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Associations between the White Sea colonial hydroid Dynamena pumila and microorganisms

Published online by Cambridge University Press:  14 June 2012

O.A. Gorelova ,
O.I. Baulina ,
I.A. Kosevich  and
E.S. Lobakova
O.A. Gorelova
Affiliation:
Faculty of Biology, M.V. Lomonosov Moscow State University, Moscow 119991, Russia
O.I. Baulina
Affiliation:
Faculty of Biology, M.V. Lomonosov Moscow State University, Moscow 119991, Russia
I.A. Kosevich*
Affiliation:
Faculty of Biology, M.V. Lomonosov Moscow State University, Moscow 119991, Russia
E.S. Lobakova
Affiliation:
Faculty of Biology, M.V. Lomonosov Moscow State University, Moscow 119991, Russia
*
Correspondence should be addressed to: I.A. Kosevich, Faculty of Biology, M.V. Lomonosov Moscow State University, Moscow 119991, Russia email: ikos@mail.ru
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Abstract

Marine sessile invertebrates with outer skeleton constitute additional substrate for a diverse group of epibiotic organisms. Colonial hydroids are no exception. Large numbers of motile and sessile organisms use hydroid colonies covered with chitinous perisarc for permanent or temporal attachment. Such epibiotic associations between colonial hydroids and microorganisms are poorly studied and mostly known for subtropical regions. There are no data about the development of such epibiotic association and type of its specificity yet. The present paper for the first time describes the epibiotic association of the colonial thecate hydroid Dynamena pumila from the high latitude sea. We reconstruct the spatial and temporal development of such epibiotic community and analyse the organization of the multicomponent biofilm covering the hydroid colony. Comparison of the epibiotic community in different seasons indicates for holding out of the basal features and components of the community during the whole year. Ultrastructural investigations revealed that components of the biofilm affect the outer skeleton of the hydroid colony that results in penetration of the microorganisms into the skeleton and even soft tissues. Our data allow supposing that association of hydroid D. pumila with a microorganism community has features of a symbiotic system.

Keywords

thecate hydroidDynamena pumilaepibiotic microorganism communitybiofilmsymbiotic associationmicroalgaecyanobacteriabacteria
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 93 , Issue 1 , February 2013 , pp. 69 - 80
Copyright
Copyright © Marine Biological Association of the United Kingdom 2012

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References

REFERENCES

Achituv, Y., Benayahu, Y. and Hanania, J. (1992) Planulae brooding and acquisition of zooxanthellae in Xenia macrospiculata (Cnidaria: Octocorallia). Helgoländer Meeresuntersuchungen 46, 301–310.CrossRefGoogle Scholar
Apprill, A.M. and Gates, R.D. (2007) Recognizing diversity in coral symbiotic dinoflagellate communities. Molecular Ecology 16, 1127–1134.CrossRefGoogle ScholarPubMed
Bavestrello, G., Cerrano, C., Cattaneo, V.R. and Sarà, M. (1996) Relations between Eudendrium glomeratum (Cnidaria, Hydromedusae) and its associated vagile fauna. Scientia Marina (Barcelona) 60, 137–143.Google Scholar
Bavestrello, G., Cerrano, C., Di Camillo, C., Puce, S., Romagnoli, T., Tazioli, S. and Totti, C. (2008) The ecology of protists epibiontic on marine hydroids. Journal of the Marine Biological Association of the United Kingdom 88, 1611–1617.CrossRefGoogle Scholar
Beloussov, L.V., Labas, J.A., Kazakova, N.I. and Zaraisky, A.G. (1989) Cytophysiology of growth pulsations in hydroid polyps. Journal of Experimental Zoology 249, 258–270.CrossRefGoogle Scholar
