Journal of Microbiology

, Volume 53, Issue 3, pp 193–200 | Cite as

Microbial ecology in Hydra: Why viruses matter

  • Thomas C.G. Bosch
  • Juris A. Grasis
  • Tim Lachnit
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Abstract

While largely studied because of their harmful effects on human health, there is growing appreciation that viruses are also important members of the animal holobiont. This review highlights recent findings on viruses associated with Hydra and related Cnidaria. These early evolutionary diverging animals not only select their bacterial communities but also select for viral communities in a species-specific manner. The majority of the viruses associating with these animals are bacteriophages. We demonstrate that the animal host and its virome have evolved into a homeostatic, symbiotic relationship and propose that viruses are an important part of the Hydra holobiont by controlling the species-specific microbiome. We conclude that beneficial virus-bacterial-host interactions should be considered as an integral part of animal development and evolution.

Keywords

innate immunity host-microbe interaction holobiont virus evolution microbiota Hydra 
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References

  1. Barash, Y., Sulam, R., Loya, Y., and Rosenberg, E. 2005. Bacterial strain BA-3 and a filterable factor cause a white plague-like disease in corals from the Eilat coral reef. Aquat. Microbiol. Ecol. 40, 183–189.CrossRefGoogle Scholar
  2. 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 2013. Bacteriophage adhering to mucus provide a non-host-derived immunity. Proc. Natl. Acad. Sci. USA 110, 10771–10776.CrossRefPubMedCentralPubMedGoogle Scholar
  3. Barton, E.S., White, D.W., Cathelyn, J.S., Brett-McClellan, K.A., Engle, M., Diamond, M.S., and Virgin, H.W. 2007. Herpesvirus latency confers symbiotic protection from bacterial infection. Nature 447, 326–329.CrossRefPubMedGoogle Scholar
  4. Ben-Haim, Y. and Rosenberg, E. 2002. A novel Vibrio sp. pathogen of the coral Pocillopora damincornis. Mar. Biol. 141, 47–55.CrossRefGoogle Scholar
  5. Ben-Haim, Y., Zicherman-Keren, M., and Rosenberg, E. 2003a. Temperature-regulated bleaching and lysis of the coral Pocillopora damicornis by the novel pathogen Vibrio coralliilyticus. Appl. Environ. Microbiol. 69, 4236–4242.CrossRefPubMedCentralPubMedGoogle Scholar
  6. Ben-Haim, Y., Thompson, F.L., Thompson, C.C., Cnockaert, M.C., Hoste, B., Swings, J., and Rosenberg, E. 2013b. Vibrio coralliilyticus sp. nov., a temperature-dependent pathogen of the coral Pocillopora damicornis. Int. J. Syst. Evol. Microbiol. 53, 309–315.CrossRefGoogle Scholar
  7. Biagi, E., Candela, M., Franceschi, C., and Brigidi, P. 2011. The aging gut microbiota: new perspectives. Ageing Res. Rev. 10, 428–429.CrossRefPubMedGoogle Scholar
  8. Biagi, E., Candela, M., Fairweather-Tait, S., Franceschi, C., and Brigidi, P. 2012. Aging of the human metaorganism: the microbial counterpart. Age (Dordr) 34, 247–267.CrossRefGoogle Scholar
  9. Bosch, T.C.G. 2012a. What Hydra has to say about the role and origin of symbiotic interactions. Biol. Bull. 223, 78–84.PubMedGoogle Scholar
  10. Bosch, T.C.G. 2012b. Understanding complex host-microbe interactions in Hydra. Gut Microbes 3, 1–7.CrossRefGoogle Scholar
  11. Bosch, T.C.G. 2013. Cnidarian-microbe interactions and the origin of innate immunity in metazoans. Ann. Rev. Microbiol. 67, 499–518.CrossRefGoogle Scholar
