The Battle Within: Interactions of Bacteriophages and Bacteria in the Gastrointestinal Tract

Cell Host and Microbe

Volumn 25, Issue 2, 2019, Pages 210-218

  De Sordi, Luisa ^a,b   Lourenço, Marta ^a,b   Debarbieux, Laurent ^a  

^a INSTITUT PASTEUR   (France)

^b SORBONNE UNIVERSITÉ   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; BACTERIOPHAGE DNA; BACTERIOPHAGE RECEPTOR;

ANTIBIOTIC RESISTANCE; BACTERIAL VIRULENCE; BACTERIOPHAGE; COEVOLUTION; FECAL MICROBIOTA TRANSPLANTATION; FECES MICROFLORA; GASTROINTESTINAL TRACT; HUMAN; INTESTINE FLORA; METAGENOMICS; MICROBE-MICROBE INTERACTION; NONHUMAN; PHENOTYPIC VARIATION; POPULATION DYNAMICS; PRIORITY JOURNAL; REVIEW; ANIMAL; BACTERIUM; GERMFREE ANIMAL; MICROBIOLOGY; MOUSE; ORGANISMAL INTERACTION; PHYSIOLOGY; VIROLOGY;

ANIMALS; BACTERIA; BACTERIOPHAGES; BIOLOGICAL COEVOLUTION; GASTROINTESTINAL MICROBIOME; GASTROINTESTINAL TRACT; HUMANS; MICE; MICROBIAL INTERACTIONS; SPECIFIC PATHOGEN-FREE ORGANISMS;

EID: 85060770052     PISSN: 19313128     EISSN: 19346069     Source Type: Journal    
DOI: 10.1016/j.chom.2019.01.018     Document Type: Review

References (89)

