1932

Abstract

High-throughput sequencing technologies have revolutionized how we think about viruses. Investigators can now go beyond pathogenic viruses and have access to the thousands of viruses that inhabit our bodies without causing clinical symptoms. By studying their interactions with each other, with other microbes, and with host genetics and immune systems, we can learn how they affect health and disease. This article reviews current knowledge of the composition and diversity of the human virome in physiologically healthy individuals. It focuses on recent results from metagenomics studies and discusses the contribution of bacteriophages and eukaryotic viruses to human health.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-micro-102215-095431
2016-09-08
2024-10-14
Loading full text...

Full text loading...

/deliver/fulltext/micro/70/1/annurev-micro-102215-095431.html?itemId=/content/journals/10.1146/annurev-micro-102215-095431&mimeType=html&fmt=ahah

Literature Cited

  1. Abeles SR, Ly M, Santiago-Rodriguez TM, Pride DT. 1.  2015. Effects of long term antibiotic therapy on human oral and fecal viromes. PLOS ONE 10:e0134941 [Google Scholar]
  2. Abeles SR, Pride DT. 2.  2014. Molecular bases and role of viruses in the human microbiome. J. Mol. Biol. 426:3892–906 [Google Scholar]
  3. Abeles SR, Robles-Sikisaka R, Ly M, Lum AG, Salzman J. 3.  et al. 2014. Human oral viruses are personal, persistent and gender-consistent. ISME J. 8:1753–67 [Google Scholar]
  4. Antonsson A, Erfurt C, Hazard K, Holmgren V, Simon M. 4.  et al. 2003. Prevalence and type spectrum of human papillomaviruses in healthy skin samples collected in three continents. J. Gen. Virol. 84:1881–86 [Google Scholar]
  5. Arvin A, Campadelli-Fiume G, Mocarski E, Moore PS, Roizman B. 5.  et al. 2007. Human Herpesviruses: Biology, Therapy, and Immunoprophylaxis Cambridge, UK: Cambridge Univ. Press [Google Scholar]
  6. Barfoot R, Denham S, Gyure LA, Hall JG, Hobbs SM. 6.  et al. 1989. Some properties of dendritic macrophages from peripheral lymph. Immunology 68:233–39 [Google Scholar]
  7. Barr JJ, Auro R, Furlan M, Whiteson KL, Erb ML. 7.  et al. 2013. Bacteriophage adhering to mucus provide a non–host-derived immunity. PNAS 110:10771–76 [Google Scholar]
  8. Barr JJ, Auro R, Sam-Soon N, Kassegne S, Peters G. 8.  et al. 2015. Subdiffusive motion of bacteriophage in mucosal surfaces increases the frequency of bacterial encounters. PNAS 112:13675–80 [Google Scholar]
  9. Barton ES, White DW, Cathelyn JS, Brett-McClellan KA, Engle M. 9.  et al. 2007. Herpesvirus latency confers symbiotic protection from bacterial infection. Nature 447:326–29 [Google Scholar]
  10. Beijerinck MW. 10.  1898. Concerning a contagium vivum fluidum as cause of the spot disease of tobacco leaves. See 57. 33–52
  11. Bernardin F, Operskalski E, Busch M, Delwart E. 11.  2010. Transfusion transmission of highly prevalent commensal human viruses. Transfusion 50:2474–83 [Google Scholar]
  12. Bhattarai N, Stapleton JT. 12.  2012. GB virus C: The good boy virus?. Trends Microbiol. 20:124–30 [Google Scholar]
  13. Bock M, Stoye JP. 13.  2000. Endogenous retroviruses and the human germline. Curr. Opin. Genet. Dev. 10:651–55 [Google Scholar]
  14. Boller K, Schonfeld K, Lischer S, Fischer N, Hoffmann A. 14.  et al. 2008. Human endogenous retrovirus HERV-K113 is capable of producing intact viral particles. J. Gen. Virol. 89:567–72 [Google Scholar]
