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The marine sponge Ianthella basta can recover from stress-induced tissue regression

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Abstract

Sponges often exhibit tissue regression in response to stressful conditions. This study investigated whether handling stress invoked tissue regression in Ianthella basta and assessed whether sponges could recover from this regressed tissue state. Six necrotic specimens and 12 healthy explants were collected at Orpheus Is. Australia and transported to aquarium facilities. Sponges were photographed daily and an integrated density (ID) measurement was used to quantify tissue regression. Histological samples were taken from sponge explants to compare cellular organization. Bacterial communities of regressed and recovered tissue were compared using Denaturing Gradient Gel Electrophoresis (DGGE). After 12 h both necrotic and healthy sponges displayed substantial tissue regression. However, within 72 h all sponges recovered to their original condition. The ID of the sponge tissue doubled, confirming tissue recovery in I. basta. Sponges affected by tissue regression had significantly fewer choanocyte chambers and more densely packed granulated cells than recovered sponges. DGGE revealed the same microbial symbionts in both regressed and recovered sponges. Handling stress associated with collection and transportation is sufficient to invoke tissue regression in this species, but sponges can rapidly recover. This study contributes to our understanding of how sponges respond to environmental pressures, influencing population resilience and persistence.

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References

  • Angermeier, H., J. Kamke, U. R. Abdelmohsen, G. Krohne, J. R. Pawlik, N. L. Lindquist & U. Hentschel, 2011. The pathology of sponge orange band disease affecting the Caribbean barrel sponge Xestospongia muta. FEMS Microbiology Ecology 75: 218–230.

    Article  PubMed  CAS  Google Scholar 

  • Ayling, A. L., 1983. Growth and regeneration rates in thinly encrusting Demospongiae from temperate waters. Biological Bulletin 165: 343–352.

    Article  Google Scholar 

  • Bancroft, J. D. & A. Stevens, 1990. Theory and Practice of Histological Techniques. Churchill Livingstone, Edinburgh.

    Google Scholar 

  • Barthel, D. & B. Wolfrath, 1989. Tissue sloughing in the sponge Halichondria panicea: a fouling organism prevents being fouled. Oecologia 78: 357–360.

    Article  Google Scholar 

  • Böhm, M., U. Hentschel, A. B. Friedrich, L. Fieseler, R. Steffen, V. Gamulin, C. I. Müller & W. E. G. Müller, 2001. Molecular response of the sponge Suberites domuncula to bacterial infection. Marine Biology 139: 1037–1045.

    Article  Google Scholar 

  • de Goeij, J. M., A. de Kluijver, F. C. van Duyl, J. Vacelet, R. H. Wijffels, A. F. P. M. de Goeij, J. P. M. Cleutjens & B. Schutte, 2009. Cell kinetics of the marine sponge Halisarca caerulea reveal rapid cell turnover and shedding. The Journal of Experimental Biology 212: 3892–3900.

    Article  PubMed  Google Scholar 

  • Fafanđel, M., W. E. G. Müller & R. Batel, 2003. Molecular response to TBT stress in marine sponge Suberites domuncula: proteolytical cleavage and phosphorylation of KRS_SD protein kinase. Journal of Experimental Marine Biology and Ecology 297: 239–252.

    Article  Google Scholar 

  • Fell, P. E., 1974. Diapause in the gemmules of the marine sponge, Haliclona oculata. Biological Bulletin 147: 333–351.

    Article  PubMed  CAS  Google Scholar 

  • Ferris, M. J., G. Muyzer & D. M. Ward, 1996. Denaturing gradient gel electrophoresis profiles of 16S rRNA-defined populations inhabiting a hot spring microbial mat community. Applied and Environmental Microbiology 62: 340–346.

    PubMed  CAS  Google Scholar 

  • Francis, J. C., S. Trabanino, R. J. Baerwald & F. W. Harrison, 1990. Analysis of the reduction-regeneration cycle in Ephydatia fluviatilis (Porifera: Spongillidae) with scanning electron microscopy. Transactions of the American Microscopical Society 109: 254–264.

    Article  Google Scholar 

  • Hartman, W. D., 1958. Natural history of the marine sponges of southern New England. Bulletin of the Peabody Museum of Natural History (Yale University) 12: 1–155.

    Google Scholar 

  • Hentschel, U., J. Hopke, M. Horn, A. B. Friedrich, M. Wagner, J. Hacker & B. S. Moore, 2002. Molecular evidence for a uniform microbial community in sponges from different oceans. Applied and Environmental Microbiology 68: 4431–4440.

    Article  PubMed  CAS  Google Scholar 

  • Hentschel, U., K. M. Usher & M. W. Taylor, 2006. Marine sponges as microbial fermenters. FEMS Microbiology Ecology 55: 167–177.

