Microbial approaches for targeting antibiotic-resistant bacteria

Microbial Biotechnology

Volumn 10, Issue 5, 2017, Pages 1047-1053

  Wong, Wing Fei ^a   Santiago, Marina ^b  

^a Open Biome   (United States)

^b Finch Therapeutics Group   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIOCIN; SHORT CHAIN FATTY ACID; ANTIINFECTIVE AGENT;

ALPHAPROTEOBACTERIA; ANTIBIOTIC RESISTANCE; BACTERIAL COLONIZATION; BACTERIOPHAGE; BDELLOVIBRIO; BIOREMEDIATION; COLON CELL; COMMENSALISM; CRISPR CAS SYSTEM; DOUBLE STRANDED DNA BREAK; ENTEROBACTER CLOACAE; FECAL MICROBIOTA TRANSPLANTATION; GENETIC ENGINEERING; HORIZONTAL GENE TRANSFER; HOSPITALIZATION; HUMAN; IN VIVO STUDY; INTESTINE FLORA; KLEBSIELLA PNEUMONIAE; MICAVIBRIO; NONHUMAN; PEPTOCLOSTRIDIUM DIFFICILE; REVIEW; SPORE GERMINATION; ANIMAL; BACTERIAL INFECTION; BACTERIUM; DRUG EFFECT; GENETICS; METABOLISM; MICROBIOLOGY; MICROFLORA;

ANIMALS; ANTI-BACTERIAL AGENTS; BACTERIA; BACTERIAL INFECTIONS; DRUG RESISTANCE, BACTERIAL; HUMANS; MICROBIOTA;

EID: 85026737266     PISSN: 17517907     EISSN: 17517915     Source Type: Journal    
DOI: 10.1111/1751-7915.12783     Document Type: Review

References (82)

