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Breck A Duerkop & Lora V Hooper AffiliationsCorresponding author Nature Immunology 14, 654–659 (2013) doi:10.1038/ni.2614 Received 18 February 2013 Accepted 16 April 2013 Published online 18 June 2013 The human body is colonized with a diverse resident microflora that includes viruses. Recent studies of metagenomes have begun to characterize the composition of the human 'virobiota' and its associated genes (the 'virome'), and have fostered the emerging field of host-virobiota interactions. In this Perspective, we explore how resident viruses interact with the immune system. We review recent findings that highlight the role of the immune system in shaping the composition of the virobiota and consider how resident viruses may impact host immunity. Finally, we discuss the implications of virobiota–immune system interactions for human health. Hooper, L.V., Littman, D.R. & Macpherson, A.J. Interactions between the microbiota and the immune system. Science 336, 1268–1273 (2012). CASADSPubMedArticle 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, 220–230 (2012). CASADSPubMedArticle White, D.W., Suzanne Beard, R. & Barton, E.S. Immune modulation during latent herpesvirus infection. Immunol. Rev. 245, 189–208 (2012). CASPubMedArticle Handley, S.A. et al. Pathogenic simian immunodeficiency virus infection is associated with expansion of the enteric virome. Cell 151, 253–266 (2012). CASPubMedArticle Reyes, A. et al. Viruses in the faecal microbiota of monozygotic twins and their mothers. Nature 466, 334–338 (2010). CASADSISIPubMedArticle Minot, S. et al. The human gut virome: inter-individual variation and dynamic response to diet. Genome Res. 21, 1616–1625 (2011). CASADSPubMedArticle Foulongne, V. et al. Human skin microbiota: high diversity of DNA viruses identified on the human skin by high throughput sequencing. PLoS ONE 7, e38499 (2012). CASADSPubMedArticle Zhang, T. et al. RNA viral community in human feces: prevalence of plant pathogenic viruses. PLoS Biol. 4, e3 (2006). CASPubMedArticle Turnbaugh, P.J. et al. A core gut microbiome in obese and lean twins. Nature 457, 480–484 (2009). CASADSISIPubMedArticle Pride, D.T. et al. Evidence of a robust resident bacteriophage population revealed through analysis of the human salivary virome. ISME J. 6, 915–926 (2012). CASPubMedArticle Breitbart, M. et al. Viral diversity and dynamics in an infant gut. Res. Microbiol. 159, 367–373 (2008). CASISIPubMedArticle Weinbauer, M.G. Ecology of prokaryotic viruses. FEMS Microbiol. Rev. 28, 127–181 (2004). CASISIPubMedArticle DeMarini, D.M. & Lawrence, B.K. Prophage induction by DNA topoisomerase II poisons and reactive-oxygen species: role of DNA breaks. Mutat. Res. 267, 1–17 (1992). CASPubMedArticle 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, 17621–17626 (2012). ADSPubMedArticle Kim, M.S., Park, E.J., Roh, S.W. & Bae, J.W. Diversity and abundance of single-stranded DNA viruses in human feces. Appl. Environ. Microbiol. 77, 8062–8070 (2011). CASPubMedArticle Canchaya, C., Fournous, G., Chibani-Chennoufi, S., Dillmann, M.L. & Brussow, H. Phage as agents of lateral gene transfer. Curr. Opin. Microbiol. 6, 417–424 (2003). CASISIPubMedArticle Pride, D.T., Salzman, J. & Relman, D.A. Comparisons of clustered regularly interspaced short palindromic repeats and viromes in human saliva reveal bacterial adaptations to salivary viruses. Environ. Microbiol. 