1. Banks, D.J., Lei, B., Musser, J.M., Prophage induction and expression of prophage-encoded virulence factors in group A Streptococcus serotype M3 strain MGAS315. Infect. Immun. 71 (2003), 7079–7086.
2. Barnhart, B.J., Cox, S.H., Jett, J.H., Prophage induction and inactivation by UV light. J. Virol. 18 (1976), 950–955.
3. 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.
4. Belkaid, Y., Hand, T.W., Role of the microbiota in immunity and inflammation. Cell 157 (2014), 121–141.
5. Bille, E., Meyer, J., Jamet, A., Euphrasie, D., Barnier, J.P., Brissac, T., Larsen, A., Pelissier, P., Nassif, X., A virulence-associated filamentous bacteriophage of Neisseria meningitidis increases host-cell colonisation. PLoS Pathog., 13, 2017, e1006495.
6. Bobay, L.M., Touchon, M., Rocha, E.P., Pervasive domestication of defective prophages by bacteria. Proc. Natl. Acad. Sci. USA 111 (2014), 12127–12132.
7. Bolduc, B., Youens-Clark, K., Roux, S., Hurwitz, B.L., Sullivan, M.B., iVirus: facilitating new insights in viral ecology with software and community data sets imbedded in a cyberinfrastructure. ISME J. 11 (2017), 7–14.
8. Breitbart, M., Bonnain, C., Malki, K., Sawaya, N.A., Phage puppet masters of the marine microbial realm. Nat. Microbiol. 3 (2018), 754–766.
9. Brugiroux, S., Beutler, M., Pfann, C., Garzetti, D., Ruscheweyh, H.J., Ring, D., Diehl, M., Herp, S., Lötscher, Y., Hussain, S., et al. Genome-guided design of a defined mouse microbiota that confers colonization resistance against Salmonella enterica serovar Typhimurium. Nat. Microbiol., 2, 2016, 16215.
10. Brüssow, H., Canchaya, C., Hardt, W.D., Phages and the evolution of bacterial pathogens: from genomic rearrangements to lysogenic conversion. Microbiol. Mol. Biol. Rev. 68 (2004), 560–602.
11. Canchaya, C., Proux, C., Fournous, G., Bruttin, A., Brüssow, H., Prophage genomics. Microbiol. Mol. Biol. Rev. 67 (2003), 238–276.
12. Casjens, S., Prophages and bacterial genomics: what have we learned so far?. Mol. Microbiol. 49 (2003), 277–300.
13. Cornuault, J.K., Petit, M.A., Mariadassou, M., Benevides, L., Moncaut, E., Langella, P., Sokol, H., De Paepe, M., Phages infecting Faecalibacterium prausnitzii belong to novel viral genera that help to decipher intestinal viromes. Microbiome, 6, 2018, 65.
14. d'Herelle, M.F. (1917). Sur un microbe invisible antagoniste des bacilles dysentériques. C. R. Acad. Sci. 165, 373–375.
15. de Jonge, P.A., Nobrega, F.L., Brouns, S.J.J., Dutilh, B.E., Molecular and evolutionary determinants of bacteriophage host range. Trends Microbiol. 27 (2019), 51–63.
16. De Paepe, M., Hutinet, G., Son, O., Amarir-Bouhram, J., Schbath, S., Petit, M.A., Temperate phages acquire DNA from defective prophages by relaxed homologous recombination: the role of Rad52-like recombinases. PLoS Genet., 10, 2014, e1004181.
17. De Paepe, M., Tournier, L., Moncaut, E., Son, O., Langella, P., Petit, M.A., Carriage of λ latent virus is costly for its bacterial host due to frequent reactivation in monoxenic mouse intestine. PLoS Genet., 12, 2016, e1005861.
18. De Sordi, L., Khanna, V., Debarbieux, L., The gut microbiota facilitates drifts in the genetic diversity and infectivity of bacterial viruses. Cell Host Microbe 22 (2017), 801–808.
19. De Sordi, L., Lourenço, M., Debarbieux, L., “I will survive”: A tale of bacteriophage-bacteria coevolution in the gut. Gut Microbes, 2018, 1–8.
20. Debarbieux, L., Bacterial sensing of bacteriophages in communities: the search for the Rosetta stone. Curr. Opin. Microbiol. 20 (2014), 125–130.
21. Denou, E., Berger, B., Barretto, C., Panoff, J.M., Arigoni, F., Brüssow, H., Gene expression of commensal Lactobacillus johnsonii strain NCC533 during in vitro growth and in the murine gut. J. Bacteriol. 189 (2007), 8109–8119.
22. Diard, M., Bakkeren, E., Cornuault, J.K., Moor, K., Hausmann, A., Sellin, M.E., Loverdo, C., Aertsen, A., Ackermann, M., De Paepe, M., et al. Inflammation boosts bacteriophage transfer between Salmonella spp. Science 355 (2017), 1211–1215.
23. Doron, S., Melamed, S., Ofir, G., Leavitt, A., Lopatina, A., Keren, M., Amitai, G., and Sorek, R. (2018). Systematic discovery of antiphage defense systems in the microbial pangenome. Science 359.
