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Characterization of Leucetta prolifera, a calcarean cyanosponge from south-western Australia, and its symbionts

Published online by Cambridge University Press:  08 September 2015

Jane Fromont
Affiliation:
Department of Aquatic Zoology, Western Australian Museum, Locked Bag 49, Welshpool DC, WA 6986, Australia
Megan J. Huggett
Affiliation:
Centre for Marine Ecosystems Research, School of Natural Sciences, Edith Cowan University, 270 Joondalup Drive, Joondalup WA 6027, Australia
Sabine K. Lengger
Affiliation:
Department of Chemistry, WA Organic and Isotope Geochemistry Centre, The Institute for Geoscience Research, Curtin University, GPO Box U1987, Perth, WA 6845, Australia
Kliti Grice
Affiliation:
Department of Chemistry, WA Organic and Isotope Geochemistry Centre, The Institute for Geoscience Research, Curtin University, GPO Box U1987, Perth, WA 6845, Australia
Christine H.L. Schönberg*
Affiliation:
Department of Aquatic Zoology, Western Australian Museum, Locked Bag 49, Welshpool DC, WA 6986, Australia Australian Institute of Marine Science, Oceans Institute, 39 Fairway, Crawley, WA 6009, Australia
*
Correspondence should be addressed to:C.H.L. Schönberg, Oceans Institute at the University of Western Australia, 35 Stirling Highway, Crawley, WA 6009, Australia email: christine.schonberg@uwa.edu.au

Abstract

The biology and ecology of calcarean sponges are not as well understood as they are for demosponges. Here, in order to gain new insights, particularly about symbiotic relationships, the calcarean sponge Leucetta prolifera was sampled from south-western Australia and examined for its assumed photosymbionts. Pulse amplitude modulated fluorometry and extraction of photopigments established that the sponge was photosynthetic. Molecular analysis of the bacterial symbionts via sequencing of the V1–V3 region of the 16S rDNA gene confirmed that between 5 and 22% of all sequences belonged to the phylum Cyanobacteria, depending on the individual sample, with the most dominant strain aligning with Hormoscilla spongeliae, a widely distributed sponge symbiont. Analysis of fatty acids suggested that the sponge obtains nutrition through photosynthates from its symbionts. The relationship is assumed to be mutualistic, with the sponge receiving dietary support and the cyanobacteria sheltering in the sponge tissues. We list all Calcarea presently known to harbour photosymbionts.

Type
Research Article
Copyright
Copyright © Marine Biological Association of the United Kingdom 2015 

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References

REFERENCES

Bavestrello, G., Arillo, A., Calcinai, B., Cattaneo-Vietti, R., Cerrano, C., Gaino, E., Penna, A. and Sarà, M. (2000) Parasitic diatoms inside Antarctic sponges. Biological Bulletin 198, 2933.CrossRefGoogle ScholarPubMed
Bligh, E.G. and Dyer, W.J. (1959) A rapid method of total lipid extraction and purification. Canadian Journal of Biochemistry and Physiology 37, 911917.CrossRefGoogle ScholarPubMed
Burlando, B., Sabatini, M.A. and Gaino, E. (1988) Association between calcareous Clathrina cerebrum (Haeckel) and bacteria: electron microscope study. Journal of Experimental Marine Biology and Ecology 116, 3542.CrossRefGoogle Scholar
Cárdenas, P. and Rapp, H.T. (2013) Disrupted spiculogenesis in deep-water Geodiidae (Porifera, Demospongiae) growing in shallow waters. Invertebrate Biology 132, 173194.CrossRefGoogle Scholar
