1932

Abstract

The gut microbiome is a dense and metabolically active consortium of microorganisms and viruses located in the lower gastrointestinal tract of the human body. Bacteria and their viruses (phages) are the most abundant members of the gut microbiome. Investigating their biology and the interplay between the two is important if we are to understand their roles in human health and disease. In this review, we summarize recent advances in resolving the taxonomic structure and ecological functions of the complex community of phages in the human gut—the gut phageome. We discuss how age, diet, and geography can all have a significant impact on phageome composition. We note that alterations to the gut phageome have been observed in several diseases such as inflammatory bowel disease, irritable bowel syndrome, and colorectal cancer, and we evaluate whether these phageome changes can directly or indirectly contribute to disease etiology and pathogenesis. We also highlight how lack of standardization in studying the gut phageome has contributed to variation in reported results.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-micro-032421-105754
2023-09-15
2024-05-02
Loading full text...

Full text loading...

/deliver/fulltext/micro/77/1/annurev-micro-032421-105754.html?itemId=/content/journals/10.1146/annurev-micro-032421-105754&mimeType=html&fmt=ahah

Literature Cited

  1. 1.
    Adriaenssens EM, Farkas K, Harrison C, Jones DL, Allison HE, McCarthy AJ. 2018. Viromic analysis of wastewater input to a river catchment reveals a diverse assemblage of RNA viruses. mSystems 3:e00025–18
    [Google Scholar]
  2. 2.
    Aggarwala V, Liang G, Bushman FD. 2017. Viral communities of the human gut: metagenomic analysis of composition and dynamics. Mob. DNA 8:12
    [Google Scholar]
  3. 3.
    Ansari MH, Ebrahimi M, Fattahi MR, Gardner MG, Safarpour AR et al. 2020. Viral metagenomic analysis of fecal samples reveals an enteric virome signature in irritable bowel syndrome. BMC Microbiol. 20:123
    [Google Scholar]
  4. 4.
    Barylski J, Kropinski AM, Alikhan NF, Adriaenssens EM, ICTV Rep. Consort 2020. ICTV virus taxonomy profile: Herelleviridae. J. Gen. Virol. 101:362–63
    [Google Scholar]
  5. 5.
    Beller L, Deboutte W, Falony G, Vieira-Silva S, Tito RY et al. 2021. Successional stages in infant gut microbiota maturation. mBio 12:e0185721
    [Google Scholar]
  6. 6.
    Beller L, Deboutte W, Vieira-Silva S, Falony G, Tito RY et al. 2022. The virota and its transkingdom interactions in the healthy infant gut. PNAS 119:e2114619119
    [Google Scholar]
  7. 7.
    Benler S, Yutin N, Antipov D, Rayko M, Shmakov S et al. 2021. Thousands of previously unknown phages discovered in whole-community human gut metagenomes. Microbiome 9:78
    [Google Scholar]
  8. 8.
    Bin Jang H, Bolduc B, Zablocki O, Kuhn JH, Roux S et al. 2019. Taxonomic assignment of uncultivated prokaryotic virus genomes is enabled by gene-sharing networks. Nat. Biotechnol. 37:632–39
    [Google Scholar]
  9. 9.
    Boling L, Cuevas DA, Grasis JA, Kang HS, Knowles B et al. 2020. Dietary prophage inducers and antimicrobials: toward landscaping the human gut microbiome. Gut Microbes 11:721–34
    [Google Scholar]
  10. 10.
    Borodovich T, Shkoporov AN, Ross RP, Hill C. 2022. Phage-mediated horizontal gene transfer and its implications for the human gut microbiome. Gastroenterol. Rep. 10:goac012
    [Google Scholar]
  11. 11.
    Breitbart M, Haynes M, Kelley S, Angly F, Edwards RA et al. 2008. Viral diversity and dynamics in an infant gut. Res. Microbiol. 159:367–73
    [Google Scholar]
  12. 12.
    Camarillo-Guerrero LF, Almeida A, Rangel-Pineros G, Finn RD, Lawley TD. 2021. Massive expansion of human gut bacteriophage diversity. Cell 184:1098–109.e9
    [Google Scholar]
  13. 13.