  12. Bosch, T.C.G. 2014. Rethinking the role of immunity: lessons from Hydra. Trends Immunol. 35, 495–502.CrossRefPubMedGoogle Scholar
  13. Bosch, T.C.G. and McFall-Ngai, M.J. 2011. Metaorganisms as the new frontier. Zoology 114, 185–190.CrossRefPubMedCentralPubMedGoogle Scholar
  14. Brucker, R.M. and Bordenstein, S.R. 2012. Speciation by symbiosis. Trends Ecol. Evol. 27, 443–451.CrossRefPubMedGoogle Scholar
  15. Brucker, R.M. and Bordenstein, S.R. 2013a. The capacious hologenome. Zoology 116, 260–261.CrossRefPubMedGoogle Scholar
  16. Brucker, R.M. and Bordenstein, S.R. 2013b. The hologenomic basis of speciation: gut bacteria cause hybrid lethality in the genus Nasonia. Science 341, 667–669.CrossRefGoogle Scholar
  17. Brucker, R.M. and Bordenstein, S.R. 2014. Response to comment on “The hologenomic basis of speciation: gut bacteria cause hybrid lethality in the genus Nasonia”. Science 345, 1011.CrossRefPubMedGoogle Scholar
  18. Chanishvili, N. 2012. Phage therapy-history from Twort and d’Herelle through Soviet experience to current approaches. Adv. Virus Res. 83, 3–40.CrossRefPubMedGoogle Scholar
  19. Chapman, J.A., Kirkness, E.F., Simakov, O., Hampson, S.E., Mitros, T., Weinmaier, T., Rattei, T., Balasubramanian, P.G., Borman, J., Busam, D., et al 2010. The dynamic genome of Hydra. Nature 464, 592–596.CrossRefPubMedGoogle Scholar
  20. Cohen, Y., Joseph Pollock, F., Rosenberg, E., and Bourne, D.G. 2013. Phage therapy treatment of the coral pathogen Vibrio coralliilyticus. Microbiologyopen 2, 64–74.CrossRefPubMedCentralPubMedGoogle Scholar
  21. Duerkop, B. and Hooper, L.V. 2013. Resident viruses and their interactions with the immune system. Nat. Immunol. 14, 654–659.CrossRefPubMedCentralPubMedGoogle Scholar
  22. Eberl, G. 2010. A new vision of immunity: homeostasis of the superorganism. Mucosal Immunol. 3, 450–460.CrossRefPubMedGoogle Scholar
  23. Efrony, R., Atad, I., and Rosenberg, E. 2008. Phage therapy of coral white plague disease: properties of phage BA3. Curr. Microbiol. 58, 139–145.CrossRefPubMedGoogle Scholar
  24. Frankenfeld, C.L., Atkinson, C., Wähälä, K., and Lampe, J.W. 2014. Obesity prevalence in relation to gut microbial environments capable of producing equol or O-desmethylangolensin from the isoflavone daidzein. Eur. J. Clin. Nutr. 68, 526–530.CrossRefPubMedGoogle Scholar
  25. Franzenburg, S., Walter, J., Künzel, S., Wang, J., Baines, J.F., Bosch, T.C.G., and Fraune, S. 2013a. Distinct antimicrobial peptide expression determines host species-specific bacterial associations. Proc. Natl. Acad. Sci. USA 110, E3730–3738.CrossRefPubMedCentralPubMedGoogle Scholar
  26. Franzenburg, S., Fraune, S., Altrock, P.M., Künzel, S., Baines, J.F., Traulsen, A., and Bosch, T.C.G. 2013b Bacterial colonization of Hydra hatchlings follows a robust temporal pattern. ISME J. 7, 781–790.CrossRefPubMedCentralPubMedGoogle Scholar
  27. Fraune, S., Anton-Erxleben, F., Augustin, R., Franzenburg, S., Knop, M., Schröder, K., Willoweit-Ohl, D., and Bosch, T.C.G. 2014. Bacteria-bacteria interactions within the microbiota of the ancestral metazoan Hydra contribute to fungal resistance. ISME J. doi: 10.1038/ismej.2014.239.Google Scholar
  28. Fraune, S., and Bosch, T.C.G. 2007. Long-term maintenance of species-specific bacterial microbiota in the basal metazoan Hydra. Proc. Natl. Acad. Sci. USA 104, 13146–13151.CrossRefPubMedCentralPubMedGoogle Scholar