  15. Breitbart M, Haynes M, Kelley S, Angly F, Edwards RA. 15.  et al. 2008. Viral diversity and dynamics in an infant gut. Res. Microbiol. 159:367–73 [Google Scholar]
  16. Breitbart M, Hewson I, Felts B, Mahaffy JM, Nulton J. 16.  et al. 2003. Metagenomic analyses of an uncultured viral community from human feces. J. Bacteriol. 185:6220–23 [Google Scholar]
  17. Breitbart M, Rohwer F. 17.  2005. Method for discovering novel DNA viruses in blood using viral particle selection and shotgun sequencing. Biotechniques 39:729–36 [Google Scholar]
  18. Cadwell K. 18.  2015. The virome in host health and disease. Immunity 42:805–13 [Google Scholar]
  19. Canuti M, Deijs M, Jazaeri Farsani SM, Holwerda M, Jebbink MF. 19.  et al. 2014. Metagenomic analysis of a sample from a patient with respiratory tract infection reveals the presence of a gamma-papillomavirus. Front. Microbiol. 5:347 [Google Scholar]
  20. Chamberland C. 20.  1884. Sur un filtre donnant de l'eau physiologiquement pure. C. R. Acad. Sci. Paris 99:247–48 [Google Scholar]
  21. Clemente JC, Ursell LK, Parfrey LW, Knight R. 21.  2012. The impact of the gut microbiota on human health: an integrative view. Cell 148:1258–70 [Google Scholar]
  22. Colson P, Fancello L, Gimenez G, Armougom F, Desnues C. 22.  et al. 2013. Evidence of the megavirome in humans. J. Clin. Virol. 57:191–200 [Google Scholar]
  23. Cortez MH, Weitz JS. 23.  2014. Coevolution can reverse predator-prey cycles. PNAS 111:7486–91 [Google Scholar]
  24. d'Hérelle F. 24.  1917. Sur un microbe invisible antagoniste des bacilles dysentriques. Compt. Rend. Acad. Sci. 165:373 [Google Scholar]
  25. David LA, Weil A, Ryan ET, Calderwood SB, Harris JB. 25.  et al. 2015. Gut microbial succession follows acute secretory diarrhea in humans. mBio 6:e00381–15 [Google Scholar]
  26. De Paepe M, Leclerc M, Tinsley CR, Petit MA. 26.  2014. Bacteriophages: an underestimated role in human and animal health?. Front. Cell Infect. Microbiol. 4:39 [Google Scholar]
  27. de Villiers EM. 27.  2013. Cross-roads in the classification of papillomaviruses. Virology 445:2–10 [Google Scholar]
  28. De Vlaminck I, Khush KK, Strehl C, Kohli B, Luikart H. 28.  et al. 2013. Temporal response of the human virome to immunosuppression and antiviral therapy. Cell 155:1178–87 [Google Scholar]
  29. Deng X, Terunuma H, Handema R, Sakamoto M, Kitamura T. 29.  et al. 2000. Higher prevalence and viral load of TT virus in saliva than in the corresponding serum: another possible transmission route and replication site of TT virus. J. Med. Virol. 62:531–37 [Google Scholar]
  30. Dewannieux M, Blaise S, Heidmann T. 30.  2005. Identification of a functional envelope protein from the HERV-K family of human endogenous retroviruses. J. Virol. 79:15573–77 [Google Scholar]
  31. Dickson RP, Erb-Downward JR, Martinez FJ, Huffnagle GB. 31.  2016. The microbiome and the respiratory tract. Annu. Rev. Physiol. 78:481–504 [Google Scholar]
  32. Dinakaran V, Rathinavel A, Pushpanathan M, Sivakumar R, Gunasekaran P, Rajendhran J. 32.  2014. Elevated levels of circulating DNA in cardiovascular disease patients: Metagenomic profiling of microbiome in the circulation. PLOS ONE 9:e105221 [Google Scholar]
  33. Duerkop BA, Hooper LV. 33.  2013. Resident viruses and their interactions with the immune system. Nat. Immunol. 14:654–59 [Google Scholar]