    Cao J, Wang C, Zhang Y, Lei G, Xu K et al. 2021. Integrated gut virome and bacteriome dynamics in COVID-19 patients. Gut Microbes 13:1887722
    [Google Scholar]
  14. 14.
    Cenens W, Makumi A, Mebrhatu MT, Lavigne R, Aertsen A. 2013. Phage-host interactions during pseudolysogeny: lessons from the Pid/dgo interaction. Bacteriophage 3:e25029
    [Google Scholar]
  15. 15.
    Cheng Y, Ling Z, Li L. 2020. The intestinal microbiota and colorectal cancer. Front. Immunol. 11:615056
    [Google Scholar]
  16. 16.
    Chey WD, Kurlander J, Eswaran S. 2015. Irritable bowel syndrome: a clinical review. JAMA 313:949–58
    [Google Scholar]
  17. 17.
    Clooney AG, Sutton TDS, Shkoporov AN, Holohan RK, Daly KM et al. 2019. Whole-virome analysis sheds light on viral dark matter in inflammatory bowel disease. Cell Host Microbe 26:764–78.e5
    [Google Scholar]
  18. 18.
    Conceição-Neto N, Zeller M, Lefrère H, De Bruyn P, Beller L et al. 2015. Modular approach to customise sample preparation procedures for viral metagenomics: a reproducible protocol for virome analysis. Sci. Rep. 5:16532
    [Google Scholar]
  19. 19.
    Coughlan S, Das A, O'Herlihy E, Shanahan F, O'Toole PW, Jeffery IB. 2021. The gut virome in Irritable Bowel Syndrome differs from that of controls. Gut Microbes 13:1
    [Google Scholar]
  20. 20.
    de Jonge PA, Wortelboer K, Scheithauer TPM, van den Born BH, Zwinderman AH et al. 2022. Gut virome profiling identifies a widespread bacteriophage family associated with metabolic syndrome. Nat. Commun. 13:3594
    [Google Scholar]
  21. 21.
    De Sordi L, Lourenço M, Debarbieux L. 2019. The battle within: interactions of bacteriophages and bacteria in the gastrointestinal tract. Cell Host Microbe 25:210–18
    [Google Scholar]
  22. 22.
    Dejea CM, Wick EC, Hechenbleikner EM, White JR, Mark Welch JL et al. 2014. Microbiota organization is a distinct feature of proximal colorectal cancers. PNAS 111:18321–26
    [Google Scholar]
  23. 23.
    Dekker E, Tanis PJ, Vleugels JLA, Kasi PM, Wallace MB. 2019. Colorectal cancer. Lancet 394:1467–80
    [Google Scholar]
  24. 24.
    Devoto AE, Santini JM, Olm MR, Anantharaman K, Munk P et al. 2019. Megaphages infect Prevotella and variants are widespread in gut microbiomes. Nat. Microbiol. 4:693–700
    [Google Scholar]
  25. 25.
    Dutilh BE, Cassman N, McNair K, Sanchez SE, Silva GG et al. 2014. A highly abundant bacteriophage discovered in the unknown sequences of human faecal metagenomes. Nat. Commun. 5:4498
    [Google Scholar]
  26. 26.
    Edwards RA, Vega AA, Norman HM, Ohaeri M, Levi K et al. 2019. Global phylogeography and ancient evolution of the widespread human gut virus crAssphage. Nat. Microbiol. 4:1727–36
    [Google Scholar]
  27. 27.
    Fernandes MA, Verstraete SG, Phan TG, Deng X, Stekol E et al. 2019. Enteric virome and bacterial microbiota in children with ulcerative colitis and Crohn disease. J. Pediatr. Gastroenterol. Nutr. 68:30–36
    [Google Scholar]
  28. 28.
    Gao R, Zhu Y, Kong C, Xia K, Li H et al. 2021. Alterations, interactions, and diagnostic potential of gut bacteria and viruses in colorectal cancer. Front. Cell Infect. Microbiol. 11:657867
    [Google Scholar]
  29. 29.
