What Hydra has to say about the role and origin of symbiotic interactions

Biological Bulletin

Volumn 223, Issue 1, 2012, Pages 78-84

  Bosch, Thomas C G ^a  

^a UNIVERSITY OF KIEL   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ALGA; BACTERIUM; COEVOLUTION; GENOME; SEXUAL BEHAVIOR; SYMBIONT;

ALGAE; HYDRA; HYDRA VIRIDIS;

EID: 84866383708     PISSN: 00063185     EISSN: None     Source Type: Journal    
DOI: 10.1086/BBLv223n1p78     Document Type: Review

References (64)

1. Augustin, R., and T. C. G. Bosch. 2011. Cnidarian immunity: a tale of two barriers. Adv. Exp. Med. Biol. 708: 1-16.
2. Augustin, R., F. Anton-Erxleben, S. Jungnickel, G. Hemmrich, B. Spudy, R. Podschun, and T. C. G. Bosch. 2009. Activity of the novel peptide Arminin against multiresistant human pathogens shows the considerable potential of phylogenetically ancient organisms as drug sources. Antimicrob. Agents Chemother. 53: 5245-5250.
3. Augustin, R., S. Fraune, and T.C.G. Bosch. 2010. How Hydra senses and destroys microbes. Semin. Immunol. 22: 54-58.
4. Blanc, G., G. Duncan, I. Agarkova, M. Borodovsky, J. Gurnon, A. Kuo, E. Lindquist, S. Lucas, J. Pangilinan, J. Polle et al. 2010. The Chlorella variabilis NC64A genome reveals adaptation to photosymbiosis, coevolution with viruses, and cryptic sex. Plant Cell 22: 2943-2955.
5. Bosch, T. C. G. 2012. Understanding complex host-microbe interactions in Hydra. Gut Microbes (In press).
6. Bosch, T. C. G., and M. McFall-Ngai. 2011. Metaorganisms as the new frontier. Zoology 114: 185-189.
7. Bosch, T. C. G., R. Augustin, F. Anton-Erxleben, S. Fraune, G. Hemmrich, H. Zill, P. Rosenstiel, G. Jacobs, S. Schreiber, M. Leippe et al. 2009. Uncovering the evolutionary history of innate immunity: the simple metazoan Hydra uses epithelial cells for host defence. Dev. Comp. Immunol. 33: 559-569.
8. Campbell, R. D. 1990. Transmission of symbiotic algae through sexual reproduction in Hydra: movement of algae into the oocyte. Tissue Cell 22: 137-147.
9. Chapman, J. A., E. F. Kirkness, O. Simakov, S. E. Hampson, T. Mitros, T. Weinmaier, T. Rattei, P. G. Balasubramanian, J. Borman, D. Busam et al. 2010. The dynamic genome of Hydra. Nature 464: 592-596.
10. Cook, C. B., and M. O. Kelty. 1982. Glycogen, protein, and lipid content of green, aposymbiotic and nonsymbiotic hydra during starvation. J. Exp. Zool. 222: 1-9.
11. Dana, C. E., K. M. Glauber, T. A. Chan, D. M. Bridge, and R. E. Steele. 2012. Incorporation of a horizontally transferred gene into an operon during cnidarian evolution. PLoS One 7: e31643.
12. Domazet-Loso, T., and D. Tautz. 2008. An ancient evolutionary origin of genes associated with human genetic diseases. Mol. Biol. Evol. 25: 2699-2707.
13. Fitzgerald, K. A., and Z. J. Chen. 2006. Sorting out Toll signals. Cell 125: 834-836.
14. Fraune, S., and T. C. G. Bosch. 2007. Long-term maintenance of species-specific bacterial microbiota in the basal metazoan Hydra. Proc. Natl. Acad. Sci. USA 104: 13146-13151.
15. Fraune, S., and T. C. G. Bosch.2010. Why bacteria matter in animal development and evolution. Bioessays 32: 571-580.
16. Fraune, S., Y. Abe, and T. C. G. Bosch. 2009. Disturbing epithelial homeostasis in the metazoan Hydra leads to drastic changes in associated microbiota. Environ. Microbiol. 11: 2361-2369.
17. Fraune, S., R. Augustin, F. Anton-Erxleben, J. Wittlieb, C. Gelhaus, V. B. Klimovich, M. P. Samoilovich, and T. C. G. Bosch. 2010. In an early branching metazoan, bacterial colonization of the embryo is controlled by maternal antimicrobial peptides Proc. Natl. Acad. Sci. USA 107: 18067-18072.
18. Gregory, T. R. 2002. Genome size and developmental complexity. Genetica 115: 131-146.
19. Gregory, T. R., and P. D. N. Hebert. 1999. The modulation of DNA content: proximate causes and ultimate consequences. Genome Res. 9: 317-324.
