nrmicro2538 21407243
28. Zarepour M, Bhullar K, Montero M, Ma C, Huang T, Velcich A, et al. The mucin muc2 limits pathogen burdens and epithelial barrier dysfunction during salmonella enterica serovar typhimurium colitis. Infect Immun 2013, Oct;81(10):3672–83. doi: 10.1128/IAI.00854-13 23876803
29. Buffie CG, Jarchum I, Equinda M, Lipuma L, Gobourne A, Viale A, et al. Profound alterations of intestinal microbiota following a single dose of clindamycin results in sustained susceptibility to clostridium difficile-induced colitis. Infect Immun 2012, Jan;80(1):62–73. doi: 10.1128/IAI.05496-11 22006564
30. Hibbing ME, Fuqua C, Parsek MR, Peterson SB, Bacterial competition: Surviving and thriving in the microbial jungle. Nat Rev Microbiol 2010, Jan;8(1):15–25. doi: 10.1038/nrmicro2259 19946288
31. Lam LH, Monack DM, Intraspecies competition for niches in the distal gut dictate transmission during persistent salmonella infection. PLoS Pathog 2014, Dec;10(12):e1004527. doi: 10.1371/journal.ppat.1004527 25474319
32. Meador JP, Caldwell ME, Cohen PS, Conway T, Escherichia coli pathotypes occupy distinct niches in the mouse intestine. Infect Immun 2014, May;82(5):1931–8. doi: 10.1128/IAI.01435-13 24566621
33. Pacheco AR, Curtis MM, Ritchie JM, Munera D, Waldor MK, Moreira CG, Sperandio V, Fucose sensing regulates bacterial intestinal colonization. Nature 2012, Dec 6;492(7427):113–7. doi: 10.1038/nature11623 23160491
34. Chang DE, Smalley DJ, Tucker DL, Leatham MP, Norris WE, Stevenson SJ, et al. Carbon nutrition of escherichia coli in the mouse intestine. Proc Natl Acad Sci U S A 2004, May 11;101(19):7427–32. 15123798
35. Pultz NJ, Hoskins LC, Donskey CJ, Vancomycin-resistant enterococci may obtain nutritional support by scavenging carbohydrate fragments generated during mucin degradation by the anaerobic microbiota of the colon. Microb Drug Resist 2006;12(1):63–7. 16584311
36. Ferreyra JA, Ng KM, Sonnenburg JL, The enteric two-step: Nutritional strategies of bacterial pathogens within the gut. Cell Microbiol 2014, Jul;16(7):993–1003. doi: 10.1111/cmi.12300 24720567
37. Liao YC, Huang TW, Chen FC, Charusanti P, Hong JS, Chang HY, et al. An experimentally validated genome-scale metabolic reconstruction of klebsiella pneumoniae MGH 78578, iyl1228. J Bacteriol 2011, Apr;193(7):1710–7. doi: 10.1128/JB.01218-10 21296962
38. Schinner SA, Mokszycki ME, Adediran J, Leatham-Jensen M, Conway T, Cohen PS, Escherichia coli EDL933 requires gluconeogenic nutrients to successfully colonize the intestines of streptomycin-treated mice precolonized with E. Coli nissle 1917. Infect Immun 2015, May;83(5):1983–91. doi: 10.1128/IAI.02943-14 25733524
39. Jakobsson HE, Rodríguez-Piñeiro AM, Schütte A, Ermund A, Boysen P, Bemark M, et al. The composition of the gut microbiota shapes the colon mucus barrier. EMBO Rep 2015, Feb;16(2):164–77. doi: 10.15252/embr.201439263 25525071
40. O'Boyle CJ, MacFie J, Mitchell CJ, Johnstone D, Sagar PM, Sedman PC, Microbiology of bacterial translocation in humans. Gut 1998, Jan;42(1):29–35. 9505882
41. Farache J, Koren I, Milo I, Gurevich I, Kim KW, Zigmond E, et al. Luminal bacteria recruit CD103+ dendritic cells into the intestinal epithelium to sample bacterial antigens for presentation. Immunity 2013, Mar 21;38(3):581–95. doi: 10.1016/j.immuni.2013.01.009 23395676
42. Diehl GE, Longman RS, Zhang JX, Breart B, Galan C, Cuesta A, et al. Microbiota restricts trafficking of bacteria to mesenteric lymph nodes by CX(3)CR1(hi) cells. Nature 2013, Feb 7;494(7435):116–20. doi: 10.1038/nature11809 23334413
43. Buffie CG, Bucci V, Stein RR, McKenney PT, Ling L, Gobourne A, et al. Precision microbiome reconstitution restores bile acid mediated resistance to clostridium difficile. Nature 2015, Jan 8;517(7533):205–8. doi: 10.1038/nature13828 25337874
44. Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, et al. Introducing mothur: Open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 2009, Dec;75(23):7537–41. doi: 10.1128/AEM.01541-09 19801464
45. DeSantis TZ, Hugenholtz P, Larsen N, Rojas M, Brodie EL, Keller K, et al. Greengenes, a chimera-checked 16S rrna gene database and workbench compatible with ARB. Appl Environ Microbiol 2006, Jul;72(7):5069–72. 16820507
46. Swidsinski A, Weber J, Loening-Baucke V, Hale LP, Lochs H, Spatial organization and composition of the mucosal flora in patients with inflammatory bowel disease. J Clin Microbiol 2005, Jul;43(7):3380–9. 16000463
47. Amann RI, Krumholz L, Stahl DA, Fluorescent-oligonucleotide probing of whole cells for determinative, phylogenetic, and environmental studies in microbiology. J Bacteriol 1990, Feb;172(2):762–70. 1688842
48. Loy A, Maixner F, Wagner M, Horn M, ProbeBase—an online resource for rrna-targeted oligonucleotide probes: New features 2007. Nucleic Acids Res 2007, Jan;35(Database issue):D800–4. 17099228
49. Waar K, Degener JE, van Luyn MJ, Harmsen HJ, Fluorescent in situ hybridization with specific DNA probes offers adequate detection of enterococcus faecalis and enterococcus faecium in clinical samples. J Med Microbiol 2005, Oct;54(Pt 10):937–44. 16157547
50. Loonen LM, Stolte EH, Jaklofsky MT, Meijerink M, Dekker J, van Baarlen P, Wells JM, REG3γ-deficient mice have altered mucus distribution and increased mucosal inflammatory responses to the microbiota and enteric pathogens in the ileum. Mucosal Immunol 2014, Jul;7(4):939–47. doi: 10.1038/mi.2013.109 24345802
51. Gouyer V, Gottrand F, Desseyn JL, The extraordinarily complex but highly structured organization of intestinal mucus-gel unveiled in multicolor images. PLoS One 2011;6(4):e18761. doi: 10.1371/journal.pone.0018761 21533274