  34. Duhaime MB, Deng L, Poulos BT, Sullivan MB. 34.  2012. Towards quantitative metagenomics of wild viruses and other ultra-low concentration DNA samples: a rigorous assessment and optimization of the linker amplification method. Environ. Microbiol. 14:2526–37 [Google Scholar]
  35. Dutilh BE, Cassman N, McNair K, Sanchez SE, Silva GG. 35.  et al. 2014. A highly abundant bacteriophage discovered in the unknown sequences of human faecal metagenomes. Nat. Commun. 5:4498 [Google Scholar]
  36. Fancello L, Desnues C, Raoult D, Rolain JM. 36.  2011. Bacteriophages and diffusion of genes encoding antimicrobial resistance in cystic fibrosis sputum microbiota. J. Antimicrob. Chemother. 66:2448–54 [Google Scholar]
  37. Feng H, Shuda M, Chang Y, Moore PS. 37.  2008. Clonal integration of a polyomavirus in human Merkel cell carcinoma. Science 319:1096–100 [Google Scholar]
  38. Flint SJ, Enquist LW, Racaniello VR, Skalka AM. 38.  2009. Principles of Virology Washington, DC: ASM Press [Google Scholar]
  39. Foca A, Liberto MC, Quirino A, Marascio N, Zicca E, Pavia G. 39.  2015. Gut inflammation and immunity: What is the role of the human gut virome?. Mediat. Inflamm. 2015:326032 [Google Scholar]
  40. Foulongne V, Sauvage V, Hebert C, Dereure O, Cheval J. 40.  et al. 2012. Human skin microbiota: high diversity of DNA viruses identified on the human skin by high throughput sequencing. PLOS ONE 7:e38499 [Google Scholar]
  41. Furuta RA, Sakamoto H, Kuroishi A, Yasiui K, Matsukura H, Hirayama F. 41.  2015. Metagenomic profiling of the viromes of plasma collected from blood donors with elevated serum alanine aminotransferase levels. Transfusion 55:1889–99 [Google Scholar]
  42. Gallian P, Biagini P, Zhong S, Touinssi M, Yeo W. 42.  et al. 2000. TT virus: a study of molecular epidemiology and transmission of genotypes 1, 2 and 3. J. Clin. Virol. 17:43–49 [Google Scholar]
  43. Gardner SD, Field AM, Coleman DV, Hulme B. 43.  1971. New human papovavirus (B.K.) isolated from urine after renal transplantation. Lancet 1:1253–57 [Google Scholar]
  44. Goldsmith CS, Miller SE. 44.  2009. Modern uses of electron microscopy for detection of viruses. Clin. Microbiol. Rev. 22:552–63 [Google Scholar]
  45. Gorski A, Kniotek M, Perkowska-Ptasinska A, Mroz A, Przerwa A. 45.  et al. 2006. Bacteriophages and transplantation tolerance. Transplant. Proc. 38:331–33 [Google Scholar]
  46. Gorski A, Miedzybrodzki R, Borysowski J, Dabrowska K, Wierzbicki P. 46.  et al. 2012. Phage as a modulator of immune responses: Practical implications for phage therapy. Adv. Virus Res. 83:41–71 [Google Scholar]
  47. Gorski A, Wazna E, Dabrowska BW, Dabrowska K, Switala-Jelen K, Miedzybrodzki R. 47.  2006. Bacteriophage translocation. FEMS Immunol. Med. Microbiol. 46:313–19 [Google Scholar]
  48. Goto K, Sugiyama K, Ando T, Mizutani F, Terabe K. 48.  et al. 2000. Detection rates of TT virus DNA in serum of umbilical cord blood, breast milk and saliva. Tohoku J. Exp. Med. 191:203–7 [Google Scholar]
  49. Halary S, Temmam S, Desnues C. 49.  2016. Viral metagenomics: Are we missing the giants?. Current Opin. Microbiol. 31:34–43 [Google Scholar]
  50. Handelsman J, Rondon MR, Brady SF, Clardy J, Goodman RM. 50.  1998. Molecular biological access to the chemistry of unknown soil microbes: a new frontier for natural products. Chem. Biol. 5:R245–49 [Google Scholar]
  51. Hannigan GD, Meisel JS, Tyldsley AS, Zheng Q, Hodkinson BP. 51.  et al. 2015. The human skin double-stranded DNA virome: topographical and temporal diversity, genetic enrichment, and dynamic associations with the host microbiome. mBio 6:e01578–15 [Google Scholar]