    Garmaeva S, Gulyaeva A, Sinha T, Shkoporov AN, Clooney AG et al. 2021. Stability of the human gut virome and effect of gluten-free diet. Cell Rep. 35:109132
    [Google Scholar]
  30. 30.
    Gogokhia L, Buhrke K, Bell R, Hoffman B, Brown DG et al. 2019. Expansion of bacteriophages is linked to aggravated intestinal inflammation and colitis. Cell Host Microbe 25:285–99.e8
    [Google Scholar]
  31. 31.
    Gregory AC, Zablocki O, Zayed AA, Howell A, Bolduc B, Sullivan MB. 2020. The Gut Virome Database reveals age-dependent patterns of virome diversity in the human gut. Cell Host Microbe 28:724–40.e8
    [Google Scholar]
  32. 32.
    Guerin E, Hill C. 2020. Shining light on human gut bacteriophages. Front. Cell Infect. Microbiol. 10:481
    [Google Scholar]
  33. 33.
    Guerin E, Shkoporov A, Stockdale SR, Clooney AG, Ryan FJ et al. 2018. Biology and taxonomy of crAss-like bacteriophages, the most abundant virus in the human gut. Cell Host Microbe 24:653–64.e6
    [Google Scholar]
  34. 34.
    Gulyaeva A, Garmaeva S, Ruigrok R, Wang D, Riksen NP et al. 2022. Discovery, diversity, and functional associations of crAss-like phages in human gut metagenomes from four Dutch cohorts. Cell Rep. 38:110204
    [Google Scholar]
  35. 35.
    Gupta VK, Paul S, Dutta C. 2017. Geography, ethnicity or subsistence-specific variations in human microbiome composition and diversity. Front. Microbiol. 8:1162
    [Google Scholar]
  36. 36.
    Hannigan GD, Duhaime MB, Ruffin MT 4th, Koumpouras CC, Schloss PD. 2018. Diagnostic potential and interactive dynamics of the colorectal cancer virome. mBio 9:6e02248–18
    [Google Scholar]
  37. 37.
    Hashemi Goradel N, Heidarzadeh S, Jahangiri S, Farhood B, Mortezaee K et al. 2019. Fusobacterium nucleatum and colorectal cancer: a mechanistic overview. J. Cell Physiol. 234:2337–44
    [Google Scholar]
  38. 38.
    Hobbs Z, Abedon ST. 2016. Diversity of phage infection types and associated terminology: the problem with ‘Lytic or lysogenic. ’. FEMS Microbiol. Lett. 363:7fnw047
    [Google Scholar]
  39. 39.
    Hoyles L, McCartney AL, Neve H, Gibson GR, Sanderson JD et al. 2014. Characterization of virus-like particles associated with the human faecal and caecal microbiota. Res. Microbiol. 165:10803–12
    [Google Scholar]
  40. 40.
    Imai T, Inoue R, Nishida A, Yokota Y, Morishima S et al. 2022. Features of the gut prokaryotic virome of Japanese patients with Crohn's disease. J. Gastroenterol. 57:559–70
    [Google Scholar]
  41. 41.
    Johansen J, Plichta DR, Nissen JN, Jespersen ML, Shah SA et al. 2022. Genome binning of viral entities from bulk metagenomics data. Nat. Commun. 13:965
    [Google Scholar]
  42. 42.
    Kanauchi O, Fukuda M, Matsumoto Y, Ishii S, Ozawa T et al. 2006. Eubacterium limosum ameliorates experimental colitis and metabolite of microbe attenuates colonic inflammatory action with increase of mucosal integrity. World J. Gastroenterol. 12:71071–77
    [Google Scholar]
  43. 43.
    Kim KH, Bae JW. 2011. Amplification methods bias metagenomic libraries of uncultured single-stranded and double-stranded DNA viruses. Appl. Environ. Microbiol. 77:7663–68
    [Google Scholar]
  44. 44.
    Kim MS, Bae JW. 2016. Spatial disturbances in altered mucosal and luminal gut viromes of diet-induced obese mice. Environ. Microbiol. 18:1498–510
    [Google Scholar]
  45. 45.
