Inhibiting antibiotic-resistant Enterobacteriaceae by microbiota-mediated intracellular acidification

Journal of Experimental Medicine

Volumn 216, Issue 1, 2019, Pages 84-98

  Sorbara, Matthew T ^a   Dubin, Krista ^a,e   Littmann, Eric R ^a   Moody, Thomas U ^a   Fontana, Emily ^a   Seok, Ruth ^a   Leiner, Ingrid M ^a,b   Taur, Ying ^b,e   Peled, Jonathan U ^a,c,e   Van Den Brink, Marcel R M ^a,c,e   Litvak, Yael ^d   Bäumler, Andreas J ^d   Chaubard, Jean Luc ^a   Pickard, Amanda J ^a   Cross, Justin R ^a   Pamer, Eric G ^a,b,e  

^a MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^b Infectious Diseases Service   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d Davis School of Medicine ^*  (United States)

^e WEILL CORNELL MEDICAL COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMPICILLIN; ANTIBIOTIC AGENT; NITRATE; OXYGEN; SHORT CHAIN FATTY ACID; FATTY ACID;

ACIDIFICATION; ANIMAL EXPERIMENT; ANTIBACTERIAL ACTIVITY; ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIUM ISOLATE; CONTROLLED STUDY; ENTEROBACTERIACEAE; ESCHERICHIA COLI; KLEBSIELLA PNEUMONIAE; MICROFLORA; MOUSE; NONHUMAN; PH; PRIORITY JOURNAL; PROTEUS MIRABILIS; SEPSIS; ANIMAL; COLON; ENTEROBACTERIACEAE INFECTION; FEMALE; GROWTH, DEVELOPMENT AND AGING; HUMAN; INTESTINE FLORA; MALE; METABOLISM; MICROBIOLOGY; PATHOLOGY;

ANIMALS; COLON; DRUG RESISTANCE, BACTERIAL; ENTEROBACTERIACEAE; ENTEROBACTERIACEAE INFECTIONS; FATTY ACIDS; FEMALE; GASTROINTESTINAL MICROBIOME; HUMANS; HYDROGEN-ION CONCENTRATION; MALE; MICE;

EID: 85059927753     PISSN: 00221007     EISSN: 15409538     Source Type: Journal    
DOI: 10.1084/jem.20181639     Document Type: Article

References (47)

