Dynamic Modulation of the Gut Microbiota and Metabolome by Bacteriophages in a Mouse Model

Cell Host and Microbe

Volumn 25, Issue 6, 2019, Pages 803-814.e5

  Hsu, Bryan B ^a,b   Gibson, Travis E ^c   Yeliseyev, Vladimir ^c   Liu, Qing ^c   Lyon, Lorena ^a,b   Bry, Lynn ^c   Silver, Pamela A ^a,b   Gerber, Georg K ^c  

^a HARVARD MEDICAL SCHOOL   (United States)

^b HARVARD UNIVERSITY   (United States)

^c BRIGHAM AND WOMEN S HOSPITAL   (United States)

Author keywords

bacteriophage; gut metabolome; gut microbiome; microbiota; phage resistance; phage therapy; virus

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; IN VIVO STUDY; INTESTINE FLORA; METABOLOME; MICROBIAL COMMUNITY; MODULATION; MOUSE; MOUSE MODEL; NONHUMAN; PHAGE THERAPY; PREDATION; ANIMAL; BACTERIOLYSIS; BACTERIOPHAGE; CHEMISTRY; FECES; GERMFREE ANIMAL; GROWTH, DEVELOPMENT AND AGING; ORGANISMAL INTERACTION;

ANIMALS; BACTERIOLYSIS; BACTERIOPHAGES; FECES; GASTROINTESTINAL MICROBIOME; GERM-FREE LIFE; METABOLOME; MICE; MICROBIAL INTERACTIONS;

EID: 85066807634     PISSN: 19313128     EISSN: 19346069     Source Type: Journal    
DOI: 10.1016/j.chom.2019.05.001     Document Type: Article

References (68)