1. Amaral, K.F., Rogero, M.M., Fock, R.A., Borelli, P., and Gavini, G. (2007) Cytotoxicity analysis of EDTA and citric acid applied on murine resident macrophages culture. Int Endod J 40: 338–343.
2. Becattini, S., Taur, Y., and Pamer, E.G. (2016) Antibiotic-induced changes in the intestinal microbiota and disease. Trends Mol Med 22: 458–478.
3. Bilinski, J., Grzesiowski, P., Sorensen, N., Madry, K., Muszynski, J., Robak, K., et al. (2017) Fecal microbiota transplantation in patients with blood disorders inhibits gut colonization with antibiotic-resistant bacteria: results of a prospective, single-center study. Clin Infect Dis [Epub ahead of print]. doi: 10.1093/cid/cix252.
4. Biliński, J., Grzesiowski, P., Muszyński, J., Wróblewska, M., Mądry, K., Robak, K., et al. (2016) Fecal microbiota transplantation inhibits multidrug-resistant gut pathogens: preliminary report performed in an immunocompromised host. Arch Immunol Ther Exp (Warsz) 64: 255–258.
5. Boileau, M.J., Mani, R., Breshears, M.A., Gilmour, M., Taylor, J.D., and Clinkenbeard, K.D. (2016) Efficacy of Bdellovibrio bacteriovorus 109J for the treatment of dairy calves with experimentally induced infectious bovine keratoconjunctivitis. Am J Vet Res 77: 1017–1028.
6. Borysowski, J., Weber-Dabrowska, B., and Górski, A. (2006) Bacteriophage endolysins as a novel class of antibacterial agents. Exp Biol Med (Maywood) 231: 366–377.
7. Brandl, K., Plitas, G., Mihu, C., Ubeda, C., Jia, T., Fleisher, M., et al. (2008) Vancomycin-resistant enterococci exploit antibiotic-induced innate immune deficits. Nature 455: 804–807.
8. Bruttin, A., and Brüssow, H. (2005) Human volunteers receiving Escherichia coli phage T4 orally: a safety test of phage therapy. Antimicrob Agents Chemother 49: 2874–2878.
9. Caballero, S., Kim, S., Carter, R.A., Leiner, I.M., Sušac, B., Miller, L., et al. (2017) Cooperating commensals restore colonization resistance to vancomycin-resistant Enterococcus faecium. Cell Host Microbe 21: 592–602. e4.
10. Carlet, J. (2012) The gut is the epicentre of antibiotic resistance. Antimicrob Resist Infect Control 1: 39.
11. Chung, W.S.F., Walker, A.W., Louis, P., Parkhill, J., Vermeiren, J., Bosscher, D., et al. (2016) Modulation of the human gut microbiota by dietary fibres occurs at the species level. BMC Biol 14: 3.
12. Citorik, R.J., Mimee, M., and Lu, T.K. (2014) Sequence-specific antimicrobials using efficiently delivered RNA-guided nucleases. Nat Biotechnol 32: 1141–1145.
13. Crum-Cianflone, N., Sullivan, E., and Gonzalo, B.-L. (2015) Fecal microbiota transplantation and successful resolution of multidrug-resistant-organism colonization. J Clin Microbiol 53: 1986–1989.
14. Davido, B., Batista, R., Michelon, H., Lepainteur, M., Bouchand, F., Lepeule, R., et al. (2017) Is faecal microbiota transplantation an option to eradicate highly drug-resistant enteric bacteria carriage? J Hosp Infect 95: 433–437.
15. De Santis, S., Cavalcanti, E., Mastronardi, M., Jirillo, E., and Chieppa, M. (2015) Nutritional keys for intestinal barrier modulation. Front Immunol 6: 612.
16. Desai, M.S., Seekatz, A.M., Koropatkin, N.M., Kamada, N., Hickey, C.A., Wolter, M., et al. (2016) A Dietary fiber-deprived gut microbiota degrades the colonic mucus barrier and enhances pathogen susceptibility. Cell 167: 1339–1353. e21.
17. Dinan, T.G., and Cryan, J.F. (2012) Regulation of the stress response by the gut microbiota: implications for psychoneuroendocrinology. Psychoneuroendocrinology 37: 1369–1378.
18. Drekonja, D., Reich, J., Gezahegn, S., Greer, N., Shaukat, A., MacDonald, R., et al. (2015) Fecal microbiota transplantation for Clostridium difficile infection: a systematic review. Ann Intern Med 162: 630–638.
19. Dubberke, E.R., Mullane, K.M., Gerding, D.N., Lee, C.H., Louie, T.J., Guthertz, H., and Jones, C. (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: ofw133.
20. Earle, K.A., Billings, G., Sigal, M., Lichtman, J.S., Hansson, G.C., Elias, J.E., et al. (2015) Quantitative imaging of gut microbiota spatial organization. Cell Host Microbe 18: 478–488.