1. Becattini, S., E.R. Littmann, R.A. Carter, S.G. Kim, S.M. Morjaria, L. Ling, Y. Gyaltshen, E. Fontana, Y. Taur, I.M. Leiner, and E.G. Pamer. 2017. Com-mensal microbes provide first line defense against Listeria monocyto-genes infection. J. Exp. Med. 214:1973–1989. https://doi.org/10.1084/jem.20170495
2. Biagi, E., D. Zama, C. Nastasi, C. Consolandi, J. Fiori, S. Rampelli, S. Turroni, M. Centanni, M. Severgnini, C. Peano, et al. 2015. Gut microbiota trajectory in pediatric patients undergoing hematopoietic SCT. Bone Marrow Transplant. 50:992–998. https://doi.org/10.1038/bmt.2015.16
3. Bohnhoff, M., C.P. Miller, and W.R. Martin. 1964a. Resistance of the Mouse’s Intestinal Tract to Experimental Salmonella Infection. I. Factors Which Interfere with the Initiation of Infection by Oral Inoculation. J. Exp. Med. 120:805–816. https://doi.org/10.1084/jem.120.5.805
4. Bohnhoff, M., C.P. Miller, and W.R. Martin. 1964b. Resistance of the Mouse’s Intestinal Tract to Experimental Salmonella Infection. Ii. Factors Responsible for Its Loss Following Streptomycin Treatment. J. Exp. Med. 120:817–828. https://doi.org/10.1084/jem.120.5.817
5. Buffie, C.G., and E.G. Pamer. 2013. Microbiota-mediated colonization resistance against intestinal pathogens. Nat. Rev. Immunol. 13:790–801. https://doi.org/10.1038/nri3535
6. Byndloss, M.X., E.E. Olsan, F. Rivera-Chávez, C.R. Tiffany, S.A. Cevallos, K.L. Lokken, T.P. Torres, A.J. Byndloss, F. Faber, Y. Gao, et al. 2017. Microbiota-activated PPAR-γ signaling inhibits dysbiotic Enterobacteriaceae expansion. Science. 357:570–575. https://doi.org/10.1126/science.aam9949
7. Caporaso, J.G., C.L. Lauber, W.A. Walters, D. Berg-Lyons, J. Huntley, N. Fierer, S.M. Owens, J. Betley, L. Fraser, M. Bauer, et al. 2012. Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. ISME J. 6:1621–1624. https://doi.org/10.1038/ismej.2012.8
8. Centers for Disease Control and Prevention. 2013. Antibiotic Resistance Threats in the United States. https://www.cdc.gov/drugresistance/threat-report-2013/pdf/ar-threats-2013-508.pdf (accessed August 1, 2018)
9. DeFilipp, Z., J.U. Peled, S. Li, J. Mahabamunuge, Z. Dagher, A.E. Slingerland, C. Del Rio, B. Valles, M.E. Kempner, M. Smith, et al. 2018. Third-party fecal microbiota transplantation following allo-HCT reconstitutes microbiome diversity. Blood Adv. 2:745–753. https://doi.org/10.1182/bloodadvances.2018017731
10. den Besten, G., K. van Eunen, A.K. Groen, K. Venema, D.J. Reijngoud, and B.M. Bakker. 2013. The role of short-chain fatty acids in the interplay between diet, gut microbiota, and host energy metabolism. J. Lipid Res. 54:2325–2340. https://doi.org/10.1194/jlr.R036012
11. Duncan, S.H., P. Louis, J.M. Thomson, and H.J. Flint. 2009. The role of pH in determining the species composition of the human colonic microbiota. Environ. Microbiol. 11:2112–2122. https://doi.org/10.1111/j.1462-2920.2009.01931.x
12. Edgar, R.C. 2013. UPARSE: highly accurate OTU sequences from microbial am-plicon reads. Nat. Methods. 10:996–998. https://doi.org/10.1038/nmeth.2604
13. Edgar, R.C., and H. Flyvbjerg. 2015. Error filtering, pair assembly and error correction for next-generation sequencing reads. Bioinformatics. 31:3476–3482. https://doi.org/10.1093/bioinformatics/btv401
14. Farmer, A.D., S.D. Mohammed, G.E. Dukes, S.M. Scott, and A.R. Hobson. 2014. Caecal pH is a biomarker of excessive colonic fermentation. World J. Gastroenterol. 20:5000–5007. https://doi.org/10.3748/wjg.v20.i17.5000
15. Gantois, I., R. Ducatelle, F. Pasmans, F. Haesebrouck, I. Hautefort, A. Thompson, J.C. Hinton, and F. Van Immerseel. 2006. Butyrate specifically down-regulates salmonella pathogenicity island 1 gene expression. Appl. Environ. Microbiol. 72:946–949. https://doi.org/10.1128/AEM.72.1.946-949.2006
16. Haak, B.W., E.R. Littmann, J.L. Chaubard, A.J. Pickard, E. Fontana, F. Adhi, Y. Gyaltshen, L. Ling, S.M. Morjaria, J.U. Peled, et al. 2018. Impact of gut colonization with butyrate-producing microbiota on respiratory viral infection following allo-HCT. Blood. 131:2978–2986.