  52. Haynes M, Rohwer F. 52.  2011. The human virome. Metagenomics of the Human Body KE Nelson 63–77 New York: Springer [Google Scholar]
  53. Hill DA, Hoffmann C, Abt MC, Du Y, Kobuley D. 53.  et al. 2010. Metagenomic analyses reveal antibiotic-induced temporal and spatial changes in intestinal microbiota with associated alterations in immune cell homeostasis. Mucosal Immunol. 3:148–58 [Google Scholar]
  54. 54. Hum. Microbiome Proj. Consort. 2012. Structure, function and diversity of the healthy human microbiome. Nature 486:207–14 [Google Scholar]
  55. Inami T, Konomi N, Arakawa Y, Abe K. 55.  2000. High prevalence of TT virus DNA in human saliva and semen. J. Clin. Microbiol. 38:2407–8 [Google Scholar]
  56. Ivanovski D. 56.  1892. Concerning the mosaic disease of tobacco plant. See 57. 27–30
  57. Johnson J. 57.  1942. Phytopathological Classics. Saint Paul, MN: Am. Phytopathol. Soc. (from German) [Google Scholar]
  58. Kapusinszky B, Minor P, Delwart E. 58.  2012. Nearly constant shedding of diverse enteric viruses by two healthy infants. J. Clin. Microbiol. 50:3427–34 [Google Scholar]
  59. Kilic AO, Pavlova SI, Alpay S, Kilic SS, Tao L. 59.  2001. Comparative study of vaginal Lactobacillus phages isolated from women in the United States and Turkey: prevalence, morphology, host range, and DNA homology. Clin. Diagn. Lab. Immunol. 8:31–39 [Google Scholar]
  60. Kim K-H, Bae J-W. 60.  2011. Amplification methods bias metagenomic libraries of uncultured single-stranded and double-stranded DNA viruses. Appl. Environ. Microbiol. 77:7663–68 [Google Scholar]
  61. Kim K-H, Chang HW, Nam YD, Roh SW, Kim MS. 61.  et al. 2008. Amplification of uncultured single-stranded DNA viruses from rice paddy soil. Appl. Environ. Microbiol. 74:5975–85 [Google Scholar]
  62. Kim MS, Park EJ, Roh SW, Bae JW. 62.  2011. Diversity and abundance of single-stranded DNA viruses in human feces. Appl. Environ. Microbiol. 77:8062–70 [Google Scholar]
  63. King AMQ, Adams MJ, Carstens EB, Lefkowitz EJ. 63.  2011. Virus Taxonomy: Ninth Report of the International Committee on Taxonomy of Viruses London: Elsevier [Google Scholar]
  64. Law J, Jovel J, Patterson J, Ford G, O'Keefe S. 64.  et al. 2013. Identification of hepatotropic viruses from plasma using deep sequencing: a next generation diagnostic tool. PLOS ONE 8:e60595 [Google Scholar]
  65. Lecuit M, Eloit M. 65.  2013. The human virome: new tools and concepts. Trends Microbiol. 21:510–15 [Google Scholar]
  66. Lee SM, Donaldson GP, Mikulski Z, Boyajian S, Ley K, Mazmanian SK. 66.  2013. Bacterial colonization factors control specificity and stability of the gut microbiota. Nature 501:426–29 [Google Scholar]
  67. Li L, Deng X, Linsuwanon P, Bangsberg D, Bwana MB. 67.  et al. 2013. AIDS alters the commensal plasma virome. J. Virol. 87:10912–15 [Google Scholar]
  68. Li SK, Leung RK, Guo HX, Wei JF, Wang JH. 68.  et al. 2012. Detection and identification of plasma bacterial and viral elements in HIV/AIDS patients in comparison to healthy adults. Clin. Microbiol. Infect. 18:1126–33 [Google Scholar]
  69. Lim ES, Zhou Y, Zhao G, Bauer IK, Droit L. 69.  et al. 2015. Early life dynamics of the human gut virome and bacterial microbiome in infants. Nat. Med. 21:1228–34 [Google Scholar]