20. Grimsley, N., B. Pequin, C. Bachy, H. Moreau, and G. Piganeau. 2010. Cryptic sex in the smallest eukaryotic marine green alga. Mol. Biol. Evol. 27: 47-54.
21. Habetha, M., and T.C.G. Bosch. 2005. Symbiotic Hydra express a plant-like peroxidase gene during oogenesis. J. Exp. Biol. 208: 2157-2164.
22. Habetha, M., F. Anton-Erxleben, K. Neumann, and T. C. G. Bosch. 2003. The Hydra viridis/Chlorella symbiosis. (I) Growth and sexual differentiation in polyps without symbionts. Zoology 106: 101-108.
23. Hamann, O. 1882. Zur Entstehung und Entwicklung der grünen Zellen bei Hydra. Z. Wiss. Zool. 37: 457-464.
24. Hemmrich, G., and T. C. G. Bosch. 2008. Compagen, a comparative genomics platform for early branching metazoan animals, reveals early origins of genes regulating stem cell differentiation. BioEssays 20: 1010-1018.
25. Hemmrich, G., D. J. Miller, and T. C. G. Bosch. 2007a. The evolution of immunity: a low-life perspective. Trends Immunol. 28: 449-454.
26. Hemmrich, G., B. Anokhin, H. Zacharias, and T.C.G. Bosch. 2007b. Molecular phylogenetics in Hydra, a classical model in evolutionary developmental biology. Mol. Phylogenet. Evol. 44: 281-290.
27. Hemmrich, G., K. Khalturin, A.-M. Boehm, M. Puchert, F. Anton-Erxleben, J. Wittlieb, U. C. Klostermeier, P. Rosenstiel, H.-H. Oberg, T. Domazet-Lošo 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. (In press).
28. Huss, V. A. R., C. Holweg, B. Seidel, V. Reich, M. Rahat, and E. Kessler. 1993/94. There is an ecological basis for host/symbiont specificity in chlorella/hydra symbioses. Endocyt. Cell Res. 10: 35-46.
29. Iwasaki, A., and R. Medzhitov. 2004. Toll-like receptor control of the adaptive immune responses. Nat. Immunol. 5: 987-995.
30. Jolley, E., and D. C. Smith. 1978. The green Hydra symbiosis. I. Isolation culture and characteristics of the Chlorella symbiont of the "European" Hydra viridis. New Phytol. 81: 637-645.
31. Jung, S., A. J. Dingley, R. Augustin, F. Anton-Erxleben, M. Stanisak, C. Gelhaus, T. Gutsmann, M. U. Hammer, R. Podschun, M. Leippe, et al. 2009. Hydramacin-1: Structure and antibacterial activity of a protein from the basal metazoan Hydra. J. Biol. Chem. 284: 1896-1905.
32. Khalturin, K., G. Hemmrich, S. Fraune, R. Augustin, and T. C. G. Bosch. 2009. More than just orphans: Are taxonomically restricted genes important in evolution? Trends Genet. 25: 404-413.
33. Kortschak, R. D., G. Samuel, R. Saint, and D. J. Miller. 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.
34. Lange, C., G. Hemmrich, U. C. Klostermeier, J. A. López-Quintero, D. J. Miller, T. Rahn, Y. Weiss, T. C. G. Bosch, and P. Rosenstiel. 2011. Defining the origins of the NOD-like receptor system at the base of animal evolution. Mol. Biol. Evol. 28: 1687-1702.
35. Lenhoff, H. M., and L. Muscatine. 1963. On the role of algae symbiotic with Hydra. Science 142: 956-958.
36. McAuley, P. J. 1981. Control of cell division of the intracellular Chlorella symbionts in green Hydra. J. Cell Sci. 47: 197-206.
37. McAuley, P. J. 1985. Regulation of numbers of symbiotic Chlorella in digestive cells of green hydra. Endocyt. Cell Res. 2: 179-190.
38. Meints, R. H., K. Lee, D. E. Burbank, and J. L. Van Etten. 1984. Infection of a Chlorella-like alga with the virus, PBCV-1: ultrastructural studies. Virology 138: 341-346.
39. Michalek-Wagner, K. and B. L. Willis. 2001. Impacts of bleaching on the soft coral Lobophytum compactum. I. Fecundity, fertilization and offspring viability. Coral Reefs 19: 231-239.
40. Miller, D. J., G. Hemmrich, E. E. Ball, D. C. Hayward, K. Khalturin, N. Funayama, K. Agata and T. C. G. Bosch. 2007. The innate immune repertoire in Cnidaria-ancestral complexity and stochastic gene loss. Genome Biol. 8: R59.
41. Muscatine, L. 1965. Symbiosis of hydra and algae. III. Extracellular products of the algae. Comp. Biochem. Physiol. 16: 77-92.
