Impact of microbial derived secondary bile acids on colonization resistance against Clostridium difficile in the gastrointestinal tract

Anaerobe

Volumn 41, Issue , 2016, Pages 44-50

  Winston, Jenessa A ^a   Theriot, Casey M ^a  

^a NORTH CAROLINA STATE UNIVERSITY   (United States)

Author keywords

Antibiotics; Clostridium difficile; Colonization resistance; Gut microbiota; Secondary bile acids

Indexed keywords

BILE ACID; CEFOPERAZONE; CHENODEOXYCHOLIC ACID; CHOLIC ACID; CLINDAMYCIN; COLISTIN; GENTAMICIN; GLYCOCHOLIC ACID; KANAMYCIN; LITHOCHOLIC ACID; METRONIDAZOLE; TAUROCHOLIC ACID; URSODEOXYCHOLIC ACID; VANCOMYCIN; ANTIINFECTIVE AGENT;

ARTICLE; BACTERIAL COLONIZATION; BACTERIAL GROWTH; BILE ACID SYNTHESIS; CLOSTRIDIUM; CLOSTRIDIUM DIFFICILE INFECTION; CLOSTRIDIUM SCINDENS; FECAL MICROBIOTA TRANSPLANTATION; GASTROINTESTINAL TRACT; HUMAN; ILEITIS; INTESTINE FLORA; METABOLOMICS; NONHUMAN; PEPTOCLOSTRIDIUM DIFFICILE; PRIORITY JOURNAL; RECURRENT INFECTION; SINGLE DRUG DOSE; SPORE GERMINATION; ANIMAL; DISEASE PREDISPOSITION; DRUG EFFECTS; DRUG RESISTANCE; ENTEROCOLITIS, PSEUDOMEMBRANOUS; MICROBIOLOGY; PHYSIOLOGY;

ANIMALS; ANTI-BACTERIAL AGENTS; BILE ACIDS AND SALTS; CLOSTRIDIUM DIFFICILE; DISEASE SUSCEPTIBILITY; DRUG RESISTANCE, NEOPLASM; ENTEROCOLITIS, PSEUDOMEMBRANOUS; GASTROINTESTINAL MICROBIOME; GASTROINTESTINAL TRACT; HUMANS;

EID: 84975497516     PISSN: 10759964     EISSN: 10958274     Source Type: Journal    
DOI: 10.1016/j.anaerobe.2016.05.003     Document Type: Article

References (77)