Caroppo, C., Albertano, P., Bruno, L., Montinari, M., Rizzi, M., Vigliotta, G. and Pagliara, P. (2012) Identification and characterization of a new Halomicronema species (Cyanobacteria) isolated from the Mediterranean marine sponge Petrosia ficiformis (Porifera). Fottea, Olomouc 12, 315326.CrossRefGoogle Scholar
Carter, H.J. (1878) On Teichonia, a new family of calcareous sponges with description of two species. Annals and Magazine of Natural History 2, 3540.CrossRefGoogle Scholar
Cerrano, C., Arillo, A., Bavestrello, G., Calcinai, B., Cattaneo-Vietti, R., Penna, A., Sarà, M. and Totti, C. (2000) Diatom invasion in the Antarctic hexactinellid sponge Scolymastra joubini. Polar Biology 23, 441444.CrossRefGoogle Scholar
Cerrano, C., Calcinai, B., Cucchiari, E., Di Camillo, C., Totti, C. and Bavestrello, G. (2004) The diversity of relationships between Antarctic sponges and diatoms: the case of Mycale acerata Kirkpatrick 1907 (Porifera, Demospongiae). Polar Biology 27, 231237.CrossRefGoogle Scholar
Chikaraishi, Y., Tanaka, R., Tanaka, A. and Ohkouchi, N. (2009) Fractionation of hydrogen isotopes during phytol biosynthesis. Organic Geochemistry 40, 569573.CrossRefGoogle Scholar
Cohen, Z. and Vonshak, A. (1991) Fatty acid composition of Spirulina and Spirulina-like cyanobacteria in relation to their chemotaxonomy. Phytochemistry 30, 205206.CrossRefGoogle Scholar
D'Ambrosio, M., Tato, M., Pocsfalvi, G., Debitus, C. and Pietra, F. (1999) Leucascandrolide B, a new 16-membered, extensively methyl-branched polyoxygenated macrolide from the calcareons sponge Leucascandra caveolata from northeastern waters of New Caledonia. Helvetica Chimica Acta 82, 347353.3.0.CO;2-9>CrossRefGoogle Scholar
Dawson, D., Grice, K., Edwards, D.S. and Alexander, R. (2007) The effect of source and maturity on the stable isotopic compositions of individual hydrocarbons in sediments and crude oils from the Vulcan Sub-basin, Timor Sea, Northern Australia. Organic Geochemistry 38, 10151038.CrossRefGoogle Scholar
DeSantis, T.Z., Hugenholtz, P., Larsen, N., Rojas, M., Brodie, E.L., Keller, K., Huber, T., Dalevi, D., Hu, P. and Andersen, G.L. (2006) Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Applied and Environmental Microbiology 72, 50695072.CrossRefGoogle ScholarPubMed
Díaz, M.C. (1999) Perspectives on sponge-cyanobacterial symbioses. Memoirs of the Queensland Museum 44, 154.Google Scholar
Díaz, M.C., Thacker, R.W., Rützler, K. and Piantoni, C. (2007) Two new haplosclerid sponges from Caribbean Panama with symbiotic filamentous cyanobacteria, and an overview of sponge-cyanobacteria associations. In Custódio, M.R., Hajdu, E., Lôbo-Hajdu, G. and Muricy, G. (eds) Porifera research: biodiversity, innovation and sustainability. Rio de Janeiro: Museu Nacional, pp. 3139.Google Scholar
Duclaux, G.N. (1977) Recherches sur quelques associations symbiotiques d'algues et de métazoaires. PhD thesis. Université Pierre et Marie Curie, Paris, 292 pp.Google Scholar
Edgar, R.C., Haas, B.J., Clemente, J.C., Quince, C. and Knight, R. (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27, 21942200.CrossRefGoogle ScholarPubMed
Eichner, M., Rost, B. and Kranz, S.A. (2014) Diversity of ocean acidification effects on marine N-2 fixers. Journal of Experimental Marine Biology and Ecology 457, 199207.CrossRefGoogle Scholar
Erwin, P.M. and Thacker, R.W. (2007) Incidence and identity of photosynthetic symbionts in Caribbean coral reef sponge assemblages. Journal of the Marine Biological Association of the United Kingdom 87, 16831692.CrossRefGoogle Scholar