24. Draper, L.A., Ryan, F.J., Smith, M.K., Jalanka, J., Mattila, E., Arkkila, P.A., Ross, R.P., Satokari, R., Hill, C., Long-term colonisation with donor bacteriophages following successful faecal microbial transplantation. Microbiome, 6, 2018, 220.
25. Duerkop, B.A., Clements, C.V., Rollins, D., Rodrigues, J.L., Hooper, L.V., A composite bacteriophage alters colonization by an intestinal commensal bacterium. Proc. Natl. Acad. Sci. USA 109 (2012), 17621–17626.
26. Dutilh, B.E., Cassman, N., McNair, K., Sanchez, S.E., Silva, G.G., Boling, L., Barr, J.J., Speth, D.R., Seguritan, V., Aziz, R.K., et al. A highly abundant bacteriophage discovered in the unknown sequences of human faecal metagenomes. Nat. Commun., 5, 2014, 4498.
27. Enault, F., Briet, A., Bouteille, L., Roux, S., Sullivan, M.B., Petit, M.A., Phages rarely encode antibiotic resistance genes: a cautionary tale for virome analyses. ISME J. 11 (2017), 237–247.
28. Enav, H., Kirzner, S., Lindell, D., Mandel-Gutfreund, Y., Béjà O., Adaptation to sub-optimal hosts is a driver of viral diversification in the ocean. Nat. Commun., 9, 2018, 4698.
29. Erez, Z., Steinberger-Levy, I., Shamir, M., Doron, S., Stokar-Avihail, A., Peleg, Y., Melamed, S., Leavitt, A., Savidor, A., Albeck, S., et al. Communication between viruses guides lysis-lysogeny decisions. Nature 541 (2017), 488–493.
30. Faruque, S.M., Naser, I.B., Islam, M.J., Faruque, A.S., Ghosh, A.N., Nair, G.B., Sack, D.A., Mekalanos, J.J., Seasonal epidemics of cholera inversely correlate with the prevalence of environmental cholera phages. Proc. Natl. Acad. Sci. USA 102 (2005), 1702–1707.
31. 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.
32. 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.
33. Galtier, M., De Sordi, L., Sivignon, A., de Vallée, A., Maura, D., Neut, C., Rahmouni, O., Wannerberger, K., Darfeuille-Michaud, A., Desreumaux, P., et al. Bacteriophages Targeting Adherent Invasive Escherichia coli Strains as a Promising New Treatment for Crohn's Disease. J. Crohns Colitis 11 (2016), 840–847.
34. Gandon, S., Buckling, A., Decaestecker, E., Day, T., Host-parasite coevolution and patterns of adaptation across time and space. J. Evol. Biol. 21 (2008), 1861–1866.
35. Gentile, C.L., Weir, T.L., The gut microbiota at the intersection of diet and human health. Science 362 (2018), 776–780.
36. Goerke, C., Köller, J., Wolz, C., Ciprofloxacin and trimethoprim cause phage induction and virulence modulation in Staphylococcus aureus. Antimicrob. Agents Chemother. 50 (2006), 171–177.
37. Hall, A.R., Scanlan, P.D., Morgan, A.D., Buckling, A., Host-parasite coevolutionary arms races give way to fluctuating selection. Ecol. Lett. 14 (2011), 635–642.
38. Hannigan, G.D., Duhaime, M.B., Koutra, D., Schloss, P.D., Biogeography and environmental conditions shape bacteriophage-bacteria networks across the human microbiome. PLoS Comput. Biol., 14, 2018, e1006099.
39. Harrison, E., Brockhurst, M.A., Ecological and evolutionary benefits of temperate phage: what does or doesn't kill you makes you stronger. BioEssays, 39, 2017.
40. Hochberg, M.E., An ecosystem framework for understanding and treating disease. Evol. Med. Public Health 2018 (2018), 270–286.
41. Holst Sørensen, M.C., van Alphen, L.B., Fodor, C., Crowley, S.M., Christensen, B.B., Szymanski, C.M., Brøndsted, L., Phase variable expression of capsular polysaccharide modifications allows Campylobacter jejuni to avoid bacteriophage infection in chickens. Front. Cell. Infect. Microbiol., 2, 2012, 11.
42. Howard-Varona, C., Hargreaves, K.R., Abedon, S.T., Sullivan, M.B., Lysogeny in nature: mechanisms, impact and ecology of temperate phages. ISME J. 11 (2017), 1511–1520.
43. Kim, M.S., Bae, J.W., Lysogeny is prevalent and widely distributed in the murine gut microbiota. ISME J. 12 (2018), 1127–1141.
44. 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.
45. Kronheim, S., Daniel-Ivad, M., Duan, Z., Hwang, S., Wong, A.I., Mantel, I., Nodwell, J.R., Maxwell, K.L., A chemical defence against phage infection. Nature 564 (2018), 283–286.