21. Edgar, R., Friedman, N., Molshanski-Mor, S., and Qimron, U. (2012) Reversing bacterial resistance to antibiotics by phage-mediated delivery of dominant sensitive genes. Appl Environ Microbiol 78: 744–751.
22. Eysenbach, L., Allegretti, J. R., Aroniadis, O., Brandt, L., Donovan, D., Mischer, M., et al. (2016) Clearance of vancomycin-resistant Enterococcus colonization with fecal microbiota transplantation among patients with recurrent Clostridium difficile infection. IDSA; URL https://idsa.confex.com/idsa/2016/webprogram/Paper59960.html.
23. Fenton, M., Ross, P., McAuliffe, O., O'Mahony, J., and Coffey, A. (2010) Recombinant bacteriophage lysins as antibacterials. Bioeng Bugs 1: 9–16.
24. Freedman, A. (2014) Use of stool transplant to clear fecal colonization with carbapenem-resistant enterobacteraciae (CRE): proof of concept. IDSA; URL https://idsa.confex.com/idsa/2014/webprogram/Paper47124.html.
25. Fung, T.C., Olson, C.A., and Hsiao, E.Y. (2017) Interactions between the microbiota, immune and nervous systems in health and disease. Nat Neurosci 20: 145–155.
26. Gaca, A., and Gilmore, M. (2016) Killing of VRE Enterococcus faecalis by commensal strains: evidence for evolution and accumulation of mobile elements in the absence of competition. Gut Microbes 7: 90–96.
27. Gandra, S., Barter, D.M., and Laxminarayan, R. (2014) Economic burden of antibiotic resistance: how much do we really know? Clin Microbiol Infect 20: 973–980.
28. García-Fernández, S., Morosini, M.-I., Cobo, M., Foruny, J.R., López-Sanromán, A., Cobo, J., et al. (2016) Gut eradication of VIM-1 producing ST9 Klebsiella oxytoca after fecal microbiota transplantation for diarrhea caused by a Clostridium difficile hypervirulent R027 strain. Diagn Microbiol Infect Dis 86: 470–471.
29. Gilmore, M., Rauch, M., Ramsey, M., Himes, P., Varahan, S., Manson, J., et al. (2015) Pheromone killing of multidrug-resistant Enterococcus faecalis V583 by native commensal strains. Proc Natl Acad Sci USA 112: 7273–7278.
30. Goverse, G., Molenaar, R., Macia, L., Tan, J., Erkelens, M.N., Konijn, T., et al. (2017) Diet-derived short chain fatty acids stimulate intestinal epithelial cells to induce mucosal tolerogenic dendritic cells. J Immunol 198: 2172–2181.
31. Jang, M.-O., An, J., Jung, S.-I., and Park, K.-H. (2014) Refractory Clostridium difficile infection cured with fecal microbiota transplantation in vancomycin-resistant Enterococcus colonized patient. Intest Res 13: 80–84.
32. Jones, R.M. (2016) The influence of the gut microbiota on host physiology: in pursuit of mechanisms. Yale J Biol Med 89: 285–297.
33. Jouhten, H., Mattila, E., Arkkila, P., and Satokari, R. (2016) Reduction of antibiotic resistance genes in intestinal microbiota of patients with recurrent Clostridium difficile infection after fecal microbiota transplantation. Clin Infect Dis 63: 710–711.
34. Kadouri, D.E., To, K., Shanks, R.M.Q., and Doi, Y. (2013) Predatory bacteria: a potential ally against multidrug-resistant gram-negative pathogens. PLoS ONE 8: e63397.
35. Khoruts, A., and Sadowsky, M. (2016) Understanding the mechanisms of faecal microbiota transplantation. Nat Rev Gastroenterol Hepatol 13: 508–516.
36. Kinnebrew, M., Ubeda, C., Zenewicz, L., Smith, N., Flavell, R., and Pamer, E. (2010) Bacterial flagellin stimulates Toll-like receptor 5-dependent defense against vancomycin-resistant Enterococcus infection. J Infect Dis 201: 534–543.
37. Lagier, J., Million, M., Fournier, P., Brouqui, P., and Raoult, D. (2015) Faecal microbiota transplantation for stool decolonization of OXA-48 carbapenemase-producing Klebsiella pneumoniae. J Hosp Infect 90: 173–174.
38. Loeffler, J.M., Nelson, D., and Fischetti, V.A. (2001) Rapid killing of Streptococcus pneumoniae with a bacteriophage cell wall hydrolase. Science 294: 2170–2172.
39. Lombardo, M.-J. (2015) Vancomycin-resistant enterococcal (VRE) titers diminish among patients with recurrent Clostridium difficile infection after administration of SER-109, a novel microbiome agent. IDSA; URL https://idsa.confex.com/idsa/2015/webprogram/Paper53205.html.
40. Lu, T.K., and Collins, J.J. (2007) Dispersing biofilms with engineered enzymatic bacteriophage. Proc Natl Acad Sci USA 104: 11197–11202.