Feldmann, J. (1933) Sur quelques cyanophycées vivant dans le tissue des éponges. Archives de Zoologie Experimentale et Générale 75, 331404.Google Scholar
Fromont, J., Vanderklift, M. and Klautau, M. (2013) Sessile fauna of a temperate, shallow water Western Australian environment. Conference Abstracts of the Ninth World Sponge Conference, Fremantle, Western Australia 8384. Available at http://www.aims.gov.au/web/sponge/home.Google Scholar
Gao, Z.-M., Wang, Y., Lee, O.O., Tian, R.-M., Wong, Y.H., Bougouffa, S., Batang, Z., Al-Suwailem, A., Lafi, F.F., Bajic, V.B. and Qian, P.-Y. (2014) Pyrosequencing reveals the microbial communities in the Red Sea sponge Carteriospongia foliascens and their impressive shifts in abnormal tissues. Microbial Ecology 68, 621632.CrossRefGoogle ScholarPubMed
Grice, K., Klein Breteler, W.C., Schouten, S., Grossi, V., De Leeuw, J.W. and Sinninghe-Damsté, J.S. (1998) The effects of zooplankton herbivory on biomarker proxy records. Paleoceanography 13, 686693.CrossRefGoogle Scholar
Grice, K., Lu, H., Zhou, Y., Stuart-Williams, H. and Farquhar, G.D. (2008) Biosynthetic and environmental effects on the stable carbon isotopic compositions of anteiso- (3-methyl) and iso- (2-methyl) alkanes in tobacco leaves. Phytochemistry 69, 28072814.CrossRefGoogle ScholarPubMed
Guckert, J., Antworth, C.P., Nichols, P.D. and White, D.C. (1985) Phospholipid, ester-linked fatty acid profiles as reproducible assays for changes in prokaryotic community structure of estuarine sediments. Federation of European Microbiological Societies Microbiology Letters 31, 147158.CrossRefGoogle Scholar
Guiry, M.D. and Guiry, G.M. (2014) AlgaeBase. Galway: National University of Ireland, World-wide electronic publication, available at: http://www.algaebase.org (last visited on 12 November 2014).Google Scholar
Heinzelmann, S.M., Bale, N.J., Hopmans, E.C., Sinninghe Damste, J.S., Schouten, S. and van der Meer, M.T.J. (2014) Critical assessment of glyco- and phospholipid separation by using silica chromatography. Applied and Environmental Microbiology 80, 360365.CrossRefGoogle ScholarPubMed
Hentschel, U., Usher, K.M. and Taylor, M.W. (2006) Marine sponges as microbial fermenters. Federation of European Microbiological Societies Microbiology Ecology 55, 167177.CrossRefGoogle ScholarPubMed
Hill, M. and Hill, A. (2012) The magnesium inhibition and arrested phagosome hypotheses: new perspectives on the evolution and ecology of Symbiodinium symbioses. Biological Reviews 87, 804821.Google Scholar
Kaneda, T. (1991) Iso- and anteiso-fatty acids in bacteria: biosynthesis, function, and taxonomic significance. Microbiology and Molecular Biology Reviews 55, 288302.Google ScholarPubMed
Kartika, R. (2008) Programs towards tetrahydropyran containing small macrolides of cyanobacterial origins: synthetic methodology development and total synthesis. PhD thesis. University of Notre Dame, Fremantle, Australia, 605 pp.Google Scholar
Kozich, J.J., Westcott, S.L., Baxter, N.T., Highlander, S.K. and Schloss, P.D. (2013) Development of a dual-index sequencing strategy and curation pipeline for analyzing amplicon sequence data on the MiSeq Illumina sequencing platform. Applied and Environmental Microbiology 79, 51125120.CrossRefGoogle ScholarPubMed
Lemloh, M.-L., Fromont, J., Brümmer, F. and Usher, K.M. (2009) Diversity and abundance of photosynthetic sponges in temperate Western Australia. BioMed Central Ecology 9, 4 (13 pp).Google ScholarPubMed