  29. Fraune, S. and Bosch, T.C.G. 2010. Why bacteria matter in animal development and evolution. Bioessays 32, 571–580.CrossRefPubMedGoogle Scholar
  30. Gilbert, S.F., Sapp, J., and Tauber, A.I. 2012. A symbiotic view of life: we have never been individuals. Q. Rev. Biol. 87, 325–341.CrossRefPubMedGoogle Scholar
  31. Grasis, J.A., Lachnit, T., Anton-Erxleben, F., Lim, Y.W., Schmieder, R., Fraune, S., Franzenburg, S., Insua, S., Machado, G., Haynes, M., et al 2014. Species-specific viromes in the ancestral holobiont Hydra. PLoS One 9, e109952.Google Scholar
  32. Hemmrich, G., Khalturin, K., Boehm, A.M., Puchert, M., Anton-Erxleben, F., Wittlieb, J., Klostermeier, U.C., Rosenstiel, P., Oberg, H.H., Domazet-Lošo, T., et al 2012. Molecular signatures of the three stem cell lineages in Hydra and the emergence of stem cell function at the base of multicellularity. Mol. Biol. Evol. doi: 10.1093/molbev/mss13.Google Scholar
  33. 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 2013. Microbiota modulate behavioral and physiological abnormalities associated with neurodevelopmental disorders. Cell 155, 1451–1463.CrossRefPubMedCentralPubMedGoogle Scholar
  34. Human Microbiome Project Consortium. 2012. Structure, function and diversity of the healthy human microbiome. Nature 486, 207–214.CrossRefGoogle Scholar
  35. Kaiko, G.E. and Stappenbeck, T.S. 2014. Host-microbe interactions shaping the gastrointestinal environment. Trends Immunol. 35, 538–548.CrossRefPubMedGoogle Scholar
  36. Kernbauer, E., Ding, Y., and Cadwell, K. 2014. An enteric virus can replace the beneficial function of commensal bacteria. Nature doi: 10.1038/nature13960.Google Scholar
  37. Knoll, A.H. and Sperling, E. 2014. Oxygen and animals in Earth history. Proc. Natl. Acad. Sci. USA 111, 3907–3908.CrossRefPubMedCentralPubMedGoogle Scholar
  38. Kortschak, R.D., Samuel, G., Saint, R., and Miller, D.J. 2003. EST analysis of the cnidarian Acropora millepora reveals extensive gene loss and rapid sequence divergence in the model invertebrates. Curr. Biol. 13, 2190–2195.CrossRefPubMedGoogle Scholar
  39. Lederberg, J. 1996. Smaller fleas … ad infinitum: Therapeutic bacteriophage redux. Proc. Natl. Acad. Sci. USA 93, 3167–3168.CrossRefPubMedCentralPubMedGoogle Scholar
  40. Li, X., Feng, J., and Sun, R. 2011. Oxidative stress induces reactivation of Kaposi’s sarcoma-associated herpesvirus and death of primary effusion lymphoma cells. J. Virol. 85, 715–724.CrossRefPubMedCentralPubMedGoogle Scholar
  41. Liévin-Le Moal, V. and Servin, A.L. 2006. The front line of enteric host defense against unwelcome intrusion of harmful microorganisms: mucin, antimicrobial peptides, and microbiota. Clin. Microbiol. Rev. 19, 315–337.CrossRefGoogle Scholar
  42. McFall-Ngai, M., Hadfield, M.G., Bosch, T.C.G., Carey, H.V., Domazet-Loso, T., Douglas, A.E., Dubilier, N., Eberl, G., Fukami, T., Gilbert, S.F., et al 2013. Animals in a bacterial world, a new imperative for the life sciences. Proc. Natl. Acad. Sci. USA 110, 3229–3236.CrossRefPubMedCentralPubMedGoogle Scholar
  43. Miller, D.J., Ball, E.E., and Technau, U. 2005. Cnidarians and ancestral genetic complexity in the animal kingdom. Trends Genet. 21, 536–539.CrossRefPubMedGoogle Scholar
  44. Mills, D.B., Ward, L.M., Jones, C.A., Sweeten, B., Forth, M., Treusch, A.H., and Canfield, D.E. 2014. Oxygen requirements of the earliest animals. Proc. Natl. Acad. Sci. USA 111, 4168–4172.CrossRefPubMedCentralPubMedGoogle Scholar