17. Hecht, A.L., B.W. Casterline, Z.M. Earley, Y.A. Goo, D.R. Goodlett, and J. Bubeck Wardenburg. 2016. Strain competition restricts colonization of an enteric pathogen and prevents colitis. EMBO Rep. 17:1281–1291. https://doi.org/10.15252/embr.201642282
18. Human Microbiome Project Consortium. 2012. Structure, function and diversity of the healthy human microbiome. Nature. 486:207–214. https://doi.org/10.1038/nature11234
19. Jacobson, A., L. Lam, M. Rajendram, F. Tamburini, J. Honeycutt, T. Pham, W. Van Treuren, K. Pruss, S.R. Stabler, K. Lugo, et al. 2018. A Gut Commen-sal-Produced Metabolite Mediates Colonization Resistance to Salmonella Infection. Cell Host Microbe. 24:296–307.e7. https://doi.org/10.1016/j.chom.2018.07.002
20. Jia, B., A.R. Raphenya, B. Alcock, N. Waglechner, P. Guo, K.K. Tsang, B.A. Lago, B.M. Dave, S. Pereira, A.N. Sharma, et al. 2017. CARD 2017: expansion and model-centric curation of the comprehensive antibiotic resistance database. Nucleic Acids Res. 45(D1):D566–D573. https://doi.org/10.1093/nar/gkw1004
21. Kamada, N., Y.G. Kim, H.P. Sham, B.A. Vallance, J.L. Puente, E.C. Martens, and G. Núñez. 2012. Regulated virulence controls the ability of a pathogen to compete with the gut microbiota. Science. 336:1325–1329. https://doi.org/10.1126/science.1222195
22. Kaminski, J., M.K. Gibson, E.A. Franzosa, N. Segata, G. Dantas, and C. Huttenhower. 2015. High-Specificity Targeted Functional Profiling in Microbial Communities with ShortBRED. PLOS Comput. Biol. 11:e1004557. https://doi.org/10.1371/journal.pcbi.1004557
23. Kelly, C.J., L.E. Glover, E.L. Campbell, D.J. Kominsky, S.F. Ehrentraut, B.E. Bowers, A.J. Bayless, B.J. Saeedi, and S.P. Colgan. 2013. Fundamental role for HIF-1α in constitutive expression of human β defensin-1. MucosalImmunol. 6:1110–1118. https://doi.org/10.1038/mi.2013.6
24. Kelly, C.J., L. Zheng, E.L. Campbell, B. Saeedi, C.C. Scholz, A.J. Bayless, K.E. Wilson, L.E. Glover, D.J. Kominsky, A. Magnuson, et al. 2015. Crosstalk between Microbiota-Derived Short-Chain Fatty Acids and Intestinal Epithelial HIF Augments Tissue Barrier Function. Cell Host Microbe. 17:662–671. https://doi.org/10.1016/j.chom.2015.03.005
25. Kim, S., A. Covington, and E.G. Pamer. 2017. The intestinal microbiota: Antibiotics, colonization resistance, and enteric pathogens. Immunol. Rev. 279:90–105. https://doi.org/10.1111/imr.12563
26. Lawhon, S.D., R. Maurer, M. Suyemoto, and C. Altier. 2002. Intestinal short-chain fatty acids alter Salmonella typhimurium invasion gene expression and virulence through BarA/SirA. Mol. Microbiol. 46:1451–1464. https://doi.org/10.1046/j.1365-2958.2002.03268.x
27. Luli, G.W., and W.R. Strohl. 1990. Comparison of growth, acetate production, and acetate inhibition of Escherichia coli strains in batch and fed-batch fermentations. Appl. Environ. Microbiol. 56:1004–1011.
28. Lupp, C., M.L. Robertson, M.E. Wickham, I. Sekirov, O.L. Champion, E.C. Gaynor, and B.B. Finlay. 2007. Host-mediated inflammation disrupts the intestinal microbiota and promotes the overgrowth of Enterobacteriaceae. Cell Host Microbe. 2:119–129. https://doi.org/10.1016/j.chom.2007.06.010
29. Martinez, K.A. II, R.D. Kitko, J.P. Mershon, H.E. Adcox, K.A. Malek, M.B. Berk-men, and J.L. Slonczewski. 2012. Cytoplasmic pH response to acid stress in individual cells of Escherichia coli and Bacillus subtilis observed by fluorescence ratio imaging microscopy. Appl. Environ. Microbiol. 78:3706–3714. https://doi.org/10.1128/AEM.00354-12
30. McMurdie, P.J., and S. Holmes. 2013. phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PLoS One. 8:e61217. https://doi.org/10.1371/journal.pone.0061217
31. Ng, K.M., J.A. Ferreyra, S.K. Higginbottom, J.B. Lynch, P.C. Kashyap, S. Go-pinath, N. Naidu, B. Choudhury, B.C. Weimer, D.M. Monack, and J.L. Sonnenburg. 2013. Microbiota-liberated host sugars facilitate post-antibiotic expansion of enteric pathogens. Nature. 502:96–99. https://doi.org/10.1038/nature12503