1. [1] Hall, I.C., O'Toole, E., Intestinal flora in new-born infants: with a description of a new pathogenic anaerobe, Bacillus difficilis. Am. J. Dis. Child. 49 (1935), 390–402.
2. [2] Lessa, F.C., Mu, Y., Bamberg, W.M., Beldavs, Z.G., Dumyati, G.K., Dunn, J.R., et al. Burden of Clostridium difficile infection in the United States. N. Engl. J. Med. 372 (2015), 825–834.
3. [3] Gerding, D.N., Lessa, F.C., The epidemiology of Clostridium difficile infection inside and outside health care institutions. Infect. Dis. Clin. North Am. 29 (2015), 37–50.
4. [4] Dubberke, E.R., Olsen, M.A., Burden of Clostridium difficile on the healthcare system. Clin. Infect. Dis. 55:Suppl. 2 (2012), S88–S92.
5. [5] U.S.D.o.H.a.H. Services, Antibiotic Resistance Threats in the United States. 2013, Centers for Disease Control and Prevention [online].
6. [6] Tartof, S.Y., Rieg, G.K., Wei, R., Tseng, H.F., Jacobsen, S.J., Yu, K.C., A comprehensive assessment across the healthcare continuum: risk of hospital-associated Clostridium difficile infection due to outpatient and inpatient antibiotic exposure. Infect. Control Hosp. Epidemiol. 36 (2015), 1409–1416.
7. [7] Abou Chakra, C.N., Pepin, J., Sirard, S., Valiquette, L., Risk factors for recurrence, complications and mortality in Clostridium difficile infection: a systematic review. PLoS One, 9, 2014, e98400.
8. [8] Antonopoulos, D.A., Huse, S.M., Morrison, H.G., Schmidt, T.M., Sogin, M.L., Young, V.B., Reproducible community dynamics of the gastrointestinal microbiota following antibiotic perturbation. Infect. Immun. 77 (2009), 2367–2375.
9. [9] Dethlefsen, L., Huse, S., Sogin, M.L., Relman, D.A., The pervasive effects of an antibiotic on the human gut microbiota, as revealed by deep 16S rRNA sequencing. PLoS Biol., 6, 2008, e280.
10. [10] Antunes, L.C., Han, J., Ferreira, R.B., Lolic, P., Borchers, C.H., Finlay, B.B., Effect of antibiotic treatment on the intestinal metabolome. Antimicrob. Agents Chemother. 55 (2011), 1494–1503.
11. [11] Theriot, C.M., Koenigsknecht, M.J., Carlson, P.E. Jr., Hatton, G.E., Nelson, A.M., Li, B., et al. Antibiotic-induced shifts in the mouse gut microbiome and metabolome increase susceptibility to Clostridium difficile infection. Nat. Commun., 5, 2014, 3114.
12. [12] Buffie, C.G., Bucci, V., Stein, R.R., McKenney, P.T., Ling, L., Gobourne, A., et al. Precision microbiome reconstitution restores bile acid mediated resistance to Clostridium difficile. Nature 517 (2015), 205–208.
13. [13] Buffie, C.G., 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. 80 (2012), 62–73.
14. [14] Reeves, A.E., Theriot, C.M., Bergin, I.L., Huffnagle, G.B., Schloss, P.D., Young, V.B., The interplay between microbiome dynamics and pathogen dynamics in a murine model of Clostridium difficile Infection. Gut Microbes 2 (2014), 145–158.
15. [15] Vollaard, E.J., Clasener, H.A., Colonization resistance. Antimicrob. Agents Chemother. 38 (1994), 409–414.
16. [16] Sorg, J.A., Microbial bile acid metabolic clusters: the bouncers at the bar. Cell Host Microbe 16 (2014), 551–552.
17. [17] Weingarden, A.R., Chen, C., Bobr, A., Yao, D., Lu, Y., Nelson, V.M., et al. Microbiota transplantation restores normal fecal bile acid composition in recurrent Clostridium difficile infection. Am. J. Physiol. Gastrointest. Liver Physiol. 306 (2014), G310–G319.
18. [18] Kociolek, Larry, K., Dale, N., Gerding. Breakthroughs in the treatment and prevention of Clostridium difficile infection. Nat. Rev. Gastroenterol. Hepatol. 13:3 (2016), 150–160.
19. [19] Kelly, C.P., LaMont, J.T., Clostridium difficile–more difficult than ever. N. Engl. J. Med. 359 (2008), 1932–1940.
20. [20] Louie, T.J., Miller, M.A., Mullane, K.M., Weiss, K., Lentnek, A., Golan, Y., et al. Fidaxomicin versus vancomycin for Clostridium difficile infection. N. Engl. J. Med. 364 (2011), 422–431.