Berrill, N.J. (1949) Growth and form in calyptoblastic hydroids. I. Comparison of a campanulid, campanilarian, sertularian and plumularian. Journal of Morphology 85, 297–335.CrossRefGoogle ScholarPubMed
Carpenter, E.J. and Foster, R.A. (2002) Marine cyanobacterial symbioses. In Rai, A., Bergman, B. and Rasmussen, U. (eds) Cyanobacteria in symbiosis. Dordrecht, The Netherlands: Kluwer Academic Publishers, pp. 11–17.Google Scholar
Carpenter, E.J. and Janson, S. (2000) Intracellular cyanobacterial symbionts in the marine diatom Climacodium frauenfeldianum (Bacillariophyceae). Journal of Phycology 36, 540–544.CrossRefGoogle ScholarPubMed
Carricart, G.J.P. and Torres, B.A.U. (1993) Zooxanthellae and chlorophyll-a responses in the scleractinian coral Montastrea cavernosa at Triangulos-W Reef, Campeche Bank, Mexico. Revista de Biologia Tropical 41, 491–494.Google Scholar
Cornelius, P.F.S. (1975) A revision of the species of Lafoeidae and Haleciidae (Coelenterata: Hydroida) recorded from Britain and nearby seas. Bulletin of the British Museum (Natural History) (Zoology Series) 28, 373–426.CrossRefGoogle Scholar
Cornelius, P.F.S. (1979) A revision of the species of Sertulariidae (Coelenterata: Hydroida) recorded from Britain and nearby seas. Bulletin of the British Museum (Natural History) (Zoology Series) 34, 243–321.Google Scholar
Davey, M.E. and O'Toole, G.A. (2000) Microbial biofilms: from ecology to molecular genetics. Microbiology and Molecular Biology Reviews 64, 847–867.CrossRefGoogle ScholarPubMed
Di Camillo, C.G., Bavestrello, G., Valisano, L. and Puce, S. (2008) Spatial and temporal distribution in a tropical hydroid assemblage. Journal of the Marine Biological Association of the United Kingdom 88, 1589–1599.CrossRefGoogle Scholar
Di Camillo, C.G., Daniel, M. and Brytaev, T.A. (2010) Symbiotic association between Solanderia secunda (Cnidaria, Hydrozoa, Solanderiidae) and Medioantenna variopinta sp. nov. (Annelida, Polychaeta, Polynoidae) from North Sulawesi (Indonesia). Helgoland Marine Research, 1–17.Google Scholar
Di Camillo, C.G., Puce, S., Romagnoli, T., Tazioli, S., Totti, C. and Bavestrello, G. (2005) Relationships between benthic diatoms and hydrozoans (Cnidaria). Journal of the Marine Biological Association of the United Kingdom 85, 1373–1380.CrossRefGoogle Scholar
Di Camillo, C., Puce, S., Romagnoli, T., Tazioli, S., Totti, C. and Bavestrello, G. (2006) Coralline algae epibionthic on thecate hydrozoans (Cnidaria). Journal of the Marine Biological Association of the United Kingdom 86, 1285–1289.CrossRefGoogle Scholar
Duval, B., Shetty, K. and Thomas, W.H. (2000) Phenolic compounds and antioxidant properties in the snow alga Chlamydomonas nivalis after exposure to UV light. Journal of Applied Phycology 11, 559–566.CrossRefGoogle Scholar
Foster, R.A. and Zehr, P. (2006) Characterization of diatom–cyanobacteria symbioses on the basis of nifH, hetR and 16S rRHA sequences. Environmental Microbiology 8, 1913–1925.CrossRefGoogle Scholar
Gorelova, O.A. and Baulina, O.I. (2009) Ultrastructure of cyanobacterium Nostoc sp. f. Blasia cell forms in persisting populations. Microbiology 78, 609–617.CrossRefGoogle Scholar
Gorelova, O.A., Baulina, O.I. and Lobakova, E.S. (2009a) Ultrastructure of cyanobacteria associated with hydroid Dynamena pumila (L., 1758). Bulletin of the Moscow Society of Nature Investigators, Biological Section 114, 166–169.Google Scholar
Gorelova, O.A., Kosevich, I.A., Baulina, O.I., Fedorenko, T.A., Torshkhoeva, A.Z. and Lobakova, E.S. (2009b) Associations between the White Sea invertebrates and oxygen-evolving phototrophic microorganisms. Moscow University Biological Sciences Bulletin 64, 16–22.CrossRefGoogle Scholar