  70. Liu J, Yan R, Zhong Q, Ngo S, Bangayan NJ. 70.  et al. 2015. The diversity and host interactions of Propionibacterium acnes bacteriophages on human skin. ISME J. 9:2078–93 [Google Scholar]
  71. Loeffler F, Frosch P. 71.  1898. Report of the Commission for Research on foot-and-mouth disease. Zent. Bakte. Parasitenkd. Infekt. Hyg. 23:371–91 [Google Scholar]
  72. Looft T, Allen HK, Cantarel BL, Levine UY, Bayles DO. 72.  et al. 2014. Bacteria, phages and pigs: the effects of in-feed antibiotics on the microbiome at different gut locations. ISME J. 8:1566–76 [Google Scholar]
  73. Lum AG, Ly M, Santiago-Rodriguez TM, Naidu M, Boehm TK, Pride DT. 73.  2015. Global transcription of CRISPR loci in the human oral cavity. BMC Genomics 16:401 [Google Scholar]
  74. Ly M, Abeles SR, Boehm TK, Robles-Sikisaka R, Naidu M. 74.  et al. 2014. Altered oral viral ecology in association with periodontal disease. mBio 5:e01133–14 [Google Scholar]
  75. Ma Y, Madupu R, Karaoz U, Nossa CW, Yang L. 75.  et al. 2014. Human papillomavirus community in healthy persons, defined by metagenomics analysis of human microbiome project shotgun sequencing data sets. J. Virol. 88:4786–97 [Google Scholar]
  76. Mayer A. 76.  1886. Concerning the mosaic disease of tobacco. See 57. 11–24
  77. Mc Grath S, van Sinderen D. 77.  2007. Bacteriophage: Genetics and Molecular Biology Norfolk, UK: Caister Acad. [Google Scholar]
  78. McLaughlin-Drubin ME, Munger K. 78.  2008. Viruses associated with human cancer. Biochim. Biophys. Acta 1782:127–50 [Google Scholar]
  79. Meessen-Pinard M, Sekulovic O, Fortier LC. 79.  2012. Evidence of in vivo prophage induction during Clostridium difficile infection. Appl. Environ. Microbiol. 78:7662–70 [Google Scholar]
  80. Minot S, Bryson A, Chehoud C, Wu GD, Lewis JD, Bushman FD. 80.  2013. Rapid evolution of the human gut virome. PNAS 110:12450–55 [Google Scholar]
  81. Minot S, Sinha R, Chen J, Li H, Keilbaugh SA. 81.  et al. 2011. The human gut virome: inter-individual variation and dynamic response to diet. Genome Res. 21:1616–25 [Google Scholar]
  82. Modi SR, Lee HH, Spina CS, Collins JJ. 82.  2013. Antibiotic treatment expands the resistance reservoir and ecological network of the phage metagenome. Nature 499:219–22 [Google Scholar]
  83. Norman JM, Handley SA, Baldridge MT, Droit L, Liu CY. 83.  et al. 2015. Disease-specific alterations in the enteric virome in inflammatory bowel disease. Cell 160:447–60 [Google Scholar]
  84. Oh J, Byrd AL, Deming C, Conlan S, Program NCS. 84.  et al. 2014. Biogeography and individuality shape function in the human skin metagenome. Nature 514:59–64 [Google Scholar]
  85. Padgett BL, Walker DL, ZuRhein GM, Eckroade RJ, Dessel BH. 85.  1971. Cultivation of papova-like virus from human brain with progressive multifocal leucoencephalopathy. Lancet 1:1257–60 [Google Scholar]
  86. Pavlova SI, Tao L. 86.  2000. Induction of vaginal Lactobacillus phages by the cigarette smoke chemical benzo[a]pyrene diol epoxide. Mutat. Res. 466:57–62 [Google Scholar]
  87. Popgeorgiev N, Boyer M, Fancello L, Monteil S, Robert C. 87.  et al. 2013. Marseillevirus-like virus recovered from blood donated by asymptomatic humans. J. Infect. Dis. 208:1042–50 [Google Scholar]
  88. Popgeorgiev N, Temmam S, Raoult D, Desnues C. 88.  2013. Describing the silent human virome with an emphasis on giant viruses. Intervirology 56:395–412 [Google Scholar]