  45. Minot, S., Sinha, R., Chen, J., Li, H., Keilbaugh, S.A., Wu, G.D., Lewis, J.D., and Bushman, F.D. 2011. The human gut virome: Interindividual variation and dynamic response to diet. Genome Res. 21, 1616–1625.CrossRefPubMedCentralPubMedGoogle Scholar
  46. Nosenko, T., Schreiber, F., Adamska, M., Adamski, M., Eitel, M., Hammel, J., Maldonado, M., Müller, W.E., Nickel, M., Schierwater, B., et al 2013. Deep metazoan phylogeny: When different genes tell different stories. Mol. Phylogenet. Evol. 67, 223–233.CrossRefPubMedGoogle Scholar
  47. Pennisi, E. 2013. Mysteries of development. How do microbes shape animal development? Science 340, 1159–1160.CrossRefPubMedGoogle Scholar
  48. Philippe, H., Brinkmann, H., Lavrov, D.V., Littlewood, D.T., Manuel, M., Wörheide, G., and Baurain, D. 2011. Resolving difficult phylogenetic questions: Why more sequences are not enough. PLoS Biol. 9, e1000602.Google Scholar
  49. Putnam, N.H., Srivastava, M., Hellsten, U., Dirks, B., Chapman, J., Salamov, A., Terry, A., Shapiro, H., Lindquist, E., Kapitonov, V.V., et al 2007. Sea anemone genome reveals ancestral eumetazoan gene repertoire and genomic organization. Science 317, 86–94.CrossRefPubMedGoogle Scholar
  50. Qin, J., Li, R., Raes, J., Arumugam, M., Burgdorf, K.S., Manichanh, C., Nielsen, T., Pons, N., Levenez, F., Yamada, T., Mende, D.R., et al 2010. A human gut microbial gene catalogue established by metagenomics sequencing. Nature 464, 59–65.CrossRefPubMedCentralPubMedGoogle Scholar
  51. Renault, S., Stasiak, K., Federici, B., and Bigot, Y. 2005. Commensal and mutualistic relationships of reoviruses with their parasitoid wasp hosts. J. Insect Physiol. 51, 137–148.CrossRefPubMedGoogle Scholar
  52. Reyes, A., Semenkovich, N.P., Whiteson, K., Rohwer, F., and Gordon, J.I. 2012. Going viral: next-generation sequencing applied to phage populations in the human gut. Nat. Rev. Microbiol. 10, 607–617.CrossRefPubMedCentralPubMedGoogle Scholar
  53. Reyes, A., Wu, M., McNulty, N.P., Rohwer, F.L., and Gordon, J.I. 2013. Gnotobiotic mouse model of phage-bacterial host dynamics in the human gut. Proc. Natl. Acad. Sci. USA 110, 20236–20241.CrossRefPubMedCentralPubMedGoogle Scholar
  54. Roossinck, M.J. 2011. The good viruses: viral mutualistic symbioses. Nat. Rev. Microbiol. 9, 99–108.CrossRefPubMedGoogle Scholar
  55. Rosenberg, E., Kellogg, A., and Rohwer, F. 2007. Coral microbiology. Oceanography 20, 146–154.CrossRefGoogle Scholar
  56. Rosenberg, E. and Zilber-Rosenberg, I. 2011. Symbiosis and development: The hologenome concept. Birth Defects Res. C Embryo Today 93, 56–66.CrossRefPubMedGoogle Scholar
  57. Roux, S., Enault, F., Robin, A., Ravet, V., Personnic, S., Theil, S., Colombet, J., Sime-Ngando, T., and Debroas, D. 2012. Assessing the diversity and specificity of two freshwater viral communities through metagenomics. PLoS One 7, e33641.Google Scholar
  58. Sharon, G., Segal, D., Ringo, J.M., Hefetz, A., Zilber-Rosenberg, I., and Rosenberg, E. 2010. Commensal bacteria play a role in mating preference of Drosophila melanogaster. Proc. Natl. Acad. Sci. USA 107, 20051–20056.CrossRefGoogle Scholar
  59. Stappenbeck, T.S., Hooper, L.V., and Gordon, J.I. 2002. Developmental regulation of intestinal angiogenesis by indigenous microbes via Paneth cells. Proc. Natl. Acad. Sci. USA 99, 15451–15455.CrossRefPubMedCentralPubMedGoogle Scholar
  60. Stern, A. and Sorek, R. 2012. The phage-host arms-race: Shaping the evolution of microbes. Bioessays 33, 43–51.CrossRefGoogle Scholar