Gorelova, O.A., Kosevich, I.A., Fedorenko, T.A., Baulina, O.I. and Lobakova, E.S. (2008) Oxygen-evolving pro- and eukaryotic phototrophic microorganisms, associated with White Sea invertebrates. In Proceedings of the International Scientific Conference and VII School in Marine Biology (June 9–13, 2008, Rostov-upon-Don). Recent problems of algology. Rostov-upon-Don: South Scientific Centre of the Russian Academy of Science Publisher, pp. 113–115.Google Scholar
Gravier-Bonnet, N. and Bourmand, C. (2005) Cloning by releasing specialized frustules in a successful epiphytic zooxanthellate haleciid (Cnidaria, Hydrozoa, Haleciidae), with comments on stolonization and frustulation. Invertebrate Reproduction and Development 48, 63–69.CrossRefGoogle Scholar
Hirooka, T., Akiyama, Y., Tsuji, N., Nakamura, T., Nagase, H., Hirata, K. and Miyamoto, K. (2003) Removal of hazardous phenols by microalgae under photoautotrophic conditions. Journal of Bioscience and Bioengineering 95, 200–203.CrossRefGoogle ScholarPubMed
Hofmann, D.K. and Brand, U. (1987) Induction of metamorphosis in the symbiotic scyphozoan Cassiopea andromeda: role of marine bacteria and of biochemicals. Symbiosis 4, 99–116.Google Scholar
Hofmann, D.K., Fitt, W.K. and Fleck, J. (1996) Checkpoints in the life-cycle of Cassiopea spp.: control of metagenesis and metamorphosis in a tropical jellyfish. International Journal of Developmental Biology 40, 331–338.Google Scholar
Hofmann, D.K. and Henninf, G. (1991) Effects of axenic culture conditions on asexual reproduction and metamorphosis in the symbiotic scyphozoan Cassiopea andromeda. Symbiosis 10, 83–93.Google Scholar
Hosny, A.E.-D.M.S., El-Shayeb, N.A., Abood, A. and Abdel-Fattah, A.M. (2010) A potent chitinolytic activity of marine Actinomycete sp. and enzymatic production of chitooligosaccharides. Australian Journal of Basic and Applied Sciences 4, 615–623.Google Scholar
Hughes, R.G., Tardent, P. and Tardent, R. (1980) Current induced variations in the growth and morphology of hydroids. In Tardent, P. and Tardent, R. (eds) Development and cellular biology of coelenterates. Amsterdam: Elsevier/North-Holland Biomedical Press, pp. 179–184.Google Scholar
Ishikura, M., Hagiwara, K., Takishita, K., Haga, M., Iwai, K. and Maruyama, T. (2004) Isolation of new Symbiodinium strains from tridacnid giant clam (Tridacna crocea) and sea slug (Pteraeolidia ianthina) using culture medium containing giant clam tissue homogenate. Marine Biotechnology (NY) 6, 378–385.CrossRefGoogle ScholarPubMed
Ivanova, A.O. (2008) Planctomycetes of sphagnum bogs: phylogenetic diversity and ecological functions. PhD thesis. Moscow State University, Moscow, Russia.Google Scholar
Janson, S. (2002) Cyanobacteria in symbiosis with diatoms. In Rai, A., Bergman, B. and Rasmussen, U. (eds) Cyanobacteria in symbiosis. Dordrecht, The Netherlands: Kluwer Academic Publishers, pp. 1–10.Google Scholar
Knight, D.P. (1970) Sclerotization of the perisarc of the calyptoblastic hydroid, Laomedea flexuosa. 1. The identification and localization of dopamine in the hydroid. Tissue and Cell 2, 467–477.CrossRefGoogle ScholarPubMed
Kosevich, I.A. and Fedosov, A.E. (2008) Morphogenesis in colonial hydroids: pulsating rudiment splitting. Russian Journal of Developmental Biology 38, 279–292.CrossRefGoogle Scholar
Kossevitch, I.A., Herrmann, K. and Berking, S. (2001) Shaping of colony elements in Laomedea flexuosa Hinks (Hydrozoa, Thecaphora) includes a temporal and spatial control of skeleton hardening. Biological Bulletin. Marine Biological Laboratory, Woods Hole 201, 417–423.CrossRefGoogle Scholar
Kuhn, A. (1914) Entwicklungsgeschichte und Verwandtschaftsbeziehungen der Hydrozoen. I.Teil: Die Hydroiden. In Spengel, J.W. (ed.) Ergebnisse und Fortschritte der Zoologie. Jena: Verlag von Gustav Fischer, pp. 1–284.Google Scholar