    Article  PubMed  CAS  Google Scholar 

  • Hughes, T. P., A. H. Baird, D. R. Bellwood, M. Card, S. R. Connolly, C. Folke, R. Grosberg, O. Hoegh-Gulberg, J. B. C. Jackson, J. Kleypas, J. Lough, P. Marshall, M. Nystrom, S. R. Palumbi, J. M. Pandolfi, B. Rosen & J. Roughgarden, 2003. Climate change, human impacts, and the resilience of coral reefs. Science 301: 929–933.

    Article  PubMed  CAS  Google Scholar 

  • Imsiecke, G., J. Munkner, B. Lorenz, N. Bachinski, W. E. G. Müller & H. C. Schroder, 1996. Inorganic polyphosphates in the developing freshwater sponge Ephydatia muelleri: effect of stress by polluted waters. Environmental Toxicology and Chemistry 15: 1329–1334.

    CAS  Google Scholar 

  • Knight, P. & P. E. Fell, 1987. Low salinity induces reversible tissue regression in the estuarine sponge Microciona prolifera (Ellis & Solander). Journal of Experimental Marine Biology and Ecology 107: 253–261.

    Article  Google Scholar 

  • Koziol, C., R. Borojevic, R. Steffen & W. E. G. Müller, 1998. Sponges (Porifera) model systems to study the shift from immortal to senescent somatic cells: the telomerase activity in somatic cells. Mechanisms of Ageing and Development 100: 107–120.

    Article  PubMed  CAS  Google Scholar 

  • Leamon, J. & P. E. Fell, 1990. Upper salinity tolerance of and salinity-induced tissue regression in the estuarine sponge Microciona prolifera. Trasactions of the American Microscopical Society 109: 265–272.

    Google Scholar 

  • Lemoine, N., N. Buell, A. Hill & M. Hill, 2007. Assessing the utility of sponge microbial symbiont communities as models to study global climate change: a case study with Halichondria bowerbanki. In Custódio, M. R., G. Lôbo-Hajdu, G. Hajdu & G. Muricy (eds), 7th International Sponge Symposium, Rio de Janeiro: 419–425.

  • Leys, S. P. & R. W. Meech, 2006. Physiology of coordination in sponges. Canadian Journal of Zoology 84: 288–306.

    Article  Google Scholar 

  • Leys, S. P., S. A. Nichols & E. D. M. Adams, 2009. Epithelia and integration in sponges. Integrative and Comparative Biology 49: 167–177.

    Article  PubMed  Google Scholar 

  • Li, C. W., J. Chen & T. E. Hua, 1998. Precambrian sponges with cellular structures. Science 279: 879–882.

    Article  PubMed  CAS  Google Scholar 

  • López-Legentil, S., B. Song, S. E. McMurray & J. R. Pawlik, 2008. Bleaching and stress in coral reef ecosystems: hsp70 expression by the giant barrel sponge Xestospongia muta. Molecular Ecology 17: 1840–1849.

    Article  PubMed  Google Scholar 

  • Louden, D., S. Whalan, E. Evans-Illidge, C. Wolff & R. de Nys, 2007. An assessment of the aquaculture potential of the tropical sponges Rhopaloeides odorabile and Coscinoderma sp. Aquaculture 270: 57–67.

    Article  Google Scholar 

  • Luter, H. M., S. Whalan & N. S. Webster, 2010. Exploring the role of microorganisms in the disease-like syndrome affecting the sponge Ianthella basta. Applied and Environmental Microbiology 76: 5736–5744.

    Article  PubMed  CAS  Google Scholar 

  • Meech, R. W., 2008. Non-neural reflexes: sponges and the origins of behavior. Current Biology 18: 70–72.

    Article  Google Scholar 

  • Müller, W. E. G., 2003. The origin of metazoan complexity: Porifera as integrated animals. Integrative and Comparative Biology 43: 3–10.

    Article  PubMed  Google Scholar 

  • Müller, W. E. G., 2006. The stem cell concept in sponges (Porifera): metazoan traits. Seminars in Cell & Developmental Biology 17: 481–491.

    Article  Google Scholar 

  • Muyzer, G., E. C. de Waal & A. G. Uitterlinden, 1993. Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA. Applied and Environmental Microbiology 59: 695–700.

    PubMed  CAS  Google Scholar 

  • Nickel, M., 2004. Kinetics and rhythm of body contractions in the sponge Tethya wilhelma (Porifera: Demospongiae). The Journal of Experimental Biology 207: 4515–4524.

    Article  PubMed  Google Scholar 

  • Olson, J. B., D. J. Gochfeld & M. Slattery, 2006. Aplysina red band syndrome: a new threat to Caribbean sponges. Diseases of Aquatic Organisms 71: 163–168.

    Article  PubMed  CAS  Google Scholar 

  • Rϋtzler, K., 1988. Mangrove sponge disease induced by cyanobacterial symbionts: failure of a primitive immune system? Diseases of Aquatic Organisms 5: 143–149.

    Article  Google Scholar 

  • Selvin, J., S. Shangmugha Priya, G. Seghal Kiran, T. Thangavelu & N. Sapna Bai, 2009. Sponge-associated marine bacteria as indicators of heavy metal pollution. Microbiological Research 164: 352–363.