46. Labrie, S.J., Samson, J.E., Moineau, S., Bacteriophage resistance mechanisms. Nat. Rev. Microbiol. 8 (2010), 317–327.
47. Lennon, J.T., Khatana, S.A., Marston, M.F., Martiny, J.B., Is there a cost of virus resistance in marine cyanobacteria?. ISME J. 1 (2007), 300–312.
48. Ley, R.E., Turnbaugh, P.J., Klein, S., Gordon, J.I., Microbial ecology: human gut microbes associated with obesity. Nature 444 (2006), 1022–1023.
49. Lourenço, M., De Sordi, L., Debarbieux, L., The diversity of bacterial lifestyles hampers bacteriophage tenacity. Viruses, 10, 2018.
50. Lwoff, A., Lysogeny. Bacteriol. Rev. 17 (1953), 269–337.
51. Manrique, P., Bolduc, B., Walk, S.T., van der Oost, J., de Vos, W.M., Young, M.J., Healthy human gut phageome. Proc. Natl. Acad. Sci. USA 113 (2016), 10400–10405.
52. Matos, R.C., Lapaque, N., Rigottier-Gois, L., Debarbieux, L., Meylheuc, T., Gonzalez-Zorn, B., Repoila, F., Lopes, Mde.F., Serror, P., Enterococcus faecalis prophage dynamics and contributions to pathogenic traits. PLoS Genet., 9, 2013, e1003539.
53. Maura, D., Galtier, M., Le Bouguénec, C., Debarbieux, L., Virulent bacteriophages can target O104:H4 enteroaggregative Escherichia coli in the mouse intestine. Antimicrob. Agents Chemother. 56 (2012), 6235–6242.
54. Middelboe, M., Holmfeldt, K., Riemann, L., Nybroe, O., Haaber, J., Bacteriophages drive strain diversification in a marine Flavobacterium: implications for phage resistance and physiological properties. Environ. Microbiol. 11 (2009), 1971–1982.
55. Minot, S., Sinha, R., Chen, J., Li, H., Keilbaugh, S.A., Wu, G.D., Lewis, J.D., Bushman, F.D., The human gut virome: inter-individual variation and dynamic response to diet. Genome Res. 21 (2011), 1616–1625.
56. Minot, S., Bryson, A., Chehoud, C., Wu, G.D., Lewis, J.D., Bushman, F.D., Rapid evolution of the human gut virome. Proc. Natl. Acad. Sci. USA 110 (2013), 12450–12455.
57. Monaco, C.L., Gootenberg, D.B., Zhao, G., Handley, S.A., Ghebremichael, M.S., Lim, E.S., Lankowski, A., Baldridge, M.T., Wilen, C.B., Flagg, M., et al. Altered virome and bacterial microbiome in human immunodeficiency virus-associated acquired immunodeficiency syndrome. Cell Host Microbe 19 (2016), 311–322.
58. Muniesa, M., Hammerl, J.A., Hertwig, S., Appel, B., Brüssow, H., Shiga toxin-producing Escherichia coli O104:H4: a new challenge for microbiology. Appl. Environ. Microbiol. 78 (2012), 4065–4073.
59. 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.
60. Obeng, N., Pratama, A.A., Elsas, J.D.V., The significance of mutualistic phages for bacterial ecology and evolution. Trends Microbiol. 24 (2016), 440–449.
61. Oh, J.H., Alexander, L.M., Pan, M., Schueler, K.L., Keller, M.P., Attie, A.D., Walter, J., van Pijkeren, J.P., Dietary fructose and microbiota-derived short-chain fatty acids promote bacteriophage production in the gut symbiont Lactobacillus reuteri. Cell Host Microbe, 2018, 10.1016/j.chom.2018.11.016 Published online December 24, 2018.
62. Ott, S.J., Waetzig, G.H., Rehman, A., Moltzau-Anderson, J., Bharti, R., Grasis, J.A., Cassidy, L., Tholey, A., Fickenscher, H., Seegert, D., et al. Efficacy of sterile fecal filtrate transfer for treating patients with Clostridium difficile infection. Gastroenterology 152 (2017), 799–811.
63. Paez-Espino, D., Eloe-Fadrosh, E.A., Pavlopoulos, G.A., Thomas, A.D., Huntemann, M., Mikhailova, N., Rubin, E., Ivanova, N.N., Kyrpides, N.C., Uncovering Earth's virome. Nature 536 (2016), 425–430.
64. Paez-Espino, D., Roux, S., Chen, I.A., Palaniappan, K., Ratner, A., Chu, K., Huntemann, M., Reddy, T.B.K., Pons, J.C., Llabrés, M., et al. IMG/VR v.2.0: an integrated data management and analysis system for cultivated and environmental viral genomes. Nucleic Acids Res. 47:D1 (2019), D678–D686.
65. Pasolli, E., Asnicar, F., Manara, S., Zolfo, M., Karcher, N., Armanini, F., Beghini, F., Manghi, P., Tett, A., Ghensi, P., et al. Extensive unexplored human microbiome diversity revealed by over 150,000 genomes from metagenomes spanning age, geography, and lifestyle. Cell 176 (2019), 649–662.
66. Qin, J., Li, Y., Cai, Z., Li, S., Zhu, J., Zhang, F., Liang, S., Zhang, W., Guan, Y., Shen, D., et al. A metagenome-wide association study of gut microbiota in type 2 diabetes. Nature 490 (2012), 55–60.