14, 2564–2576 (2012). CASPubMedArticle Ivanov, I.I. et al. Specific microbiota direct the differentiation of IL-17-producing T-helper cells in the mucosa of the small intestine. Cell Host Microbe 4, 337–349 (2008). CASISIPubMedArticle Mazmanian, S.K., Liu, C.H., Tzianabos, A.O. & Kasper, D.L. An immunomodulatory molecule of symbiotic bacteria directs maturation of the host immune system. Cell 122, 107–118 (2005). CASISIPubMedArticle Kuss, S.K. et al. Intestinal microbiota promote enteric virus replication and systemic pathogenesis. Science 334, 249–252 (2011). CASADSPubMedArticle Ichinohe, T. et al. Microbiota regulates immune defense against respiratory tract influenza A virus infection. Proc. Natl. Acad. Sci. USA 108, 5354–5359 (2011). ADSPubMedArticle Kane, M. et al. Successful transmission of a retrovirus depends on the commensal microbiota. Science 334, 245–249 (2011). CASADSPubMedArticle Schowalter, R.M., Pastrana, D.V., Pumphrey, K.A., Moyer, A.L. & Buck, C.B. Merkel cell polyomavirus and two previously unknown polyomaviruses are chronically shed from human skin. Cell Host Microbe 7, 509–515 (2010). CASISIPubMedArticle Miller, C.S., Avdiushko, S.A., Kryscio, R.J., Danaher, R.J. & Jacob, R.J. Effect of prophylactic valacyclovir on the presence of human herpesvirus DNA in saliva of healthy individuals after dental treatment. J. Clin. Microbiol. 43, 2173–2180 (2005). CASPubMedArticle Lazarevic, V. et al. Analysis of the salivary microbiome using culture-independent techniques. J. Clin. Bioinforma. 2, 4 (2012). CASPubMedArticle Bogaert, D. et al. Variability and diversity of nasopharyngeal microbiota in children: a metagenomic analysis. PLoS ONE 6, e17035 (2011). CASADSPubMedArticle Nokso-Koivisto, J., Kinnari, T.J., Lindahl, P., Hovi, T. & Pitkaranta, A. Human picornavirus and coronavirus RNA in nasopharynx of children without concurrent respiratory symptoms. J. Med. Virol. 66, 417–420 (2002). PubMedArticle Minot, S., Grunberg, S., Wu, G.D., Lewis, J.D. & Bushman, F.D. Hypervariable loci in the human gut virome. Proc. Natl. Acad. Sci. USA 109, 3962–3966 (2012). CASADSPubMedArticle Victoria, J.G. et al. Metagenomic analyses of viruses in stool samples from children with acute flaccid paralysis. J. Virol. 83, 4642–4651 (2009). CASPubMedArticle Finkbeiner, S.R. et al. Metagenomic analysis of human diarrhea: viral detection and discovery. PLoS Pathog. 4, e1000011 (2008). CASPubMedArticle Lee, Y.K. & Mazmanian, S.K. Has the microbiota played a critical role in the evolution of the adaptive immune system? Science 330, 1768–1773 (2010). CASADSISIPubMedArticle McFall-Ngai, M. Adaptive immunity: care for the community. Nature 445, 153 (2007). CASADSISIPubMedArticle Vaishnava, S. et al. The antibacterial lectin RegIIIγ promotes the spatial segregation of microbiota and host in the intestine. Science 334, 255–258 (2011). CASADSPubMedArticle Salzman, N.H. et al. Enteric defensins are essential regulators of intestinal microbial ecology. Nat. Immunol. 11, 76–83 (2010). CASISIPubMedArticle Lysholm, F. et al. Characterization of the viral microbiome in patients with severe lower respiratory tract infections, using metagenomic sequencing. PLoS ONE 7, e30875 (2012). CASADSPubMedArticle Willner, D. et al. Metagenomic analysis of respiratory tract DNA viral communities in cystic fibrosis and non-cystic fibrosis individuals. PLoS ONE 4, e7370 (2009). CASADSPubMedArticle Brandl, K. et al. Vancomycin-resistant enterococci exploit antibiotic-induced innate immune deficits. Nature 455, 804–807 (2008). CASADSISIPubMedArticle Fukuda, S. et al. Bifidobacteria can protect