    Kostic AD, Chun E, Robertson L, Glickman JN, Gallini CA et al. 2013. Fusobacterium nucleatum potentiates intestinal tumorigenesis and modulates the tumor-immune microenvironment. Cell Host Microbe 14:207–15
    [Google Scholar]
  46. 46.
    Krela-Kaźmierczak I, Zakerska-Banaszak O, Skrzypczak-Zielińska M, Łykowska-Szuber L, Szymczak-Tomczak A et al. 2022. Where do we stand in the behavioral pathogenesis of inflammatory bowel disease? The Western dietary pattern and microbiota—a narrative review. Nutrients 14:122520
    [Google Scholar]
  47. 47.
    Krupovic M, Turner D, Morozova V, Dyall-Smith M, Oksanen HM et al. 2021. Bacterial Viruses Subcommittee and Archaeal Viruses Subcommittee of the ICTV: update of taxonomy changes in 2021. Arch. Virol. 166:3239–44
    [Google Scholar]
  48. 48.
    Lacy BE, Patel NK. 2017. Rome criteria and a diagnostic approach to irritable bowel syndrome. J. Clin. Med. 6:1199
    [Google Scholar]
  49. 49.
    Lee CZ, Zoqratt M, Phipps ME, Barr JJ, Lal SK et al. 2022. The gut virome in two indigenous populations from Malaysia. Sci. Rep. 12:1824
    [Google Scholar]
  50. 50.
    Li M, Wang C, Guo Q, Xu C, Xie Z et al. 2022. More positive or more negative? Metagenomic analysis reveals roles of virome in human disease-related gut microbiome. Front. Cell Infect. Microbiol. 12:846063
    [Google Scholar]
  51. 51.
    Li Y, Zhang F, Zheng H, Kalasabail S, Hicks C et al. 2022. Fecal DNA virome is associated with the development of colorectal neoplasia in a murine model of colorectal cancer. Pathogens 11:4457
    [Google Scholar]
  52. 52.
    Liang G, Conrad MA, Kelsen JR, Kessler LR, Breton J et al. 2020. Dynamics of the stool virome in very early-onset inflammatory bowel disease. J. Crohn's Colitis 14:1600–10
    [Google Scholar]
  53. 53.
    Liang G, Zhao C, Zhang H, Mattei L, Sherrill-Mix S et al. 2020. The stepwise assembly of the neonatal virome is modulated by breastfeeding. Nature 581:470–74
    [Google Scholar]
  54. 54.
    Lim ES, Zhou Y, Zhao G, Bauer IK, Droit L et al. 2015. Early life dynamics of the human gut virome and bacterial microbiome in infants. Nat. Med. 21:1228–34
    [Google Scholar]
  55. 55.
    Los M, Wegrzyn G, Neubauer P. 2003. A role for bacteriophage T4 rI gene function in the control of phage development during pseudolysogeny and in slowly growing host cells. Res. Microbiol. 154:547–52
    [Google Scholar]
  56. 56.
    Lourenço M, Chaffringeon L, Lamy-Besnier Q, Pédron T, Campagne P et al. 2020. The spatial heterogeneity of the gut limits predation and fosters coexistence of bacteria and bacteriophages. Cell Host Microbe 28:390–401.e5
    [Google Scholar]
  57. 57.
    Lu ZH, Zhou HW, Wu WK, Fu T, Yan M et al. 2021. Alterations in the composition of intestinal DNA virome in patients with COVID-19. Front. Cell Infect. Microbiol. 11:790422
    [Google Scholar]
  58. 58.
    Mäntynen S, Laanto E, Oksanen HM, Poranen MM, Díaz-Muñoz SL. 2021. Black box of phage-bacterium interactions: exploring alternative phage infection strategies. Open. Biol. 11:210188
    [Google Scholar]
  59. 59.
    Mármol I, Sánchez-de-Diego C, Pradilla Dieste A, Cerrada E, Rodriguez Yoldi MJ. 2017. Colorectal carcinoma: a general overview and future perspectives in colorectal cancer. Int. J. Mol. Sci. 18:1197
    [Google Scholar]
  60. 60.