    Article  PubMed  CAS  Google Scholar 

  • Simpson, T. L., 1984. The Cell Biology of Sponges. Springer-Verlag New York Inc., New York, NY.

    Book  Google Scholar 

  • Srivastava, M., O. Simakov, J. Chapman, B. Fahey, M. A. E. Gauthier, T. Mitros, G. S. Richards, C. Conaco, M. Dacre, U. Hellsten, C. Larroux, N. H. Putnam, M. Stanke, M. Adamska, A. Darling, S. M. Degnan, T. H. Oakley, D. C. Plachetzki, Y. Zhai, M. Adamski, A. Calcino, S. F. Cummins, D. M. Goodstein, C. Harris, D. J. Jackson, S. P. Leys, S. Shu, B. J. Woodcroft, M. Vervoort, K. S. Kosik, G. Manning, B. M. Degnan & D. S. Rokhsar, 2010. The Amphimedon queenslandica genome and the evolution of animal complexity. Nature 466: 720–727.

    Article  PubMed  CAS  Google Scholar 

  • StatSoft I, 2002. STATISTICA (Data Analysis Software System), Version 8. StatSoft, Tulsa.

  • Tanaka, K. & Y. Watanabe, 1984. Choanocyte differentiation and morphogenesis of choanocyte chambers in the fresh-water sponge, Ephydatia fluviatilis, after reversal of developmental arrest caused by hydroxyurea. Zoological Science 1: 561–570.

    Google Scholar 

  • Taylor, M. W., P. J. Schupp, R. de Nys, S. Kjelleberg & P. D. Steinberg, 2005. Biogeography of bacteria associated with the marine sponge Cymbastela concentrica. Environmental Microbiology 7: 419–433.

    Article  PubMed  CAS  Google Scholar 

  • Taylor, M. W., R. Radax, D. Steger & M. Wagner, 2007. Sponge-associated microorganisms: evolution, ecology, and biotechnological potential. Microbiology and Molecular Biology Reviews 71: 295–347.

    Article  PubMed  CAS  Google Scholar 

  • Thoms, C., U. Hentschel, S. Schmitt & P. Schupp, 2008. Rapid tissue reduction and recovery in the sponge Aplysinella sp. Marine Biology 156: 141–153.

    Article  Google Scholar 

  • Vacelet, J. & C. Donadey, 1977. Electron microscope study of the association between some sponges and bacteria. Journal of Experimental Marine Biology and Ecology 30: 301–314.

    Article  Google Scholar 

  • Webster, N. S., & M. Taylor, 2011. Marine sponges and their microbial symbionts: love and other relationships. Environmental Microbiology. doi:10.1111/j.1462-2920.2011.02460.x.

  • Webster, N. S., R. I. Webb, M. J. Ridd, R. T. Hill & A. P. Negri, 2001. The effects of copper on the microbial community of a coral reef sponge. Environmental Microbiology 3: 19–31.

    Article  PubMed  CAS  Google Scholar 

  • Webster, N. S., R. E. Cobb & A. P. Negri, 2008a. Temperature thresholds for bacterial symbiosis with a sponge. ISME Journal 2: 830–842.

    Article  PubMed  CAS  Google Scholar 

  • Webster, N. S., J. R. Xavier, M. Freckelton, C. A. Motti & R. Cobb, 2008b. Shifts in microbial and chemical patterns within the marine sponge Aplysina aerophoba during a disease outbreak. Environmental Microbiology 10: 3366–3376.

    Article  PubMed  CAS  Google Scholar 

  • Wulff, J. L., 2006. Rapid diversity and abundance decline in a Caribbean coral reef sponge community. Biological Conservation 127: 167–176.

    Article  Google Scholar 

  • Wulff, J., 2010. Regeneration of sponges in ecological context: is regeneration an integral part of life history and morphological strategies? Integrative and Comparative Biology 50: 494–505.

    Article  PubMed  Google Scholar 

  • Zar, J. H., 1999. Biostatistical Analysis. Prentice Hall, New Jersey.

    Google Scholar 

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Acknowledgments

This study was supported by an Australian Institute of Marine Science @ James Cook University and a Marine and Tropical Science Research Facility postgraduate award to Heidi Luter. We thank Rocky de Nys for his support, Brandon Luter for his assistance with the processing of histology samples and Andrew Negri for his assistance with the photograph analysis. We also thank Jasper de Goeij and an anonymous reviewer for their helpful editorial comments.

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Correspondence to Heidi M. Luter.

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Guest editors: M. Maldonado, X. Turon, M. A. Becerro & M. J. Uriz / Ancient animals, new challenges: developments in sponge research

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Luter, H.M., Whalan, S. & Webster, N.S. The marine sponge Ianthella basta can recover from stress-induced tissue regression. Hydrobiologia 687, 227–235 (2012). https://doi.org/10.1007/s10750-011-0887-x

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