from enteropathogenic infection through production of acetate. Nature 469, 543–547 (2011). CASADSISIPubMedArticle Virgin, H.W., Wherry, E.J. & Ahmed, R. Redefining chronic viral infection. Cell 138, 30–50 (2009). CASISIPubMedArticle Barton, E.S. et al. Herpesvirus latency confers symbiotic protection from bacterial infection. Nature 447, 326–329 (2007). CASADSISIPubMedArticle Zuniga, E.I., Liou, L.Y., Mack, L., Mendoza, M. & Oldstone, M.B. Persistent virus infection inhibits type I interferon production by plasmacytoid dendritic cells to facilitate opportunistic infections. Cell Host Microbe 4, 374–386 (2008). CASISIPubMedArticle Inchley, C.J. & Howard, J.G. The immunogenicity of phagocytosed T4 bacteriophage: cell replacement studies with splenectomized and irradiated mice. Clin. Exp. Immunol. 5, 189–198 (1969). CASPubMed Nelson, J., Ormrod, D.J., Wilson, D. & Miller, T.E. Host immune status in uraemia III. Humoral response to selected antigens in the rat. Clin. Exp. Immunol. 42, 234–240 (1980). CASPubMed Gorski, A. et al. Bacteriophages and transplantation tolerance. Transplant. Proc. 38, 331–333 (2006). CASPubMedArticle Eriksson, F. et al. Tumor-specific bacteriophages induce tumor destruction through activation of tumor-associated macrophages. J. Immunol. 182, 3105–3111 (2009). CASPubMedArticle Mori, K., Kubo, T., Kibayashi, Y., Ohkuma, T. & Kaji, A. Anti-vaccinia virus effect of M13 bacteriophage DNA. Antiviral Res. 31, 79–86 (1996). CASPubMedArticle Abstract• References• Author information Hooper, L.V., Littman, D.R. & Macpherson, A.J. Interactions between the microbiota and the immune system. Science 336, 1268–1273 (2012). CASADSPubMedArticle 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, 220–230 (2012). CASADSPubMedArticle White, D.W., Suzanne Beard, R. & Barton, E.S. Immune modulation during latent herpesvirus infection. Immunol. Rev. 245, 189–208 (2012). CASPubMedArticle Handley, S.A. et al. Pathogenic simian immunodeficiency virus infection is associated with expansion of the enteric virome. Cell 151, 253–266 (2012). CASPubMedArticle Reyes, A. et al. Viruses in the faecal microbiota of monozygotic twins and their mothers. Nature 466, 334–338 (2010). CASADSISIPubMedArticle Minot, S. et al. The human gut virome: inter-individual variation and dynamic response to diet. Genome Res. 21, 1616–1625 (2011). CASADSPubMedArticle Foulongne, V. et al. Human skin microbiota: high diversity of DNA viruses identified on the human skin by high throughput sequencing. PLoS ONE 7, e38499 (2012). CASADSPubMedArticle Zhang, T. et al. RNA viral community in human feces: prevalence of plant pathogenic viruses. PLoS Biol. 4, e3 (2006). CASPubMedArticle Turnbaugh, P.J. et al. A core gut microbiome in obese and lean twins. Nature 457, 480–484 (2009). CASADSISIPubMedArticle Pride, D.T. et al. Evidence of a robust resident bacteriophage population revealed through analysis of the human salivary virome. ISME J. 6, 915–926 (2012). CASPubMedArticle Breitbart, M. et al. Viral diversity and dynamics in an infant gut. Res. Microbiol. 159, 367–373 (2008). CASISIPubMedArticle Weinbauer, M.G. Ecology of prokaryotic viruses. FEMS Microbiol. Rev. 28, 127–181 (2004). CASISIPubMedArticle DeMarini, D.M. & Lawrence, B.K. Prophage induction by DNA topoisomerase II poisons and reactive-oxygen species: role of DNA breaks. Mutat. Res. 267, 1–17 (1992). CASPubMedArticle 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, 17621–17626 (2012). ADSPubMedArticle Kim, M.S., Park, E.J., Roh, S.W. & Bae, J.W. Diversity and abundance of single-stranded DNA viruses in human feces. Appl. Environ. Microbiol. 