Kulichevskaya, I.S., Ivanova, A.O., Baulina, O.I., Bodelier, P.L.E., Sinninghe Damsté, J.S. and Dedysh, S.N. (2008) Singulisphaera acidiphila gen. nov., sp. nov., a non-filamentous, Isosphaera-like planctomycete from acidic northern wetlands. International Journal of Systematic and Evolutionary Microbiology 58, 1186–1193.CrossRefGoogle Scholar
Le Tissier, M.D.A.A. (1991) The nature of the skeleton and skeletogenic tissues in the Cnidaria. In Cornelius, P.F.S., Hughes, R.B. and Robson, E.A. (eds) Coelenterate biology: recent research on cnidaria and ctenophora. Dordrecht, The Netherlands: Kluwer Academic Publishers, pp. 397–402.CrossRefGoogle Scholar
Lee, Y.K., Lee, J.-H. and Lee, H.K. (2001) Microbial symbiosis in marine sponges. Journal of Microbiology 39, 254–264.Google Scholar
Leletkin, V.A., Nechai, E.G. and Titlyanov, E.A. (1994) Respiration rate of zooxanthellae in a native coral. Russian Journal of Marine Biology, 90–99.Google Scholar
Lobakova, E.S., Georgiev, A.A., Fedorenko, T.A. and Gorelova, O.A. (2008) Diatoms as epibionts of White Sea hydroids. In Proceedings of the International Scientific Conference and VII School in Marine Biology (June 9–13, 2008, Rostov-upon-Don). Recent problems of algology. Rostov-upon-Don: South Scientific Centre of the Russian Academy of Science Publisher, pp. 217–218.Google Scholar
Loram, J.E., Trapido-Rosenthal, H.G. and Douglas, A.E. (2007) Functional significance of genetically different symbiotic algae Symbiodinium in a coral reef symbiosis. Molecular Ecology 16, 4849–4857.CrossRefGoogle Scholar
Marques, A.C., Cantero, A.L.P. and Vervoort, W. (2000) Mediterranean species of Eudendrium Ehrenberg, 1834 (Hydrozoa, Anthomedusae, Eudendriidae) with the description of a new species. Journal of Zoology 252, 197–213.CrossRefGoogle Scholar
Maruyama, T., Ishikura, M., Yamazaki, S. and Kanai, S. (1998) Molecular phylogeny of zooxanthellate bivalves. Biological Bulletin. Marine Biological Laboratory, Woods Hole 195, 70–77.CrossRefGoogle Scholar
Millonig, G. (1964) Study on the factors which influence preservation of fine structure. In Buffa, P. (ed.) Symposium on electron microscopy. Rome: Consiglio Nazionale delle Ricerche.Google Scholar
Mujer, C.V., Andrews, D.L., Manhart, J.R., Pierce, S.K. and Rumpho, M. (1996) Chloroplast genes are expressed during intracellular symbiotic association of Vaucheria litorea plastids with the sea slug Elysia chlorotica. Proceedings of the National Academy of Sciences of the United States of America 93, 12333–12338.CrossRefGoogle ScholarPubMed
Muller-Cale, K. and Kruger, E. (1913) Symbiontische Algen bei Aglaophenia helleri und Sertularella polyzonias. Mitteilungen aus derZoologische Station zu Neapel 21, 51–64.Google Scholar
Naumov, D.V. (1969) Hydroids and hydromedusae of the USSR. Jerusalem: Israel Program for Scientific Translation.Google Scholar
Omarova, E.O., Gorelova, O.A., Zenova, G.M. and Lobakova, E.S. (2008) Actinomycetes as epibionts of White Sea colonial hydroids. In Proceedings of scientific conference dedicated to the 70th anniversary of MSU White Sea Biological Station. Moscow: Grif & Co., pp. 254–259.Google Scholar
Pyataeva, S.V., Kosevich, I.A. and Lobakova, E.S. (2006a) Endosymbionts of colonial hydroids. Moscow: Trudi Belomorskoi biostantsii biologicheskogo fakulteta, MGU.Google Scholar
Pyataeva, S.V., Lobakova, E.S. and Kosevich, I.A. (2006b) Cyanobacteria—endosymbionts of colony hydroids. Moscow University Biological Sciences Bulletin 4, 34–42.Google Scholar
Reynolds, E.S. (1963) The use of the lead citrate at high pH as an electron-opaque stain in electron microscopy. Journal of Cell Biology 17, 208–212.CrossRefGoogle ScholarPubMed