41. Lu, T.K., and Collins, J.J. (2009) Engineered bacteriophage targeting gene networks as adjuvants for antibiotic therapy. Proc Natl Acad Sci USA 106: 4629–4634.
42. Lu, T.K., and Koeris, M.S. (2011) The next generation of bacteriophage therapy. Curr Opin Microbiol 14: 524–531.
43. Markelova, N.Y. (2010) Predacious bacteria, Bdellovibrio with potential for biocontrol. Int J Hyg Environ Health 213: 428–431.
44. Millan, B., Park, H., Hotte, N., Mathieu, O., Burguiere, P., Tompkins, T., et al. (2016) Fecal microbial transplants reduce antibiotic-resistant genes in patients with recurrent Clostridium difficile infection. Clin Infect Dis 62: 1479–1486.
45. Nagao-Kitamoto, H., Kitamoto, S., Kuffa, P., and Kamada, N. (2016) Pathogenic role of the gut microbiota in gastrointestinal diseases. Intest Res 14: 127–138.
46. Nudel, K., Zhao, X., Pecora, N. and Bry, L. (2017) Defined human commensal flora suppresses horizontal transfer of carbapenem resistance genes between Enterobacteriaceae in the mouse gut. ASM Microbe AAID Abstr.
47. Olsan, E.E., Byndloss, M.X., Faber, F., Rivera-Chavez, F., Tsolis, R.M., and Baumler, A.J. (2017) Colonization resistance: the deconvolution of a complex trait. J Biol Chem 292: 8577–8581.
48. Pamer, E.G. (2016) Resurrecting the intestinal microbiota to combat antibiotic-resistant pathogens. Science 352: 535–538.
49. Peterson, L.W., and Artis, D. (2014) Intestinal epithelial cells: regulators of barrier function and immune homeostasis. Nat Rev Immunol 14: 141–153.
50. Pires, D.P., Cleto, S., Sillankorva, S., Azeredo, J., and Lu, T.K. (2016) Genetically engineered phages: a review of advances over the last decade. Microbiol Mol Biol Rev 80: 523–543.
51. Ponte, A., Pinho, R., and Mota, M. (2017) Fecal microbiota transplantation: is there a role in the eradication of carbapenem-resistant Klebsiella pneumoniae intestinal carriage? Rev Esp Enferm Dig 109: 392.
52. Roberts, R.R., Hota, B., Ahmad, I., Scott, R.D., Foster, S.D., Abbasi, F., et al. (2009) Hospital and societal costs of antimicrobial-resistant infections in a Chicago teaching hospital: implications for antibiotic stewardship. Clin Infect Dis 49: 1175–1184.
53. Rowland, I., Gibson, G., Heinken, A., Scott, K., Swann, J., Thiele, I., and Tuohy, K. (2017) Gut microbiota functions: metabolism of nutrients and other food components. Eur J Nutr [Epub ahead of print]. doi: 10.1007/s00394-017-1445-8.
54. Samson, J.E., Magadán, A.H., Sabri, M., and Moineau, S. (2013) Revenge of the phages: defeating bacterial defences. Nat Rev Microbiol 11: 675–687.
55. Sassone-Corsi, M., and Raffatellu, M. (2015) No vacancy: how beneficial microbes cooperate with immunity to provide colonization resistance to pathogens. J Immunol 194: 4081–4087.
56. Sassone-Corsi, M., Nuccio, S.-P., Liu, H., Hernandez, D., Vu, C.T., Takahashi, A.A., et al. (2016) Microcins mediate competition among Enterobacteriaceae in the inflamed gut. Nature 540: 280–283.
57. Shatzkes, K., Chae, R., Tang, C., Ramirez, G.C., Mukherjee, S., Tsenova, L., et al. (2015) Examining the safety of respiratory and intravenous inoculation of Bdellovibrio bacteriovorus and Micavibrio aeruginosavorus in a mouse model. Sci Rep 5: 12899.
58. Shatzkes, K., Singleton, E., Tang, C., Zuena, M., Shukla, S., Gupta, S., et al. (2016) Predatory bacteria attenuate Klebsiella pneumoniae burden in rat lungs. mBio 7: e01847-16.
59. Singh, R., Nood, E., Nieuwdorp, M., Dam, B., Berge, I., Geerlings, S., and Bemelman, F. (2014) Donor feces infusion for eradication of extended spectrum beta-lactamase producing Escherichia coli in a patient with end stage renal disease. Clin Microbiol Infect 20: O977–O978.
60. Sohn, K.M., Cheon, S., and Kim, Y.-S. (2016) Can fecal microbiota transplantation (FMT) eradicate fecal colonization with vancomycin-resistant enterococci (VRE)? Infect Control Hosp Epidemiol 37: 1519–1521.
61. Sommer, F., and Bäckhed, F. (2013) The gut microbiota — masters of host development and physiology. Nat Rev Microbiol 11: 227–238.
62. Sommer, F., Anderson, J.M., Bharti, R., Raes, J., and Rosenstiel, P. (2017) The resilience of the intestinal microbiota influences health and disease. Nat Rev Microbiol [Epub ahead of print]. doi:10.1038/nrmicro.2017.58.