    McGovern DP, Kugathasan S, Cho JH. 2015. Genetics of inflammatory bowel diseases. Gastroenterology 149:1163–76.e2
    [Google Scholar]
  61. 61.
    Meng M, Zhong K, Jiang T, Liu Z, Kwan HY, Su T. 2021. The current understanding on the impact of KRAS on colorectal cancer. Biomed. Pharmacother. 140:111717
    [Google Scholar]
  62. 62.
    Mihindukulasuriya KA, Mars RAT, Johnson AJ, Ward T, Priya S et al. 2021. Multi-omics analyses show disease, diet, and transcriptome interactions with the virome. Gastroenterology 161:1194–207.e8
    [Google Scholar]
  63. 63.
    Minot S, Sinha R, Chen J, Li H, Keilbaugh SA et al. 2011. The human gut virome: inter-individual variation and dynamic response to diet. Genome Res. 21:1616–25
    [Google Scholar]
  64. 64.
    Mirsepasi-Lauridsen HC, Vallance BA, Krogfelt KA, Petersen AM. 2019. Escherichia coli pathobionts associated with inflammatory bowel disease. 322e00060–18
  65. 65.
    Monaghan TM, Sloan TJ, Stockdale SR, Blanchard AM, Emes RD et al. 2020. Metagenomics reveals impact of geography and acute diarrheal disease on the Central Indian human gut microbiome. Gut Microbes 12:1752605
    [Google Scholar]
  66. 66.
    Nakatsu G, Zhou H, Wu WKK, Wong SH, Coker OO et al. 2018. Alterations in enteric virome are associated with colorectal cancer and survival outcomes. Gastroenterology 155:529–41.e5
    [Google Scholar]
  67. 67.
    Nayfach S, Páez-Espino D, Call L, Low SJ, Sberro H et al. 2021. Metagenomic compendium of 189,680 DNA viruses from the human gut microbiome. Nat. Microbiol. 6:960–70
    [Google Scholar]
  68. 68.
    Neri U, Wolf YI, Roux S, Camargo AP, Lee B et al. 2022. Expansion of the global RNA virome reveals diverse clades of bacteriophages. Cell 185:214023–37.e18
    [Google Scholar]
  69. 69.
    Nishijima S, Nagata N, Kiguchi Y, Kojima Y, Miyoshi-Akiyama T et al. 2022. Extensive gut virome variation and its associations with host and environmental factors in a population-level cohort. Nat. Commun. 13:5252
    [Google Scholar]
  70. 70.
    Norman JM, Handley SA, Baldridge MT, Droit L, Liu CY et al. 2015. Disease-specific alterations in the enteric virome in inflammatory bowel disease. Cell 160:447–60
    [Google Scholar]
  71. 71.
    Odamaki T, Kato K, Sugahara H, Hashikura N, Takahashi S et al. 2016. Age-related changes in gut microbiota composition from newborn to centenarian: a cross-sectional study. BMC Microbiol. 16:90
    [Google Scholar]
  72. 72.
    Oh JH, Alexander LM, Pan M, Schueler KL, Keller MP et al. 2019. Dietary fructose and microbiota-derived short-chain fatty acids promote bacteriophage production in the gut symbiont Lactobacillus reuteri. Cell Host Microbe 25:273–84.e6
    [Google Scholar]
  73. 73.
    Paez-Espino D, Zhou J, Roux S, Nayfach S, Pavlopoulos GA et al. 2019. Diversity, evolution, and classification of virophages uncovered through global metagenomics. Microbiome 7:157
    [Google Scholar]
  74. 74.
    Pérez-Brocal V, García-López R, Vázquez-Castellanos JF, Nos P, Beltrán B et al. 2013. Study of the viral and microbial communities associated with Crohn's disease: a metagenomic approach. Clin. Transl. Gastroenterol. 4:e36
    [Google Scholar]
  75. 75.