1. Abrahamsson, T.R., Jakobsson, H.E., Andersson, A.F., Björkstén, B., Engstrand, L., Jenmalm, M.C., Low gut microbiota diversity in early infancy precedes asthma at school age. Clin. Exp. Allergy 44 (2014), 842–850.
2. Ackermann, H.W., Caprioli, T., Kasatiya, S.S., A large new Streptococcus bacteriophage. Can. J. Microbiol. 21 (1975), 571–574.
3. Ajslev, T.A., Andersen, C.S., Gamborg, M., Sørensen, T.I.A., Jess, T., Childhood overweight after establishment of the gut microbiota: the role of delivery mode, pre-pregnancy weight and early administration of antibiotics. Int. J. Obes. 35 (2011), 522–529.
4. Allesina, S., Tang, S., Stability criteria for complex ecosystems. Nature 483 (2012), 205–208.
5. Evans, A.M., Bridgewater, B.R., Liu, Q., Mitchell, M.W., Robinson, R.J., High resolution mass spectrometry improves data quantity and quality as compared to unit mass resolution mass spectrometry in high-throughput profiling metabolomics. Metabolomics 4 (2014), 1–7.
6. Antunes, L.C.M., Han, J., Ferreira, R.B.R., Lolić, P., Borchers, C.H., Finlay, B.B., Effect of antibiotic treatment on the intestinal metabolome. Antimicrob. Agents Chemother 55 (2011), 1494–1503.
7. Barr, J.J., Auro, R., Furlan, M., Whiteson, K.L., Erb, M.L., Pogliano, J., Stotland, A., Wolkowicz, R., Cutting, A.S., Doran, K.S., et al. Bacteriophage adhering to mucus provide a non–host-derived immunity. Proc. Natl. Acad. Sci. USA 110 (2013), 10771–10776.
8. Belkaid, Y., Hand, T.W., Role of the microbiota in immunity and inflammation. Cell 157 (2014), 121–141.
9. Betz, J.V., Anderson, K.E., Isolation and characterization of bacteriophages active on Clostridium sporogenes. J. Bacteriol 87 (1964), 408–415.
10. Bhattarai, Y., Williams, B.B., Battaglioli, E.J., Whitaker, W.R., Till, L., Grover, M., Linden, D.R., Akiba, Y., Kandimalla, K.K., Zachos, N.C., et al. Gut microbiota-produced tryptamine activates an epithelial G-protein-coupled receptor to increase colonic secretion. Cell Host Microbe 23 (2018), 775–785.e5.
11. Bisgaard, H., Li, N., Bonnelykke, K., Chawes, B.L.K., Skov, T., Paludan-Müller, G., Stokholm, J., Smith, B., Krogfelt, K.A., Reduced diversity of the intestinal microbiota during infancy is associated with increased risk of allergic disease at school age. J. Allergy Clin. Immunol 128 (2011), 646–652.
12. Blanton, L.V., Charbonneau, M.R., Salih, T., Barratt, M.J., Venkatesh, S., Ilkaveya, O., Subramanian, S., Manary, M.J., Trehan, I., Jorgensen, J.M., et al. Gut bacteria that prevent growth impairments transmitted by microbiota from malnourished children. Science, 351, 2016.
13. Brestoff, J.R., Artis, D., Commensal bacteria at the interface of host metabolism and the immune system. Nat. Immunol. 14 (2013), 676–684.
14. Britt, K., Lin Derek, M., Angus, B., Thompson John, N., The costs of evolving resistance in heterogeneous parasite environments. Proc. Biol. Sci. 279 (2012), 1896–1903.
15. Bucci, V., Tzen, B., Li, N., Simmons, M., Tanoue, T., Bogart, E., Deng, L., Yeliseyev, V., Delaney, M.L., Liu, Q., et al. MDSINE: microbial dynamical systems inference engine for microbiome time-series analyses. Genome Biol., 17, 2016, 121.
16. Buffie, C.G., Bucci, V., Stein, R.R., McKenney, P.T., Ling, L., Gobourne, A., No, D., Liu, H., Kinnebrew, M., Viale, A., et al. Precision microbiome reconstitution restores bile acid mediated resistance to Clostridium difficile. Nature 517 (2014), 205–208.