21. [21] Theriot, C.M., Schumacher, C.A., Bassis, C.M., Seekatz, A.M., Young, V.B., Effects of tigecycline and vancomycin administration on established Clostridium difficile infection. Antimicrob. Agents Chemother. 59 (2015), 1596–1604.
22. [22] Weingarden, A.R., Chen, C., Zhang, N., Graiziger, C.T., Dosa, P.I., Steer, C.J., et al. Ursodeoxycholic acid inhibits Clostridium difficile spore germination and vegetative growth, and prevents the recurrence of ileal pouchitis associated with the infection. J. Clin. Gastroenterol., October 17, 2015, 10.1097/MCG.0000000000000427.
23. [23] Ridlon, J.M., Kang, D.J., Hylemon, P.B., Bile salt biotransformations by human intestinal bacteria. J. Lipid Res. 47 (2006), 241–259.
24. [24] Hofmann, A.F., Hagey, L.R., Krasowski, M.D., Bile salts of vertebrates: structural variation and possible evolutionary significance. J. Lipid Res. 51 (2010), 226–246.
25. [25] Russell, D.W., The enzymes, regulation, and genetics of bile acid synthesis. Annu. Rev. Biochem. 72 (2003), 137–174.
26. [26] Alnouti, Y., Csanaky, I.L., Klaassen, C.D., Quantitative-profiling of bile acids and their conjugates in mouse liver, bile, plasma, and urine using LC-MS/MS. Journal of chromatography B. Anal. Technol. Biomed. Life Sci. 873 (2008), 209–217.
27. [27] Hofmann, A.F., The enterohepatic circulation of bile acids in mammals: form and functions. Front. Biosci. (Landmark Ed) 14 (2009), 2584–2598.
28. [28] Begley, M., Gahan, C.G., Hill, C., The interaction between bacteria and bile. FEMS Microbiol. Rev. 29 (2005), 625–651.
29. [29] Inagaki, T., Moschetta, A., Lee, Y.K., Peng, L., Zhao, G., Downes, M., et al. Regulation of antibacterial defense in the small intestine by the nuclear bile acid receptor. Proc. Natl. Acad. Sci. U. S. A. 103 (2006), 3920–3925.
30. [30] Setchell, K.D., Lawson, A.M., Tanida, N., Sjovall, J., General methods for the analysis of metabolic profiles of bile acids and related compounds in feces. J. Lipid Res. 24 (1983), 1085–1100.
31. [31] Jones, B.V., Begley, M., Hill, C., Gahan, C.G., Marchesi, J.R., Functional and comparative metagenomic analysis of bile salt hydrolase activity in the human gut microbiome. Proc. Natl. Acad. Sci. U. S. A. 105 (2008), 13580–13585.
32. [32] Begley, M., Hill, C., Gahan, C.G., Bile salt hydrolase activity in probiotics. Appl. Environ. Microbiol. 72 (2006), 1729–1738.
33. [33] Ridlon, J.M., Alves, J.M., Hylemon, P.B., Bajaj, J.S., Cirrhosis, bile acids and gut microbiota: unraveling a complex relationship. Gut Microbes 4 (2013), 382–387.
34. [34] Devlin, A.S., Fischbach, M.A., A biosynthetic pathway for a prominent class of microbiota-derived bile acids. Nat. Chem. Biol. 11 (2015), 685–690.
35. [35] Ridlon, J.M., Bajaj, J.S., The human gut sterolbiome: bile acid-microbiome endocrine aspects and therapeutics. Acta Pharm. Sin. B 5 (2015), 99–105.
36. [36] Ridlon, J.M., Kang, D.J., Hylemon, P.B., Bajaj, J.S., Gut microbiota, cirrhosis, and alcohol regulate bile acid metabolism in the gut. Dig. Dis. 33 (2015), 338–345.
37. [37] Wells, J.E., Williams, K.B., Whitehead, T.R., Heuman, D.M., Hylemon, P.B., Development and application of a polymerase chain reaction assay for the detection and enumeration of bile acid 7alpha-dehydroxylating bacteria in human feces. Clin. Chim. Acta Int. J. Clin. Chem. 331 (2003), 127–134.
38. [38] Kitahara, M., Takamine, F., Imamura, T., Benno, Y., Clostridium hiranonis sp. nov., a human intestinal bacterium with bile acid 7alpha-dehydroxylating activity. Int. J. Syst. Evol. Microbiol. 51 (2001), 39–44.
39. [39] Kitahara, M., Takamine, F., Imamura, T., Benno, Y., Assignment of Eubacterium sp. VPI 12708 and related strains with high bile acid 7alpha-dehydroxylating activity to Clostridium scindens and proposal of Clostridium hylemonae sp. nov., isolated from human faeces. Int. J. Syst. Evol. Microbiol. 50:Pt 3 (2000), 971–978.