  89. Pride DT, Salzman J, Haynes M, Rohwer F, Davis-Long C. 89.  et al. 2012. Evidence of a robust resident bacteriophage population revealed through analysis of the human salivary virome. ISME J. 6:915–26 [Google Scholar]
  90. Rascovan N, Monteil Bouchard S, Grob JJ, Collet-Villette AM, Gaudy-Marqueste C. 90.  et al. 2016. Human polyomavirus-6 infecting lymph nodes of a patient with an angiolymphoid hyperplasia with eosinophilia or Kimura disease. Clin. Infect. Dis. 62:1419–21 [Google Scholar]
  91. Reed W, Carroll J, Agramonte A. 91.  2001. The etiology of yellow fever: an additional note; 1901. Mil. Med. 166:44–53 [Google Scholar]
  92. Reyes A, Blanton LV, Cao S, Zhao G, Manary M. 92.  et al. 2015. Gut DNA viromes of Malawian twins discordant for severe acute malnutrition. PNAS 112:11941–46 [Google Scholar]
  93. Reyes A, Haynes M, Hanson N, Angly FE, Heath AC. 93.  et al. 2010. Viruses in the faecal microbiota of monozygotic twins and their mothers. Nature 466:334–38 [Google Scholar]
  94. Reyes A, Wu M, McNulty NP, Rohwer FL, Gordon JI. 94.  2013. Gnotobiotic mouse model of phage-bacterial host dynamics in the human gut. PNAS 110:20236–41 [Google Scholar]
  95. Robles-Sikisaka R, Ly M, Boehm T, Naidu M, Salzman J, Pride DT. 95.  2013. Association between living environment and human oral viral ecology. ISME J. 7:1710–24 [Google Scholar]
  96. Roingeard P. 96.  2008. Viral detection by electron microscopy: past, present and future. Biol. Cell 100:491–501 [Google Scholar]
  97. Rosenberg R, Johansson MA, Powers AM, Miller BR. 97.  2013. Search strategy has influenced the discovery rate of human viruses. PNAS 110:13961–64 [Google Scholar]
  98. Santiago-Rodriguez TM, Ly M, Bonilla N, Pride DT. 98.  2015. The human urine virome in association with urinary tract infections. Front. Microbiol. 6:14 [Google Scholar]
  99. Schowalter RM, Pastrana DV, Pumphrey KA, Moyer AL, Buck CB. 99.  2010. Merkel cell polyomavirus and two previously unknown polyomaviruses are chronically shed from human skin. Cell Host Microbe 7:509–15 [Google Scholar]
  100. Sharon I, Morowitz MJ, Thomas BC, Costello EK, Relman DA, Banfield JF. 100.  2013. Time series community genomics analysis reveals rapid shifts in bacterial species, strains, and phage during infant gut colonization. Genome Res. 23:111–20 [Google Scholar]
  101. Stern A, Mick E, Tirosh I, Sagy O, Sorek R. 101.  2012. CRISPR targeting reveals a reservoir of common phages associated with the human gut microbiome. Genome Res. 22:1985–94 [Google Scholar]
  102. Stremlau MH, Andersen KG, Folarin OA, Grove JN, Odia I. 102.  et al. 2015. Discovery of novel rhabdoviruses in the blood of healthy individuals from West Africa. PLOS Negl. Trop. Dis. 9:e0003631 [Google Scholar]
  103. Subramanian RP, Wildschutte JH, Russo C, Coffin JM. 103.  2011. Identification, characterization, and comparative genomic distribution of the HERV-K (HML-2) group of human endogenous retroviruses. Retrovirology 8:90 [Google Scholar]
  104. Temmam S, Monteil-Bouchard S, Robert C, Pascalis H, Michelle C. 104.  et al. 2015. Host-associated metagenomics: a guide to generating infectious RNA viromes. PLOS ONE 10:e0139810 [Google Scholar]
  105. Thurber RV, Haynes M, Breitbart M, Wegley L, Rohwer F. 105.  2009. Laboratory procedures to generate viral metagenomes. Nat. Protoc. 4:470–83 [Google Scholar]
  106. Twort FW. 106.  1915. An investigation on the nature of the ultramicroscopic viruses. Lancet 2:1241–43 [Google Scholar]