  61. Stilling, R.M., Bordenstein, S.R., Dinan, T.G., and Cryan, J.C. 2014. Friends with social benefits: host-microbe interactions as a driver of brain evolution and development? Front. Cell. Infect. Microbiol. 4, 147.CrossRefPubMedCentralPubMedGoogle Scholar
  62. Sulakvelidze, A., Alavidze, Z., and Morris, J.G.Jr. 2001. Bacteriophage therapy. Antimicrob. Agents Chemother. 45, 649–659.CrossRefGoogle Scholar
  63. Suttle, C.A. 2007. Marine viruses-major players in the global ecosystem. Nat. Rev. Microbiol. 5, 801–812.CrossRefPubMedGoogle Scholar
  64. Technau, U., Rudd, S., Maxwell, P., Gordon, P.M.K., Saina, M., Grasso, L.C., Hayward, D.C., Sensen, C.W., Saint, R., Holstein, T.W., et al 2005. Maintenance of ancestral complexity and non-metazoan genes in two basal cnidarians. Trends Genet. 21, 633–639.CrossRefPubMedGoogle Scholar
  65. Thompson, F.L., Barash, Y., Sawabe, T., Sharon, G., Swings, J., and Rosenberg, E. 2006. Thalassomonas loyana sp. nov., a causative agent of the white plague-like disease of corals on the Eilat coral reef. Int. J. Syst. Evol. Microbiol. 56, 365–368.CrossRefPubMedGoogle Scholar
  66. Trembley, A. 1744. Mémoires, Pour Servir à l´Histoire d´un Genre de Polypes d´Eau Douce, à Bras en Frome de Cornes. Verbeek, Leiden (Netherlands).Google Scholar
  67. Turnbaugh, P.J., Bäckhed, F., Fulton, L., and Gordon, J.I. 2008. Diet-induced obesity is linked to marked but reversible alterations in the mouse distal gut microbiome. Cell Host Microbe 3, 213–223.CrossRefPubMedCentralPubMedGoogle Scholar
  68. Turnbaugh, P.J., Ley, R.E., Hamady, M., Fraser-Liggett, C.M., Knight, R., and Gordon, J.I. 2007. The human microbiome project. Nature 449, 804–810.CrossRefPubMedCentralPubMedGoogle Scholar
  69. Turnbaugh, P.J., Ley, R.E., Mahowald, M.A., Magrini, V., Mardis, E.R., and Gordon, J.I. 2006. An obesity-associated gut microbiome with increased capacity for energy harvest. Nature 444, 1027–1031.CrossRefPubMedGoogle Scholar
  70. Umbach, J.L., Kramer, M.F., Jurak, I., Karnowski, H.W., Coen, D.M., and Cullen, B.R. 2008. MicroRNAs expressed by herpes simplex virus 1 during latent infection regulate viral mRNAs. Nature 454, 780–783.PubMedCentralPubMedGoogle Scholar
  71. Verbeken, G., Huys, I., Pirnay, J.P., Jennes, S., Chanishvili, N., Scheres, J., Górski, A., De Vos, D., and Ceulemans, C. 2014. Taking bacteriophage therapy seriously: a moral argument. Biomed. Res. Int. 6, 213–216.Google Scholar
  72. Virgin, H.W., Wherry, E.J., and Ahmed, R. 2009. Redefining chronic viral infection. Cell. 138, 30–50.CrossRefPubMedGoogle Scholar
  73. Weitz, J.S., Poisot, T., Meyer, J.R., Flores, C.O., Valverde, S., Sullivan, M.B., Hochberg, M.E. 2013. Phage-bacteria infection networks. Trends Microbiol. 21, 82–91.CrossRefPubMedGoogle Scholar
  74. Wittlieb, J., Khalturin, K., Lohmann, J.U., Anton-Erxleben, F., and Bosch, T.C.G. 2006. Transgenic Hydra allow in vivo tracking of individual stem cells during morphogenesis. Proc. Natl. Acad. Sci. USA 103, 6208–6211.CrossRefPubMedCentralPubMedGoogle Scholar

Copyright information

© The Microbiological Society of Korea and Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • Thomas C.G. Bosch
    • 1
  • Juris A. Grasis
    • 1
    • 2
  • Tim Lachnit
    • 1
  1. 1.Zoological InstituteChristian-Albrechts-University KielKielGermany
  2. 2.Department of BiologySan Diego State UniversitySan DiegoUSA

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