40. [40] Ridlon, J.M., Kang, D.J., Hylemon, P.B., Isolation and characterization of a bile acid inducible 7alpha-dehydroxylating operon in Clostridium hylemonae TN271. Anaerobe 16 (2010), 137–146.
41. [41] Macdonald, I.A., White, B.A., Hylemon, P.B., Separation of 7 alpha- and 7 beta-hydroxysteroid dehydrogenase activities from Clostridium absonum ATCC# 27555 and cellular response of this organism to bile acid inducers. J. Lipid Res. 24 (1983), 1119–1126.
42. [42] Dawson, J.A., Mallonee, D.H., Bjorkhem, I., Hylemon, P.B., Expression and characterization of a C24 bile acid 7 alpha-dehydratase from Eubacterium sp. strain VPI 12708 in Escherichia coli. J. Lipid Res. 37 (1996), 1258–1267.
43. [43] Mallonee, D.H., Hylemon, P.B., Sequencing and expression of a gene encoding a bile acid transporter from Eubacterium sp. strain VPI 12708. J. Bacteriol. 178 (1996), 7053–7058.
44. [44] Fiorucci, Stefano, Distrutti, Eleonora, Bile acid-activated receptors, intestinal microbiota, and the treatment of metabolic disorders. Trends Mol. Med. 21:11 (2015), 702–714.
45. [45] Ridlon, J.M., Kang, D.J., Hylemon, P.B., Bajaj, J.S., Bile acids and the gut microbiome. Curr. Opin. Gastroenterol. 30 (2014), 332–338.
46. [46] Doerner, K.C., Takamine, F., LaVoie, C.P., Mallonee, D.H., Hylemon, P.B., Assessment of fecal bacteria with bile acid 7 alpha-dehydroxylating activity for the presence of bai-like genes. Appl. Environ. Microbiol. 63 (1997), 1185–1188.
47. [47] Kuipers, F., Bloks, V.W., Groen, A.K., Beyond intestinal soap–bile acids in metabolic control. Nat. Rev. Endocrinol. 10 (2014), 488–498.
48. [48] Sayin, S.I., Wahlstrom, A., Felin, J., Jantti, S., Marschall, H.U., Bamberg, K., et al. Gut microbiota regulates bile acid metabolism by reducing the levels of tauro-beta-muricholic acid, a naturally occurring FXR antagonist. Cell Metab. 17 (2013), 225–235.
49. [49] Zhang, Y., Limaye, P.B., Renaud, H.J., Klaassen, C.D., Effect of various antibiotics on modulation of intestinal microbiota and bile acid profile in mice. Toxicol. Appl. Pharmacol. 277 (2014), 138–145.
50. [50] Theriot, C., Bowman, A., Young, V., 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, 2016 00045–15.
51. [51] Barrasa, J.I., Olmo, N., Lizarbe, M.A., Turnay, J., Bile acids in the colon, from healthy to cytotoxic molecules. Toxicol. In Vitro 27 (2013), 964–977.
52. [52] Shen, A., A gut odyssey: the impact of the microbiota on Clostridium difficile spore formation and germination. PLoS Pathog., 11, 2015, e1005157.
53. [53] Sorg, J.A., Sonenshein, A.L., Bile salts and glycine as cogerminants for Clostridium difficile spores. J. Bacteriol. 190 (2008), 2505–2512.
54. [54] Francis, M.B., Allen, C.A., Sorg, J.A., Muricholic acids inhibit Clostridium difficile spore germination and growth. PLoS One, 8, 2013, e73653.
55. [55] Sorg, J.A., Sonenshein, A.L., Inhibiting the initiation of Clostridium difficile spore germination using analogs of chenodeoxycholic acid, a bile acid. J. Bacteriol. 192 (2010), 4983–4990.
56. [56] Wilson, K.H., Kennedy, M.J., Fekety, F.R., Use of sodium taurocholate to enhance spore recovery on on a medium selective for Clostridium difficile. J. Clin. Microbiol. 15 (1982), 443–446.
57. [57] Carlson, P.E. Jr., Kaiser, A.M., McColm, S.A., Bauer, J.M., Young, V.B., Aronoff, D.M., et al. Variation in germination of Clostridium difficile clinical isolates correlates to disease severity. Anaerobe 33 (2015), 64–70.
58. [58] Heeg, D., Burns, D.A., Cartman, S.T., Minton, N.P., Spores of Clostridium difficile clinical isolates display a diverse germination response to bile salts. PLoS One, 7, 2012, e32381.
59. [59] Bhattacharjee, D., Francis, M.B., Ding, X., McAllister, K.N., Shrestha, R., Sorg, J.A., Reexamining the germination phenotypes of several Clostridium difficile strains suggests another role for the CspC germinant receptor. J. Bacteriol. 198 (2015), 777–786.