  107. van der Meijden E, Janssens RW, Lauber C, Bouwes Bavinck JN, Gorbalenya AE, Feltkamp MC. 107.  2010. Discovery of a new human polyomavirus associated with trichodysplasia spinulosa in an immunocompromized patient. PLOS Pathog. 6:e1001024 [Google Scholar]
  108. Virgin HW. 108.  2014. The virome in mammalian physiology and disease. Cell 157:142–50 [Google Scholar]
  109. Virgin HW, Wherry EJ, Ahmed R. 109.  2009. Redefining chronic viral infection. Cell 138:30–50 [Google Scholar]
  110. Waller AS, Yamada T, Kristensen DM, Kultima JR, Sunagawa S. 110.  et al. 2014. Classification and quantification of bacteriophage taxa in human gut metagenomes. ISME J. 8:1391–402 [Google Scholar]
  111. Wang J, Gao Y, Zhao F. 111.  2015. Phage-bacteria interaction network in human oral microbiome. Environ. Microbiol. In press [Google Scholar]
  112. Wang W, Jovel J, Halloran B, Wine E, Patterson J. 112.  et al. 2015. Metagenomic analysis of microbiome in colon tissue from subjects with inflammatory bowel diseases reveals interplay of viruses and bacteria. Inflamm. Bowel Dis. 21:1419–27 [Google Scholar]
  113. Willner D, Furlan M, Haynes M, Schmieder R, Angly FE. 113.  et al. 2009. Metagenomic analysis of respiratory tract DNA viral communities in cystic fibrosis and non-cystic fibrosis individuals. PLOS ONE 4:e7370 [Google Scholar]
  114. Willner D, Furlan M, Schmieder R, Grasis JA, Pride DT. 114.  et al. 2011. Metagenomic detection of phage-encoded platelet-binding factors in the human oral cavity. PNAS 108:Suppl. 14547–53 [Google Scholar]
  115. Woolhouse ME, Howey R, Gaunt E, Reilly L, Chase-Topping M, Savill N. 115.  2008. Temporal trends in the discovery of human viruses. Proc. Biol. Sci. 275:2111–15 [Google Scholar]
  116. Wylie KM, Mihindukulasuriya KA, Zhou Y, Sodergren E, Storch GA, Weinstock GM. 116.  2014. Metagenomic analysis of double-stranded DNA viruses in healthy adults. BMC Biol. 12:71 [Google Scholar]
  117. Wylie KM, Weinstock GM, Storch GA. 117.  2012. Emerging view of the human virome. Transl. Res. 160:283–90 [Google Scholar]
  118. Young JC, Chehoud C, Bittinger K, Bailey A, Diamond JM. 118.  et al. 2015. Viral metagenomics reveal blooms of anelloviruses in the respiratory tract of lung transplant recipients. Am. J. Transplant. 15:200–9 [Google Scholar]
  119. Zhang T, Breitbart M, Lee WH, Run JQ, Wei CL. 119.  et al. 2006. RNA viral community in human feces: prevalence of plant pathogenic viruses. PLOS Biol. 4:e3 [Google Scholar]
  120. Zhang X, McDaniel AD, Wolf LE, Keusch GT, Waldor MK, Acheson DW. 120.  2000. Quinolone antibiotics induce Shiga toxin-encoding bacteriophages, toxin production, and death in mice. J. Infect. Dis. 181:664–70 [Google Scholar]
  121. Zhang Z, Geng J, Tang X, Fan H, Xu J. 121.  et al. 2014. Spatial heterogeneity and co-occurrence patterns of human mucosal-associated intestinal microbiota. ISME J. 8:881–93 [Google Scholar]
  122. Zhou Y, Gao H, Mihindukulasuriya KA, La Rosa PS, Wylie KM. 122.  et al. 2013. Biogeography of the ecosystems of the healthy human body. Genome Biol. 14:R1 [Google Scholar]
  123. Zoetendal EG, Raes J, van den Bogert B, Arumugam M, Booijink CC. 123.  et al. 2012. The human small intestinal microbiota is driven by rapid uptake and conversion of simple carbohydrates. ISME J. 6:1415–26 [Google Scholar]
/content/journals/10.1146/annurev-micro-102215-095431
Loading
/content/journals/10.1146/annurev-micro-102215-095431
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