42. Muscatine, L. 1983. Isolating endosymbiotic algae from Hydra viridis. Pp. 391-392 in: Hydra: Research Methods, H. M. Lenhoff, ed. Plenum Press, New York.
43. Muscatine, L., and H. M. Lenhoff. 1963. Symbiosis: on the role of algae symbiotic with Hydra. Science 142: 956-958.
44. Muscatine, L., and H. M. Lenhoff. 1965a. Symbiosis of hydra and algae. I. Effects of some environmental cations on growth of symbiotic and aposymbiotic hydra. Biol. Bull. 128: 415-424.
45. Muscatine, L., and H. M. Lenhoff. 1965b. Symbiosis of hydra and algae. II. Effects of limited food and starvation on growth of symbiotic and aposymbiotic hydra. Biol. Bull. 129: 316-328.
46. Muscatine, L., and P. J. McAuley. 1983. Transmission of symbiotic algae to eggs of green Hydra. Cytobios 33: 111-124.
47. O'Brien, T. L. 1982. Inhibition of vacuolar membrane fusion by intracellular symbiotic algae in Hydra viridis (Florida strain). J. Exp. Zool. 223: 211-218.
48. Pardy, R. L. 1983. Preparing aposymbiotic hydra. Pp. 394-395 in Hydra: Research Methods, H. M. Lenhoff, ed. Plenum Press, New York.
49. Pool, R. R. 1979. The role of algal antigenic determinants in the recognition of potential algal symbionts by cells of chlorohydra. J. Cell. Sci. 35: 367-379.
50. Rahat, M. 1985. Competition between chlorellae in chimeric infections of Hydra viridis: the evolution of a stable symbiosis. J. Cell Sci. 77: 87-92.
51. Rahat, M., and V. Reich. 1983. A comparative study of tentacle regeneration and number in symbiotic and aposymbiotic Hydra viridis: effect of zoochlorellae. J. Exp. Zool. 227: 63-68.
52. Rahat, M., and V. Reich. 1984. Intracellular infection of aposymbiotic Hydra viridis by a foreign free-living Chlorella sp.: initiation of a stable symbiosis. J. Cell. Sci. 65: 265-277.
53. Rakoff-Nahoum, S., J. Paglino, F. Eslami-Varzaneh, S. Edberg, and R. Medzhitov. 2004. Recognition of commensal microflora by toll-like receptors is required for intestinal homeostasis. Cell 118: 229-241.
54. Roffman, B., and H. M. Lenhoff. 1969. Formation of polysaccharides by hydra from substrates produced by their endosymbiotic algae. Nature 221: 381-382.
55. Rosenberg, E., O. Koren, L. Reshef, R. Efrony, and I. Zilber-Rosenberg. 2007. The role of microorganisms in coral health, disease and evolution. Nat. Rev. Microbiol. 5: 355-362.
56. Rosenberg, E., A. Kushmaro, E. Kramarsky-Winter, E. Banin, and L. Yossi. 2009. The role of microorganisms in coral bleaching. ISME J. 3: 139-46.
57. Rosenstiel, P., E. Philipp, S. Schreiber, and T. C. G. Bosch. 2009. Evolution and function of innate immune receptors-insights from marine invertebrates. J. Innate Immun. 1: 291-300.
58. Steele, R. E., S. E. Hampson, N. A. Stover, D. F. Kibler, and H. R. Bode. 2004. Probable horizontal transfer of a gene between a protist and a cnidarian. Curr. Biol. 14: R298-299.
59. Technau, U., S. Rudd, P. Maxwell, P. M. Gordon, M. Saina, L. C. Grasso, D. C. Hayward, C. W. Sensen, R. Saint, T. W. Holstein et al. 2005. Maintenance of ancestral complexity and non-metazoan genes in two basal cnidarians. Trends Genet. 21: 633-639.
60. Thorington, G., and L. Margulis. 1981. Hydra viridis: transfer of metabolites between Hydra and symbiotic algae. Biol. Bull. 160: 175-188.
61. Vinogradov, A. E. 1995. Nucleotypic effect in homotherms: bodymass-corrected basal metabolic rate of mammals is related to genome size. Evolution 49: 1249-1259.
62. Vinogradov, A. E. 1997. Nucleotypic effect in homotherms: body mass independent resting metabolic rate of passerine birds is related to genome size. Evolution 51: 220-225.
63. Zacharias, H., B. Anokhin, K. Khalturin, and T. C. G. Bosch. 2004. Genome sizes and chromosomes in the basal metazoan Hydra. Zoology 107: 219-227.
64. Zilber-Rosenberg, I., and E. Rosenberg. 2008. Role of microorganisms in the evolution of animals and plants: the hologenome theory of evolution. FEMS Microbiol Rev. 32: 723-735.