    Roux S, Adriaenssens EM, Dutilh BE, Koonin EV, Kropinski AM et al. 2019. Minimum Information about an Uncultivated Virus Genome (MIUViG). Nat. Biotechnol. 37:29–37
    [Google Scholar]
  76. 76.
    Roux S, Hallam SJ, Woyke T, Sullivan MB. 2015. Viral dark matter and virus-host interactions resolved from publicly available microbial genomes. eLife 4:e08490
    [Google Scholar]
  77. 77.
    Schulfer A, Santiago-Rodriguez TM, Ly M, Borin JM, Chopyk J et al. 2020. Fecal viral community responses to high-fat diet in mice. mSphere 5:1e00833–19
    [Google Scholar]
  78. 78.
    Secor PR, Sweere JM, Michaels LA, Malkovskiy AV, Lazzareschi D et al. 2015. Filamentous bacteriophage promote biofilm assembly and function. Cell Host Microbe 18:549–59
    [Google Scholar]
  79. 79.
    Sender R, Fuchs S, Milo R. 2016. Revised estimates for the number of human and bacteria cells in the body. PLOS Biol. 14:e1002533
    [Google Scholar]
  80. 80.
    Shen S, Huo D, Ma C, Jiang S, Zhang J. 2021. Expanding the colorectal cancer biomarkers based on the human gut phageome. Microbiol. Spectr. 9:e0009021
    [Google Scholar]
  81. 81.
    Shkoporov AN, Clooney AG, Sutton TDS, Ryan FJ, Daly KM et al. 2019. The human gut virome is highly diverse, stable, and individual specific. Cell Host Microbe 26:527–41.e5
    [Google Scholar]
  82. 82.
    Shkoporov AN, Hill C. 2019. Bacteriophages of the human gut: the “known unknown” of the microbiome. Cell Host Microbe 25:195–209
    [Google Scholar]
  83. 83.
    Shkoporov AN, Khokhlova EV, Stephens N, Hueston C, Seymour S et al. 2021. Long-term persistence of crAss-like phage crAss001 is associated with phase variation in Bacteroides intestinalis. BMC Biol. 19:163
    [Google Scholar]
  84. 84.
    Shkoporov AN, Ryan FJ, Draper LA, Forde A, Stockdale SR et al. 2018. Reproducible protocols for metagenomic analysis of human faecal phageomes. Microbiome 6:68
    [Google Scholar]
  85. 85.
    Shkoporov AN, Turkington CJ, Hill C. 2022. Mutualistic interplay between bacteriophages and bacteria in the human gut. Nat. Rev. Microbiol. 20:12737–49
    [Google Scholar]
  86. 86.
    Sinha A, Li Y, Mirzaei MK, Shamash M, Samadfam R et al. 2022. Transplantation of bacteriophages from ulcerative colitis patients shifts the gut bacteriome and exacerbates the severity of DSS colitis. Microbiome 10:105
    [Google Scholar]
  87. 87.
    Siringan P, Connerton PL, Cummings NJ, Connerton IF. 2014. Alternative bacteriophage life cycles: the carrier state of Campylobacter jejuni. Open. Biol. 4:130200
    [Google Scholar]
  88. 88.
    Smith L, Goldobina E, Govi B, Shkoporov AN. 2023. Bacteriophages of the order Crassvirales: What do we currently know about this keystone component of the human gut virome?. Biomolecules 13:4584
    [Google Scholar]
  89. 89.
    Sutton TDS, Clooney AG, Hill C. 2020. Giant oversights in the human gut virome. Gut 69:71357–58
    [Google Scholar]
  90. 90.
    Sutton TDS, Clooney AG, Ryan FJ, Ross RP, Hill C. 2019. Choice of assembly software has a critical impact on virome characterisation. Microbiome 7:12
    [Google Scholar]
  91. 91.
    Sutton TDS, Hill C. 2019. Gut bacteriophage: current understanding and challenges. Front. Endocrinol. 10:784
    [Google Scholar]
  92. 92.
    Taboada B, Morán P, Serrano-Vázquez A, Iša P, Rojas-Velázquez L et al. 2021. The gut virome of healthy children during the first year of life is diverse and dynamic. PLOS ONE 16:e0240958
    [Google Scholar]
  93. 93.