63. Sonnenburg, J.L., Chen, C.T.L., and Gordon, J.I. (2006) Genomic and metabolic studies of the impact of probiotics on a model gut symbiont and host. PLoS Biol 4: e413.
64. Stripling, J., Kumar, R., Baddley, J.W., Nellore, A., Dixon, P., Howard, D., et al. (2015) Loss of vancomycin-resistant Enterococcus fecal dominance in an organ transplant patient with Clostridium difficile colitis after fecal microbiota transplant. Open Forum Infect Dis 2: ofv078.
65. Sulakvelidze, A., Alavidze, Z., and Morris, J.G. (2001) Bacteriophage therapy. Antimicrob Agents Chemother 45: 649–659.
66. Taur, Y., Xavier, J., Lipuma, L., Ubeda, C., Goldberg, J., Gobourne, A., et al. (2012) Intestinal domination and the risk of bacteremia in patients undergoing allogeneic hematopoietic stem cell transplantation. Clin Infect Dis 55: 905–914.
67. Ubeda, C., Bucci, V., Caballero, S., Djukovic, A., Toussaint, N., Equinda, M., et al. (2013) Intestinal microbiota containing barnesiella species cures vancomycin-resistant Enterococcus faecium colonization. Infect Immun 81: 965–973.
68. US Department of Health and Human Services, Centers for Disease Control and Prevention (2013) Antibiotic resistance threats in the United States, 2013 [Internet]. URL https://www.cdc.gov/drugresistance/pdf/ar-threats-2013-508.pdf.
69. Vaishnava, S., Behrendt, C.L., Ismail, A.S., Eckmann, L., and Hooper, L.V. (2008) Paneth cells directly sense gut commensals and maintain homeostasis at the intestinal host-microbial interface. Proc Natl Acad Sci USA 105: 20858–20863.
70. Walmagh, M., Boczkowska, B., Grymonprez, B., Briers, Y., Drulis-Kawa, Z., and Lavigne, R. (2013) Characterization of five novel endolysins from Gram-negative infecting bacteriophages. Appl Microbiol Biotechnol 97: 4369–4375.
71. Wang, I.N., Smith, D.L., and Young, R. (2000) Holins: the protein clocks of bacteriophage infections. Annu Rev Microbiol 54: 799–825.
72. Weber-Dabrowska, B., Mulczyk, M., and Górski, A. (2000) Bacteriophage therapy of bacterial infections: an update of our institute's experience. Arch Immunol Ther Exp (Warsz) 48: 547–551.
73. Wei, Y., Gong, J., Zhu, W., Guo, D., Gu, L., Li, N., and Li, J. (2015) Fecal microbiota transplantation restores dysbiosis in patients with methicillin resistant Staphylococcus aureus enterocolitis. BMC Infect Dis 15: 265.
74. Wen, L., and Duffy, A. (2017) Factors influencing the gut microbiota, inflammation, and type 2 diabetes. J Nutr 147: 1468S–1475S.
75. Westergaard, J.M., and Kramer, T.T. (1977) Bdellovibrio and the intestinal flora of vertebrates. Appl Environ Microbiol 34: 506–511.
76. Westwater, C., Kasman, L.M., Schofield, D.A., Werner, P.A., Dolan, J.W., Schmidt, M.G., and Norris, J.S. (2003) Use of genetically engineered phage to deliver antimicrobial agents to bacteria: an alternative therapy for treatment of bacterial infections. Antimicrob Agents Chemother 47: 1301–1307.
77. WHO Media Cent (2014) WHO's first global report on antibiotic resistance reveals serious, worldwide threat to public health [Internet]. URL http://www.who.int/mediacentre/news/releases/2014/amr-report/en/.
78. Wu, W., Sun, M., Chen, F., Cao, A.T., Liu, H., Zhao, Y., et al. (2016) Microbiota metabolite short-chain fatty acid acetate promotes intestinal IgA response to microbiota which is mediated by GPR43. Mucosal Immunol 10: 946–956.
79. Young, R. (1992) Bacteriophage lysis: mechanism and regulation. Microbiol Rev 56: 430–481.
80. Young, R., and Bläsi, U. (1995) Holins: form and function in bacteriophage lysis. FEMS Microbiol Rev 17: 191–205.
81. Zimmerman, M.A., Singh, N., Martin, P.M., Thangaraju, M., Ganapathy, V., Waller, J.L., et al. (2012) Butyrate suppresses colonic inflammation through HDAC1-dependent Fas upregulation and Fas-mediated apoptosis of T cells. Am J Physiol Gastrointest Liver Physiol 302: G1405–G1415.
82. Zurawski, D.V., Jones, C.L., Gancz, H.Y., Honnold, C., Gupta, S., Dharani, S., et al. (2017) Predatory bacteria as an alternative therapeutic for bacterial wound infections. ASM Microbe AAID Abstr.