67. 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.
68. Reyes, A., Semenkovich, N.P., Whiteson, K., Rohwer, F., Gordon, J.I., Going viral: next-generation sequencing applied to phage populations in the human gut. Nat. Rev. Microbiol. 10 (2012), 607–617.
69. 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.
70. Reyes, A., Blanton, L.V., Cao, S., Zhao, G., Manary, M., Trehan, I., Smith, M.I., Wang, D., Virgin, H.W., Rohwer, F., Gordon, J.I., Gut DNA viromes of Malawian twins discordant for severe acute malnutrition. Proc. Natl. Acad. Sci. USA 112 (2015), 11941–11946.
71. Roach, D.R., Debarbieux, L., Phage therapy: awakening a sleeping giant. Emerg. Top. Life Sci. 1 (2017), 93–103.
72. Routy, B., Le Chatelier, E., Derosa, L., Duong, C.P.M., Alou, M.T., Daillère, R., Fluckiger, A., Messaoudene, M., Rauber, C., Roberti, M.P., et al. Gut microbiome influences efficacy of PD-1-based immunotherapy against epithelial tumors. Science 359 (2018), 91–97.
73. Roux, S., Emerson, J.B., Eloe-Fadrosh, E.A., Sullivan, M.B., Benchmarking viromics: an in silico evaluation of metagenome-enabled estimates of viral community composition and diversity. PeerJ, 5, 2017, e3817.
74. Scanlan, P.D., Bacteria-bacteriophage coevolution in the human gut: implications for microbial diversity and functionality. Trends Microbiol. 25 (2017), 614–623.
75. 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.
76. Sharon, G., Sampson, T.R., Geschwind, D.H., Mazmanian, S.K., The central nervous system and the gut microbiome. Cell 167 (2016), 915–932.
77. Shkoporov, A.N., Khokhlova, E.V., Fitzgerald, C.B., Stockdale, S.R., Draper, L.A., Ross, R.P., Hill, C., ΦCrAss001 represents the most abundant bacteriophage family in the human gut and infects Bacteroides intestinalis. Nat. Commun., 9, 2018, 4781.
78. Silpe, J.E., Bassler, B.L., A host-produced quorum-sensing autoinducer controls a phage lysis-lysogeny decision. Cell 176 (2019), 268–280.
79. Singer, E., Wagner, M., Woyke, T., Capturing the genetic makeup of the active microbiome in situ. ISME J. 11 (2017), 1949–1963.
80. Smith, H.W., Huggins, M.B., Effectiveness of phages in treating experimental Escherichia coli diarrhoea in calves, piglets and lambs. J. Gen. Microbiol. 129 (1983), 2659–2675.
81. Sonnenburg, J.L., Xu, J., Leip, D.D., Chen, C.H., Westover, B.P., Weatherford, J., Buhler, J.D., Gordon, J.I., Glycan foraging in vivo by an intestine-adapted bacterial symbiont. Science 307 (2005), 1955–1959.
82. Stern, A., Mick, E., Tirosh, I., Sagy, O., Sorek, R., CRISPR targeting reveals a reservoir of common phages associated with the human gut microbiome. Genome Res. 22 (2012), 1985–1994.
83. Van Belleghem, J.D., Dąbrowska, K., Vaneechoutte, M., Barr, J.J., Bollyky, P.L., Interactions between bacteriophage, bacteria, and the mammalian immune system. Viruses, 11, 2018.
84. Weitz, J.S., Poisot, T., Meyer, J.R., Flores, C.O., Valverde, S., Sullivan, M.B., Hochberg, M.E., Phage-bacteria infection networks. Trends Microbiol. 21 (2013), 82–91.
85. Yutin, N., Makarova, K.S., Gussow, A.B., Krupovic, M., Segall, A., Edwards, R.A., Koonin, E.V., Discovery of an expansive bacteriophage family that includes the most abundant viruses from the human gut. Nat. Microbiol. 3 (2018), 38–46.
86. Zhao, G., Vatanen, T., Droit, L., Park, A., Kostic, A.D., Poon, T.W., Vlamakis, H., Siljander, H., Härkönen, T., Hämäläinen, A.M., et al. Intestinal virome changes precede autoimmunity in type I diabetes-susceptible children. Proc. Natl. Acad. Sci. USA 114 (2017), E6166–E6175.
87. Zhu, A., Sunagawa, S., Mende, D.R., Bork, P., Inter-individual differences in the gene content of human gut bacterial species. Genome Biol., 16, 2015, 82.
88. Zhu, X., Han, Y., Du, J., Liu, R., Jin, K., Yi, W., Microbiota-gut-brain axis and the central nervous system. Oncotarget 8 (2017), 53829–53838.
89. Zuo, T., Wong, S.H., Lam, K., Lui, R., Cheung, K., Tang, W., Ching, J.Y.L., Chan, P.K.S., Chan, M.C.W., Wu, J.C.Y., et al. Bacteriophage transfer during faecal microbiota transplantation in Clostridium difficile infection is associated with treatment outcome. Gut 67 (2018), 634–643.