Lengger, S.K., Hopmans, E.C., Sinninghe Damsté, J.S. and Schouten, S. (2012) Comparison of extraction and work up techniques for analysis of core and intact polar tetraether lipids from sedimentary environments. Organic Geochemistry 47, 3440.CrossRefGoogle Scholar
Letunic, I. and Bork, P. (2006) Interactive Tree Of Life (iTOL): an online tool for phylogenetic tree display and annotation. Bioinformatics 23, 127128.CrossRefGoogle ScholarPubMed
Letunic, I. and Bork, P. (2011) Interactive Tree Of Life v2: online annotation and display of phylogenetic trees made easy. Nucleic Acids Research 39(Suppl. 2), W475W478.CrossRefGoogle ScholarPubMed
Ludwig, W., Strunk, O., Westram, R., Richter, L., Meier, H., Yadhukumar, Buchner A., Lai, T., Steppi, S., Jobb, G., Förster, W., Brettske, I., Gerber, S., Ginhart, A.W., Gross, O., Grumann, S., Hermann, S., Jost, R., König, A., Liss, T., Lüßmann, R., May, M., Nonhoff, B., Reichel, B., Strehlow, R., Stamataki, A., Stuckman, N., Vilbig, A., Lenke, M., Ludwig, T., Bode, A. and Schleifer, K.H. (2004) ARB: a software environment for sequence data. Nucleic Acids Research 32, 13631371.CrossRefGoogle ScholarPubMed
Osburn, M.R., Sessions, A.L., Pepe-Ranney, C. and Spear, J.R. (2011) Hydrogen-isotopic variability in fatty acids from Yellowstone National Park hot spring microbial communities. Geochimica et Cosmochimica Acta 75, 48304845.CrossRefGoogle Scholar
Pape, T. (2004) Lipidbiomarker schwammassoziierter Bakterien und Archaeen. PhD thesis. Hamburg University, Hamburg, Germany, 194 pp.Google Scholar
Perea-Blázquez, A., Price, K., Davy, S.K. and Bell, J.J. (2010) Diet composition of two temperate calcareous sponges: Leucosolenia echinata and Leucetta sp. from the Wellington South Coast, New Zealand. Open Marine Biology Journal 4, 6573.CrossRefGoogle Scholar
Peterson, D.G., Dahllöf, I. and Nielsen, L.P. (2004) Effects of zinc pyrithione and copper pyrithione on microbial community structure in sediments. Environmental Toxicology and Chemistry 23, 921928.CrossRefGoogle Scholar
Pruesse, E., Peplies, J. and Glöckner, F.O. (2012) SINA: accurate high-throughput multiple sequence alignment of ribosomal RNA genes. Bioinformatics 28, 18231829.CrossRefGoogle ScholarPubMed
Rossi, A.L., de Moraes Russo, C.A., Solé-Cava, A.M., Rapp, H.T. and Klautau, M. (2011) Phylogenetic signal in the evolution of body colour and spicule skeleton in calcareous sponges. Zoological Journal of the Linnean Society 163, 10261034.CrossRefGoogle Scholar
Schönberg, C.H.L. and Loh, W.K.W. (2005) Molecular identity of the unique symbiotic dinoflagellates found in the bioeroding demosponge Cliona orientalis. Marine Ecology Progress Series 299, 157166.CrossRefGoogle Scholar
Schouten, S., Klein Breteler, W.C., Blokker, P., Schogt, N., Rijpstra, W.I., Grice, K., Baas, M. and Sinninghe-Damsté, J.S. (1998) Biosynthetic effects on the stable carbon isotopic compositions of algal lipids: implications for deciphering the carbon isotopic biomarker record. Geochimica et Cosmochimica Acta 62, 13971406.CrossRefGoogle Scholar
Schreiber, A., Wörheide, G. and Thiel, V. (2006) The fatty acids of calcareous sponges (Calcarea, Porifera). Chemistry and Physics of Lipids 143, 2937.CrossRefGoogle ScholarPubMed
Simister, R.L., Deines, P., Botté, E.S., Webster, N.S. and Taylor, M.W. (2012) Sponge-specific clusters revisited: a comprehensive phylogeny of sponge-associated microorganisms. Environmental Microbiology 14, 517524.CrossRefGoogle ScholarPubMed