77, 8062–8070 (2011). CASPubMedArticle Canchaya, C., Fournous, G., Chibani-Chennoufi, S., Dillmann, M.L. & Brussow, H. Phage as agents of lateral gene transfer. Curr. Opin. Microbiol. 6, 417–424 (2003). CASISIPubMedArticle Pride, D.T., Salzman, J. & Relman, D.A. Comparisons of clustered regularly interspaced short palindromic repeats and viromes in human saliva reveal bacterial adaptations to salivary viruses. Environ. Microbiol. 14, 2564–2576 (2012). CASPubMedArticle Ivanov, I.I. et al. Specific microbiota direct the differentiation of IL-17-producing T-helper cells in the mucosa of the small intestine. Cell Host Microbe 4, 337–349 (2008). CASISIPubMedArticle Mazmanian, S.K., Liu, C.H., Tzianabos, A.O. & Kasper, D.L. An immunomodulatory molecule of symbiotic bacteria directs maturation of the host immune system. Cell 122, 107–118 (2005). CASISIPubMedArticle Kuss, S.K. et al. Intestinal microbiota promote enteric virus replication and systemic pathogenesis. Science 334, 249–252 (2011). CASADSPubMedArticle Ichinohe, T. et al. Microbiota regulates immune defense against respiratory tract influenza A virus infection. Proc. Natl. Acad. Sci. USA 108, 5354–5359 (2011). ADSPubMedArticle Kane, M. et al. Successful transmission of a retrovirus depends on the commensal microbiota. Science 334, 245–249 (2011). CASADSPubMedArticle Schowalter, R.M., Pastrana, D.V., Pumphrey, K.A., Moyer, A.L. & Buck, C.B. Merkel cell polyomavirus and two previously unknown polyomaviruses are chronically shed from human skin. Cell Host Microbe 7, 509–515 (2010). CASISIPubMedArticle Miller, C.S., Avdiushko, S.A., Kryscio, R.J., Danaher, R.J. & Jacob, R.J. Effect of prophylactic valacyclovir on the presence of human herpesvirus DNA in saliva of healthy individuals after dental treatment. J. Clin. Microbiol. 43, 2173–2180 (2005). CASPubMedArticle Lazarevic, V. et al. Analysis of the salivary microbiome using culture-independent techniques. J. Clin. Bioinforma. 2, 4 (2012). CASPubMedArticle Bogaert, D. et al. Variability and diversity of nasopharyngeal microbiota in children: a metagenomic analysis. PLoS ONE 6, e17035 (2011). CASADSPubMedArticle Nokso-Koivisto, J., Kinnari, T.J., Lindahl, P., Hovi, T. & Pitkaranta, A. Human picornavirus and coronavirus RNA in nasopharynx of children without concurrent respiratory symptoms. J. Med. Virol. 66, 417–420 (2002). 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Enteric defensins are essential regulators of intestinal microbial ecology. Nat. Immunol. 11, 76–83 (2010). CASISIPubMedArticle Lysholm, F. et al. Characterization of the viral microbiome in patients with severe lower respiratory tract infections, using metagenomic sequencing. PLoS ONE 7, e30875 (2012). CASADSPubMedArticle Willner, D. et al. Metagenomic analysis of respiratory tract DNA viral communities in cystic fibrosis and non-cystic fibrosis individuals. PLoS ONE 4, e7370 (2009). CASADSPubMedArticle Brandl, K. et al. Vancomycin-resistant enterococci exploit antibiotic-induced innate immune deficits. Nature 455, 804–807 (2008). CASADSISIPubMedArticle Fukuda, S. et al. Bifidobacteria can protect from enteropathogenic infection through production of acetate. Nature 469, 543–547 (2011). CASADSISIPubMedArticle Virgin, H.W., Wherry, E.J. & Ahmed, R. Redefining chronic viral infection. Cell 138, 30–50 (2009). CASISIPubMedArticle Barton, E.S. et al. 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