    Tisza MJ, Buck CB. 2021. A catalog of tens of thousands of viruses from human metagenomes reveals hidden associations with chronic diseases. PNAS 118:23e2023202118
    [Google Scholar]
  94. 94.
    Tomofuji Y, Kishikawa T, Maeda Y, Ogawa K, Nii T et al. 2022. Whole gut virome analysis of 476 Japanese revealed a link between phage and autoimmune disease. Ann. Rheum. Dis. 81:278–88
    [Google Scholar]
  95. 95.
    Tomova A, Bukovsky I, Rembert E, Yonas W, Alwarith J et al. 2019. The effects of vegetarian and vegan diets on gut microbiota. Front. Nutr. 6:47
    [Google Scholar]
  96. 96.
    Turner D, Kropinski AM, Adriaenssens EM. 2021. A roadmap for genome-based phage taxonomy. Viruses 13:3506
    [Google Scholar]
  97. 97.
    Turner D, Shkoporov AN, Lood C, Millard AD, Dutilh BE et al. 2023. Abolishment of morphology-based taxa and change to binomial species names: 2022 taxonomy update of the ICTV bacterial viruses subcommittee. Arch. Virol. 168:74
    [Google Scholar]
  98. 98.
    Van Espen L, Bak EG, Beller L, Close L, Deboutte W et al. 2021. A previously undescribed highly prevalent phage identified in a Danish enteric virome catalog. mSystems 6:e0038221
    [Google Scholar]
  99. 99.
    Wagner J, Maksimovic J, Farries G, Sim WH, Bishop RF et al. 2013. Bacteriophages in gut samples from pediatric Crohn's disease patients: metagenomic analysis using 454 pyrosequencing. Inflamm. Bowel Dis. 19:1598–608
    [Google Scholar]
  100. 100.
    Yang K, Niu J, Zuo T, Sun Y, Xu Z et al. 2021. Alterations in the gut virome in obesity and type 2 diabetes mellitus. Gastroenterology 161:1257–69.e13
    [Google Scholar]
  101. 101.
    Yutin N, Benler S, Shmakov SA, Wolf YI, Tolstoy I et al. 2021. Analysis of metagenome-assembled viral genomes from the human gut reveals diverse putative CrAss-like phages with unique genomic features. Nat. Commun. 12:1044
    [Google Scholar]
  102. 102.
    Yutin N, Makarova KS, Gussow AB, Krupovic M, Segall A et al. 2018. Discovery of an expansive bacteriophage family that includes the most abundant viruses from the human gut. Nat. Microbiol. 3:38–46
    [Google Scholar]
  103. 103.
    Zhao M, Feng R, Ben-Horin S, Zhuang X, Tian Z et al. 2022. Systematic review with meta-analysis: environmental and dietary differences of inflammatory bowel disease in Eastern and Western populations. Aliment. Pharmacol. Ther. 55:266–76
    [Google Scholar]
  104. 104.
    Zuo T, Liu Q, Zhang F, Yeoh YK, Wan Y et al. 2021. Temporal landscape of human gut RNA and DNA virome in SARS-CoV-2 infection and severity. Microbiome 9:91
    [Google Scholar]
  105. 105.
    Zuo T, Lu XJ, Zhang Y, Cheung CP, Lam S et al. 2019. Gut mucosal virome alterations in ulcerative colitis. Gut 68:1169–79
    [Google Scholar]
  106. 106.
    Zuo T, Sun Y, Wan Y, Yeoh YK, Zhang F et al. 2020. Human-gut-DNA virome variations across geography, ethnicity, and urbanization. Cell Host Microbe 28:741–51.e4
    [Google Scholar]
  107. 107.
    Zuo W, Michail S, Sun F. 2022. Metagenomic analyses of multiple gut datasets revealed the association of phage signatures in colorectal cancer. Front. Cell Infect. Microbiol. 12:918010
    [Google Scholar]
/content/journals/10.1146/annurev-micro-032421-105754
Loading
/content/journals/10.1146/annurev-micro-032421-105754
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error