Romagnoli, T., Bavestrello, G., Cucchiari, E.M., De Stefano, M., Di Camillo, C.G., Pennesi, C., Puce, S. and Totti, C. (2007) Microalgal communities epibiontic on the marine hydroid Eudendrium racemosum in the Ligurian Sea during an annual cycle. Marine Biology 151, 537–552.CrossRefGoogle Scholar
Round, F.E., Sloane, J.F., Ebling, F.J. and Kitching, J.A. (1961) The ecology of Lough Ine: the hydroid Sertularia operculata (L.) and its associated flora and fauna: effects of transference to sheltered water. Journal of Ecology 49, 617–629.CrossRefGoogle Scholar
Rumpho, M.E., Pelletreau, K.N., Moustafa, A. and Bhattacharya, D. (2011) The making of a photosynthetic animal. Journal of Experimental Biology 214, 303–311.CrossRefGoogle ScholarPubMed
Rumpho, M.E., Summer, E.J. and Manhart, J.R. (2000) Solar-powered sea slugs. Mollusc/algal chloroplast symbiosis. Plant Physiology 123, 29–38.CrossRefGoogle ScholarPubMed
Scholz, B. and Liebezeit, G. (2006) Chemical screening for bioactive substances in culture media of microalgae and cyanobacteria from marine and brackish water habitats: first results. Pharmaceutical Biology 44, 544–549.CrossRefGoogle Scholar
Semple, K.T. and Cain, R.B. (1996) Biodegradation of phenols by the alga Ochromonas danica. Applied and Environmental Microbiology 62, 1265–1273.CrossRefGoogle ScholarPubMed
Siqueiros-Beltrones, D.A., Serviere-Zaragoza, E. and Argumedo-Hernandez, U. (2001) First record of the diatom Cocconeis notata Petit living inside the hydrotheca of a hydrozoan epiphyte of Macrocystis pyrifera (L.) C. Ag. Oceanides 16, 135–138.Google Scholar
Smith, D.C. (1991) Why do so few animals form endosymbiotic associations with photosynthetic microbes? Philosophical Transactions of the Royal Society, B 333, 225–230.Google Scholar
Stabili, L., Gravili, C., Tredici, S., Piraino, S., Talà, A., Boero, F. and Alifano, P. (2008) Epibiotic Vibrio luminous bacteria isolated from some Hydrozoa and Bryozoa species. Microbial Ecology 56, 625–636.CrossRefGoogle ScholarPubMed
Stabili, L., Gravili, C., Boero, F., Tredici, S. and Alifano, P. (2010) Susceptibility to antibiotics of Vibrio sp. AO1 growing in pure culture or in association with its hydroid host Aglaophenia octodonta (Cnidaria, Hydrozoa). Microbial Ecology 59, 555–562.CrossRefGoogle ScholarPubMed
Svoboda, A. and Cornelius, P.F.S. (1991) The European and Mediterranean species of Aglaophenia (Cnidaria: Hydrozoa). Leiden, The Netherlands: Zoologische Verhandelingen.Google Scholar
Taylor, M.W., Radax, R., Steger, D. and Wagner, M. (2007) Sponge-associated microorganisms: evolution, ecology, and biotechnological potential. Microbiology and Molecular Biology Reviews 71, 295–347.CrossRefGoogle ScholarPubMed
Trench, R.K. (1993) Microalgal–invertebrate symbiosis: a review. Endocytobiosis and Cell Research 9, 135–175.Google Scholar
Unson, M.D., Holland, N.D. and Faulkner, D.J. (1994) A brominated secondary metabolite synthesized by the cyanobacterial symbiont of a marine sponge and accumulation of the crystalline metabolite in the sponge tissue. Marine Biology 119, 1–11.CrossRefGoogle Scholar
Usher, K.M. (2008) The ecology and phylogeny of cyanobacterial symbionts in sponges. Marine Ecology 29, 178–192.CrossRefGoogle Scholar
Venn, A.A., Loram, J.E. and Douglas, A.E. (2008) Photosynthetic symbioses in animals. Journal of Experimental Botany 59, 1069–1080.CrossRefGoogle ScholarPubMed
Yellowlees, D., Rees, T.A.V. and Leggat, W. (2008) Metabolic interactions between algal symbionts and invertebrate hosts. Plant, Cell and Environment 31, 679–694.CrossRefGoogle ScholarPubMed
Zaika, V.E. (1991) Simbioz vodnykh zhivotnykh s vodoroslyami. [Symbiosis of Aquatic Animals with Algae]. Kiev: Naukova Dumka. [In Russian.]Google Scholar