17. Callahan, B.J., McMurdie, P.J., Rosen, M.J., Han, A.W., Johnson, A.J.A., Holmes, S.P., DADA2: high-resolution sample inference from Illumina amplicon data. Nat. Methods 13 (2016), 581–583.
18. Caspi, R., Billington, R., Ferrer, L., Foerster, H., Fulcher, C.A., Keseler, I.M., Kothari, A., Krummenacker, M., Latendresse, M., Mueller, L.A., et al. The MetaCyc database of metabolic pathways and enzymes and the BioCyc collection of pathway/genome databases. Nucleic Acids Res. 44 (2016), D471–D480.
19. Chang, J.Y., Antonopoulos, D.A., Kalra, A., Tonelli, A., Khalife, W.T., Schmidt, T.M., Young, V.B., Decreased diversity of the fecal microbiome in recurrent Clostridium difficile—associated diarrhea. J. Infect. Dis. 197 (2008), 435–438.
20. Chibani-Chennoufi, S., Sidoti, J., Bruttin, A., Kutter, E., Sarker, S., Brüssow, H., In vitro and in vivo bacteriolytic activities of Escherichia coli phages: implications for phage therapy. Antimicrob. Agents Chemother. 48 (2004), 2558–2569.
21. Connil, N., Le Breton, Y., Dousset, X., Auffray, Y., Rincé, A., Prévost, H., Identification of the Enterococcus faecalis tyrosine decarboxylase operon involved in tyramine Production. Appl. Environ. Microbiol. 68 (2002), 3537–3544.
22. Denou, E., Bruttin, A., Barretto, C., Ngom-Bru, C., Brüssow, H., Zuber, S., T4 phages against Escherichia coli diarrhea: potential and problems. Virology 388 (2009), 21–30.
23. Derrien, M., van Passel, M.W.J., van de Bovenkamp, J.H.B., Schipper, R.G., de Vos, W.M., Dekker, J., Mucin-bacterial interactions in the human oral cavity and digestive tract. Gut Microbes 1 (2010), 254–268.
24. Dias, D.A., Urban, S., Roessner, U., A historical overview of natural products in drug discovery. Metabolites 2 (2012), 303–336.
25. Dorrestein, P.C., Mazmanian, S.K., Knight, R., Finding the missing links among metabolites, microbes, and the host. Immunity 40 (2014), 824–832.
26. Estes, J.A., Terborgh, J., Brashares, J.S., Power, M.E., Berger, J., Bond, W.J., Carpenter, S.R., Essington, T.E., Holt, R.D., Jackson, J.B.C., et al. Trophic downgrading of planet earth. Science 333 (2011), 301–306.
27. Fischbach, M.A., Microbiome: focus on causation and mechanism. Cell 174 (2018), 785–790.
28. Frank, D.N., St Amand, A.L., Feldman, R.A., Boedeker, E.C., Harpaz, N., Pace, N.R., Molecular-phylogenetic characterization of microbial community imbalances in human inflammatory bowel diseases. Proc. Natl. Acad. Sci. USA 104 (2007), 13780–13785.
29. Galtier, M., De Sordi, L., Maura, D., Arachchi, H., Volant, S., Dillies, M.A., Debarbieux, L., Bacteriophages to reduce gut carriage of antibiotic resistant uropathogens with low impact on microbiota composition. Environ. Microbiol. 18 (2016), 2237–2245.
30. Gerber, G.K., Onderdonk, A.B., Bry, L., Inferring dynamic signatures of microbes in complex host ecosystems. PLoS Comput. Biol., 8, 2012, e1002624.
31. Gibson, M.K., Wang, B., Ahmadi, S., Burnham, C.A., Tarr, P.I., Warner, B.B., Dantas, G., Developmental dynamics of the preterm infant gut microbiota and antibiotic resistome. Nat. Microbiol., 1, 2016, 16024.
32. Gloor, G.B., Macklaim, J.M., Pawlowsky-Glahn, V., Egozcue, J.J., Microbiome datasets are compositional: and this is not optional. Front. Microbiol., 8, 2017, 2224.
33. Harcombe, W.R., Bull, J.J., Impact of phages on two-species bacterial communities. Appl. Environ. Microbiol. 71 (2005), 5254–5259.
34. Hibbing, M.E., Fuqua, C., Parsek, M.R., Peterson, S.B., Bacterial competition: surviving and thriving in the microbial jungle. Nat. Rev. Microbiol. 8 (2010), 15–25.