60. [60] Sorg, J.A., Sonenshein, A.L., Chenodeoxycholate is an inhibitor of Clostridium difficile spore germination. J. Bacteriol. 191 (2009), 1115–1117.
61. [61] Howerton, A., Ramirez, N., Abel-Santos, E., Mapping interactions between germinants and Clostridium difficile spores. J. Bacteriol. 193 (2011), 274–282.
62. [62] Ramirez, N., Liggins, M., Abel-Santos, E., Kinetic evidence for the presence of putative germination receptors in Clostridium difficile spores. J. Bacteriol. 192 (2010), 4215–4222.
63. [63] Weingarden, A.R., Dosa, P.I., DeWinter, E., Steer, C.J., Shaughnessy, M.K., Johnson, J.R., et al. Changes in colonic bile acid composition following fecal microbiota transplantation are sufficient to control Clostridium difficile germination and growth. PLoS One, 11, 2016, e0147210.
64. [64] Giel, J.L., Sorg, J.A., Sonenshein, A.L., Zhu, J., Metabolism of bile salts in mice influences spore germination in Clostridium difficile. PLoS One, 5, 2010.
65. [65] Koenigsknecht, M.J., Theriot, C.M., Bergin, I.L., Schumacher, C.A., Schloss, P.D., Young, V.B., Dynamics and establishment of Clostridium difficile infection in the murine gastrointestinal tract. Infect. Immun. 83 (2015), 934–941.
66. [66] Allegretti, J.R., et al. Recurrent Clostridium difficile infection associates with distinct bile acid and microbiome profiles. Aliment. Pharmacol. Ther. 43:11 (2016), 1142–1153.
67. [67] Theriot, C.M., Young, V.B., Interactions between the gastrointestinal microbiome and Clostridium difficile. Annu. Rev. Microbiol. 69 (2015), 445–461.
68. [68] Bassis, C.M., Theriot, C.M., Young, V.B., Alteration of the murine gastrointestinal microbiota by tigecycline leads to increased susceptibility to Clostridium difficile infection. Antimicrob. Agents Chemother. 58 (2014), 2767–2774.
69. [69] Kang, D.J., Ridlon, J.M., Moore, D.R. 2nd, Barnes, S., Hylemon, P.B., Clostridium scindens baiCD and baiH genes encode stereo-specific 7alpha/7beta-hydroxy-3-oxo-delta4-cholenoic acid oxidoreductases. Biochim. Biophys. Acta 1781 (2008), 16–25.
70. [70] Howerton, A., Patra, M., Abel-Santos, E., A new strategy for the prevention of Clostridium difficile infection. J. Infect. Dis. 207 (2013), 1498–1504.
71. [71] Nagaro, K.J., Phillips, S.T., Cheknis, A.K., Sambol, S.P., Zukowski, W.E., Johnson, S., et al. Nontoxigenic Clostridium difficile protects hamsters against challenge with historic and epidemic strains of toxigenic BI/NAP1/027 C. difficile. Antimicrob. Agents Chemother. 57 (2013), 5266–5270.
72. [72] Corthier, G., Dubos, F., Raibaud, P., Modulation of cytotoxin production by Clostridium difficile in the intestinal tracts of gnotobiotic mice inoculated with various human intestinal bacteria. Appl. Environ. Microbiol. 49 (1985), 250–252.
73. [73] Reeves, A.E., Koenigsknecht, M.J., Bergin, I.L., Young, V.B., Suppression of Clostridium difficile in the gastrointestinal tracts of germfree mice inoculated with a murine isolate from the family Lachnospiraceae. Infect. Immun. 80 (2012), 3786–3794.
74. [74] Lawley, T.D., Clare, S., Walker, A.W., Stares, M.D., Connor, T.R., Raisen, C., et al. Targeted restoration of the intestinal microbiota with a simple, defined bacteriotherapy resolves relapsing Clostridium difficile disease in mice. PLoS Pathog., 8, 2012, e1002995.
75. [75] Petrof, E.O., Gloor, G.B., Vanner, S.J., Weese, S.J., Carter, D., Daigneault, M.C., et al. Stool substitute transplant therapy for the eradication of Clostridium difficile infection: ‘RePOOPulating’ the gut. Microbiome, 1, 2013, 3.
76. [76] Tvede, M., Rask-Madsen, J., Bacteriotherapy for chronic relapsing Clostridium difficile diarrhoea in six patients. Lancet (London, England) 1 (1989), 1156–1160.
77. [77] Joyce, Susan, A., Gahan, Cormac GM, Bile acid modifications at the microbe-host interface: potential for nutraceutical and pharmaceutical interventions in host health. Annu. Rev. Food Sci. Technol. 7 (2016), 313–333.