Thacker, R.W. and Freeman, C.J. (2012) Sponge-microbe symbioses: recent advances and new directions. In Becerro, M.A., Uriz, M.J., Maldonado, M. and Turon, X. (eds) Advances in marine biology. Advances in sponge science, physiology, chemical and microbial diversity, biotechnology. London: Academic Press, pp. 57182.Google Scholar
Usher, K.M. (2008) The ecology and phylogeny of cyanobacterial symbionts in sponges. Marine Ecology 29, 178192.CrossRefGoogle Scholar
Van der Meer, M.T.J., Schouten, S., Sinninghe Damste, J.S., de Leeuw, J.W. and Ward, D.M. (2003) Compound-specific isotopic fractionation patterns suggest different carbon metabolisms among Chloroflexus-like bacteria in hot-spring microbial mats. Applied and Environmental Microbiology 69, 60006006.CrossRefGoogle ScholarPubMed
Van Dongen, B., Schouten, S. and Sinninghe Damsté, J. (2002) Carbon isotope variability in monosaccharides and lipids of aquatic algae and terrestrial plants. Marine Ecology Progress Series 232, 8392.CrossRefGoogle Scholar
Vicente, V. (1990) Response of sponges with autotrophic symbionts during the coral bleaching episode in Puerto Rico. Coral Reefs 8, 99202.CrossRefGoogle Scholar
Wang, Q., Garrity, G.M., Tiedje, J.M. and Cole, J.R. (2007) Naïve Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Applied and Environmental Microbiology 73, 52615267.CrossRefGoogle ScholarPubMed
Webster, N.S. and Taylor, M.W. (2012) Marine sponges and their microbial symbionts: love and other relationships. Environmental Microbiology 14, 335346.CrossRefGoogle ScholarPubMed
Wellburn, A.R. (1994) The spectral determination of chlorophylls a and b, as well as total carotenoids, using various solvents with spectrophotometers of different resolution. Journal of Plant Physiology 144, 307–131.CrossRefGoogle Scholar
Wilkinson, C.R. (1978a) Microbial associations in sponges. I. Ecology, physiology and microbial populations of coral reef sponges. Marine Biology 49, 161167.CrossRefGoogle Scholar
Wilkinson, C.R. (1978b) Microbial associations in sponges. III. Ultrastructure of the in situ associations in coral reef sponges. Marine Biology 49, 177185.CrossRefGoogle Scholar
Wilkinson, C.R. (1980) Cyanobacteria symbiotic in marine sponges. In Schwemmler, W. and Schenck, H.E.A. (eds) Endocytobiology, endosymbiosis and cell biology. Berlin: De Gruyter, pp. 9931002.Google Scholar
Wilkinson, C.R. (1982) Significance of sponges with cyanobacterial symbionts on Davies Reef, Great Barrier Reef. In Gomez, E.D., Birkeland, C.E., Buddemeier, R.W., Johannes, R.E., Marsh, J.A. Jr and Tsuda, R.T. (eds) Proceedings of the Fourth International Coral Reef Symposium, Marine Science Center, University of the Philippines, Manila, 18–22 May 1981, volume 2. The reef and man. Manila: Marine Science Centre, pp. 705712.Google Scholar
Wilkinson, C.R. (1983) Net primary productivity in coral reef sponges. Science 219, 410412.CrossRefGoogle ScholarPubMed
Wilkinson, C.R., Garrone, R. and Vacelet, J. (1984) Marine sponges discriminate between food bacteria and bacterial symbionts: electromicroscope radioautography and in situ evidence. Proceedings of the Royal Society London B 220, 519528.Google Scholar
Zhang, X., Gillespie, A.L. and Sessions, A.L. (2009) Large D/H variations in bacterial lipids reflect central metabolic pathways. Proceedings of the National Academy of Sciences USA 106, 1258012586.CrossRefGoogle Scholar
Zhu, P., Li, Q. and Wang, G. (2008) Unique microbial signatures of the alien Hawaiian marine sponge Suberites zeteki. Microbial Ecology 55, 406414.CrossRefGoogle ScholarPubMed