32. O’Loughlin, J.L., D.R. Samuelson, A.G. Braundmeier-Fleming, B.A. White, G.J. Haldorson, J.B. Stone, J.J. Lessmann, T.P. Eucker, and M.E. Konkel. 2015. The Intestinal Microbiota Influences Campylobacter jejuni Colonization and Extraintestinal Dissemination in Mice. Appl. Environ. Microbiol. 81:4642–4650. https://doi.org/10.1128/AEM.00281-15
33. Rea, M.C., C.S. Sit, E. Clayton, P.M. O’Connor, R.M. Whittal, J. Zheng, J.C. Ve-deras, R.P. Ross, and C. Hill. 2010. Thuricin CD, a posttranslationally modified bacteriocin with a narrow spectrum of activity against Clostridium difficile. Proc. Natl. Acad. Sci. USA. 107:9352–9357. https://doi.org/10.1073/pnas.0913554107
34. Rivera-Chávez, F., L.F. Zhang, F. Faber, C.A. Lopez, M.X. Byndloss, E.E. Olsan, G. Xu, E.M. Velazquez, C.B. Lebrilla, S.E. Winter, and A.J. Bäumler. 2016. Depletion of Butyrate-Producing Clostridia from the Gut Microbiota Drives an Aerobic Luminal Expansion of Salmonella. Cell Host Microbe. 19:443–454. https://doi.org/10.1016/j.chom.2016.03.004
35. Roe, A.J., D. McLaggan, I. Davidson, C. O’Byrne, and I.R. Booth. 1998. Perturbation of anion balance during inhibition of growth of Escherichia coli by weak acids. J. Bacteriol. 180:767–772.
36. Russell, A.B., S.B. Peterson, and J.D. Mougous. 2014. Type VI secretion system effectors: poisons with a purpose. Nat. Rev. Microbiol. 12:137–148. https://doi.org/10.1038/nrmicro3185
37. Salmond, C.V., R.G. Kroll, and I.R. Booth. 1984. The effect of food preservatives on pH homeostasis in Escherichia coli. J. Gen. Microbiol. 130:2845–2850.
38. Sonnenburg, E.D., and J.L. Sonnenburg. 2014. Starving our microbial self: the deleterious consequences of a diet deficient in microbiota-accessible carbohydrates. Cell Metab. 20:779–786. https://doi.org/10.1016/j.cmet.2014.07.003
39. Sorbara, M.T., and E.G. Pamer. 2018. Interbacterial mechanisms of colonization resistance and the strategies pathogens use to overcome them. Mucosal Immunol. https://doi.org/10.1038/s41385-018-0053-0
40. Taur, Y., J.B. Xavier, L. Lipuma, C. Ubeda, J. Goldberg, A. Gobourne, Y.J. Lee, K.A. Dubin, N.D. Socci, A. Viale, et al. 2012. Intestinal domination and the risk of bacteremia in patients undergoing allogeneic hematopoietic stem cell transplantation. Clin. Infect. Dis. 55:905–914. https://doi.org/10.1093/cid/cis580
41. Taur, Y., K. Coyte, J. Schluter, E. Robilotti, C. Figueroa, M. Gjonbalaj, E.R. Littmann, L. Ling, L. Miller, Y. Gyaltshen, et al. 2018. Reconstitution of the gut microbiota of antibiotic-treated patients by autologous fecal microbiota transplant. Sci. Transl. Med. 10:eaap9489. https://doi.org/10.1126/scitranslmed.aap9489
42. Topping, D.L., and P.M. Clifton. 2001. Short-chain fatty acids and human colonic function: roles of resistant starch and nonstarch polysaccharides. Physiol. Rev. 81:1031–1064. https://doi.org/10.1152/physrev.2001.81.3.1031
43. Truong, D.T., E.A. Franzosa, T.L. Tickle, M. Scholz, G. Weingart, E. Pasolli, A. Tett, C. Huttenhower, and N. Segata. 2015. MetaPhlAn2 for enhanced metagenomic taxonomic profiling. Nat. Methods. 12:902–903. https://doi.org/10.1038/nmeth.3589
44. van der Waaij, D., J.M. Berghuis-de Vries, and J.E.C. Lekkerkerk-van der Wees. 1971. Colonization resistance of the digestive tract in conventional and antibiotic-treated mice. J. Hyg. (Lond.). 69:405–411. https://doi.org/10.1017/S0022172400021653
45. Wilks, J.C., and J.L. Slonczewski. 2007. pH of the cytoplasm and periplasm of Escherichia coli: rapid measurement by green fluorescent protein fluo-rimetry. J. Bacteriol. 189:5601–5607. https://doi.org/10.1128/JB.00615-07
46. Winter, S.E., M.G. Winter, M.N. Xavier, P. Thiennimitr, V. Poon, A.M. Keestra, R.C. Laughlin, G. Gomez, J. Wu, S.D. Lawhon, et al. 2013. Host-derived nitrate boosts growth of E. coli in the inflamed gut. Science. 339:708–711. https://doi.org/10.1126/science.1232467
47. Xiong, H., R.A. Carter, I.M. Leiner, Y.W. Tang, L. Chen, B.N. Kreiswirth, and E.G. Pamer. 2015. Distinct Contributions of Neutrophils and CCR2+ Monocytes to Pulmonary Clearance of Different Klebsiella pneumoniae Strains. Infect. Immun. 83:3418–3427. https://doi.org/10.1128/IAI.00678 -15