35. Hsiao, E.Y., McBride, S.W., Hsien, S., Sharon, G., Hyde, E.R., McCue, T., Codelli, J.A., Chow, J., Reisman, S.E., Petrosino, J.F., et al. Microbiota modulate behavioral and physiological abnormalities associated with neurodevelopmental disorders. Cell 155 (2013), 1451–1463.
36. Keen, E.C., Dantas, G., Close encounters of three kinds: bacteriophages, commensal bacteria, and host immunity. Trends Microbiol. 26 (2018), 943–954.
37. Koskella, B., Brockhurst, M.A., Bacteria–phage coevolution as a driver of ecological and evolutionary processes in microbial communities. FEMS Microbiol. Rev. 38 (2014), 916–931.
38. Kozich, J.J., Westcott, S.L., Baxter, N.T., Highlander, S.K., Schloss, P.D., Development of a dual-index sequencing strategy and curation pipeline for analyzing amplicon sequence data on the MiSeq Illumina sequencing platform. Appl. Environ. Microbiol. 79 (2013), 5112–5120.
39. Kutter, E., Phage host range and efficiency of plating. Methods Mol. Biol 501 (2009), 141–149.
40. Le Roy, T., Llopis, M., Lepage, P., Bruneau, A., Rabot, S., Bevilacqua, C., Martin, P., Philippe, C., Walker, F., Bado, A., et al. Intestinal microbiota determines development of non-alcoholic fatty liver disease in mice. Gut 62 (2013), 1787–1794.
41. Lee, S.M., Donaldson, G.P., Mikulski, Z., Boyajian, S., Ley, K., Mazmanian, S.K., Bacterial colonization factors control specificity and stability of the gut microbiota. Nature 501 (2013), 426–429.
42. Lozupone, C.A., Stombaugh, J.I., Gordon, J.I., Jansson, J.K., Knight, R., Diversity, stability and resilience of the human gut microbiota. Nature 489 (2012), 220–230.
43. Lynch, S.V., Pedersen, O., The human intestinal microbiome in health and disease. N. Engl. J. Med. 375 (2016), 2369–2379.
44. Marcobal, A., De las Rivas, B.D.L., Landete, J.M., Tabera, L., Muñoz, R., Tyramine and phenylethylamine biosynthesis by food bacteria. Crit. Rev. Food Sci. Nutr. 52 (2012), 448–467.
45. Maura, D., Morello, E., du Merle, L., Bomme, P., Le Bouguénec, C., Debarbieux, L., Intestinal colonization by enteroaggregative Escherichia coli supports long-term bacteriophage replication in mice. Environ. Microbiol. 14 (2012), 1844–1854.
46. Miller, E.S., Kutter, E., Mosig, G., Arisaka, F., Kunisawa, T., Rüger, W., Bacteriophage T4 genome. Microbiol. Mol. Biol. Rev. 67 (2003), 86–156.
47. Mirzaei, M.K., Maurice, C.F., Ménage à trois in the human gut: interactions between host, bacteria and phages. Nat. Rev. Microbiol. 15 (2017), 397–408.
48. Nelson, M.B., Chase, A.B., Martiny, J.B.H., Stocker, R., Nguyen, J., Lloyd, K., Oshiro, R.T., Kearns, D.B., Schneider, J.P., Ringel, P.D., et al. The microbial olympics 2016. Nat. Microbiol., 1, 2016, 16122.
49. Norman, J.M., Handley, S.A., Baldridge, M.T., Droit, L., Liu, C.Y., Keller, B.C., Kambal, A., Monaco, C.L., Zhao, G., Fleshner, P., et al. Disease-specific alterations in the enteric virome in inflammatory bowel disease. Cell 160 (2015), 447–460.
50. Reyes, A., Blanton, L.V., Cao, S., Zhao, G., Manary, M., Trehan, I., Smith, M.I., Wang, D., Virgin, H.W., Rohwer, F., et al. Gut DNA viromes of Malawian twins discordant for severe acute malnutrition. Proc. Natl. Acad. Sci. USA 112 (2015), 11941–11946.
51. Reyes, A., Haynes, M., Hanson, N., Angly, F.E., Heath, A.C., Rohwer, F., Gordon, J.I., Viruses in the faecal microbiota of monozygotic twins and their mothers. Nature 466 (2010), 334–338.
52. Reyes, A., Wu, M., McNulty, N.P., Rohwer, F.L., Gordon, J.I., Gnotobiotic mouse model of phage–bacterial host dynamics in the human gut. Proc. Natl. Acad. Sci. USA 110 (2013), 20236–20241.
53. Schmidt, T.S.B., Raes, J., Bork, P., The human gut microbiome: From association to modulation. Cell 172 (2018), 1198–1215.
54. Seed, K.D., Yen, M., Shapiro, B.J., Hilaire, I.J., Charles, R.C., Teng, J.E., Ivers, L.C., Boncy, J., Harris, J.B., Camilli, A., Evolutionary consequences of intra-patient phage predation on microbial populations. Elife, 3, 2014, e03497.
55. Sender, R., Fuchs, S., Milo, R., Revised estimates for the number of human and bacteria cells in the body. PLoS Biol., 14, 2016, e1002533.
56. Shkoporov, A.N., Hill, C., Bacteriophages of the human gut: the “known unknown” of the microbiome. Cell Host Microbe 25 (2019), 195–209.
57. Smith, M.I., Yatsunenko, T., Manary, M.J., Trehan, I., Mkakosya, R., Cheng, J., Kau, A.L., Rich, S.S., Concannon, P., Mychaleckyj, J.C., et al. Gut microbiomes of Malawian twin pairs discordant for kwashiorkor. Science 339 (2013), 548–554.
58. Stoddard, S.F., Smith, B.J., Hein, R., Roller, B.R.K., Schmidt, T.M., rrnDB: improved tools for interpreting rRNA gene abundance in bacteria and archaea and a new foundation for future development. Nucleic Acids Res. 43 (2015), D593–D598.
59. Subramanian, S., Huq, S., Yatsunenko, T., Haque, R., Mahfuz, M., Alam, M.A., Benezra, A., DeStefano, J., Meier, M.F., Muegge, B.D., et al. Persistent gut microbiota immaturity in malnourished Bangladeshi children. Nature 510 (2014), 417–421.
60. Tartera, C., Jofre, J., Bacteriophages active against Bacteroides fragilis in sewage-polluted waters. Appl. Environ. Microbiol. 53 (1987), 1632–1637.
61. The Human Microbiome Project, Structure, function and diversity of the healthy human microbiome. Nature 486 (2012), 207–214.
62. Theriot, C.M., Koenigsknecht, M.J., Carlson, P.E., Hatton, G.E., Nelson, A.M., Li, B., Huffnagle, G.B., Z Li, J., Young, V.B., Antibiotic-induced shifts in the mouse gut microbiome and metabolome increase susceptibility to Clostridium difficile infection. Nat. Commun., 5, 2014, 3114.
63. Turnbaugh, P.J., Ley, R.E., Mahowald, M.A., Magrini, V., Mardis, E.R., Gordon, J.I., An obesity-associated gut microbiome with increased capacity for energy harvest. Nature 444 (2006), 1027–1031.
64. Weiss, M., Denou, E., Bruttin, A., Serra-Moreno, R., Dillmann, M.L., Brüssow, H., In vivo replication of T4 and T7 bacteriophages in germ-free mice colonized with Escherichia coli. Virology 393 (2009), 16–23.
65. Williams, B.B., Van Benschoten, A.H., Cimermancic, P., Donia, M.S., Zimmermann, M., Taketani, M., Ishihara, A., Kashyap, P.C., Fraser, J.S., Fischbach, M.A., Discovery and characterization of gut microbiota decarboxylases that can produce the neurotransmitter tryptamine. Cell Host Microbe 16 (2014), 495–503.
66. Yassour, M., Vatanen, T., Siljander, H., Hämäläinen, A.M., Härkönen, T., Ryhänen, S.J., Franzosa, E.A., Vlamakis, H., Huttenhower, C., Gevers, D., et al. Natural history of the infant gut microbiome and impact of antibiotic treatment on bacterial strain diversity and stability. Sci. Transl. Med., 8, 2016, 343ra81.
67. Zahid, M.S.H., Udden, S.M.N., Faruque, A.S.G., Calderwood, S.B., Mekalanos, J.J., Faruque, S.M., Effect of phage on the infectivity of Vibrio cholerae and emergence of genetic variants. Infect. Immun. 76 (2008), 5266–5273.
68. Zhu, W., Gregory, J.C., Org, E., Buffa, J.A., Gupta, N., Wang, Z., Li, L., Fu, X., Wu, Y., Mehrabian, M., et al. Gut microbial metabolite TMAO enhances platelet hyperreactivity and thrombosis risk. Cell 165 (2016), 111–124.