Hostname: page-component-586b7cd67f-rdxmf Total loading time: 0 Render date: 2024-11-26T21:18:56.891Z Has data issue: false hasContentIssue false
  • English
  • Français

The stress protein HSP70 from the marine sponge Thenea muricata

Published online by Cambridge University Press:  13 January 2016

K. Vallmann ,
C. Kivisild ,
A. Lopp ,
H.T. Rapp  and
M. Kelve
K. Vallmann*
Affiliation:
Department of Gene Technology, Tallinn University of Technology, Akadeemia tee 15, Tallinn 12618, Estonia
C. Kivisild
Affiliation:
Department of Gene Technology, Tallinn University of Technology, Akadeemia tee 15, Tallinn 12618, Estonia
A. Lopp
Affiliation:
Department of Gene Technology, Tallinn University of Technology, Akadeemia tee 15, Tallinn 12618, Estonia
H.T. Rapp
Affiliation:
Department of Biology and Centre for Geobiology, University of Bergen, Thormøhlensgate 53A, N-5020 Bergen, Norway
M. Kelve
Affiliation:
Department of Gene Technology, Tallinn University of Technology, Akadeemia tee 15, Tallinn 12618, Estonia
*
Correspondence should be addressed to:K. Vallmann, Department of Gene Technology, Tallinn University of Technology, Akadeemia tee 15, Tallinn 12618, Estonia email: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

The members of the heat shock protein 70 ( HSP70) family are among the most conserved and widely studied stress proteins. The transcription and translation levels of HSP70 genes have also been studied in several marine and freshwater sponges as molecular markers to characterize the response of sponges to various types of physiological or environmental stress conditions. Furthermore, HSP70 protein sequences have been used in phylogenetic analysis of prokaryotes and eukaryotes. In this study, the expression of HSP70 genes in the marine sponge Thenea muricata during long-term cultivation under laboratory conditions was described at the protein and mRNA levels. Though there are many studies about distribution and morphology of T. muricata, few biochemical and molecular data can be found in the literature. HSP70 gene data for several sponge species have been deposited in the NCBI database, however, those for T. muricata are not available. Therefore, HSP70 genes were characterized in this sponge. Several proteins of the HSP70 superfamily which might be induced by stress, were present in T. muricata.

Keywords

Environmental stressHSP70Thenea muricatamarine spongelong-term cultivation
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 96 , Issue 2: Proceedings of the 9th World Sponge Conference held in Fremantle Australia in 2013: New Frontiers in Sponge Science , March 2016 , pp. 573 - 581
Copyright
Copyright © Marine Biological Association of the United Kingdom 2016 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Agell, G., Uriz, M.J., Cebrian, E. and Martí, R. (2001) Does stress protein induction by copper modify natural toxicity in sponges? Environmental Toxicology and Chemistry 20, 2588–2593.CrossRefGoogle ScholarPubMed
Bairoch, A. (1992) PROSITE: a dictionary of sites and patterns in proteins. Nucleic Acids Research 20, 2013–2018.CrossRefGoogle ScholarPubMed
Bakke, T., Klungsøyr, J. and Sanni, S. (2013) Environmental impacts of produced water and drilling waste discharges from the Norwegian offshore petroleum industry. Marine Environmental Research 92, 154–169.CrossRefGoogle ScholarPubMed
Bardwell, J.C. and Craig, E.A. (1984) Major heat shock gene of Drosophila and the Escherichia coli heat-inducible dnaK gene are homologous. Proceedings of the National Academy of Sciences USA 81, 848–852.CrossRefGoogle ScholarPubMed
Batel, R., Bihari, N., Rinkevich, B., Dapper, J., Schacke, H., Schroder, H.C. and Müller, W.E.G. (1993) Modulation of organotin-induced apoptosis by the water pollutant methyl mercury in a human lymphoblastoid tumor cell line and a marine sponge. Marine Ecology Progress Series 93, 245–251.CrossRefGoogle Scholar
Borchiellini, C., Boury-Esnault, N., Vacelet, J. and Le Parco, Y. (1998) Phylogenetic analysis of the Hsp70 sequences reveals the monophyly of Metazoa and specific phylogenetic relationships between animals and fungi. Molecular Biology and Evolution 15, 647–655.CrossRefGoogle ScholarPubMed
Bradford, M.M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72, 248–254.CrossRefGoogle ScholarPubMed
Brocchieri, L., Conway de Macario, E. and Macario, A.J.L. (2008) hsp70 genes in the human genome: conservation and differentiation patterns predict a wide array of overlapping and specialized functions. BMC Evolutionary Biology 8, 19.CrossRefGoogle ScholarPubMed
Buchberger, A., Bukau, B. and Sommer, T. (2010) Protein quality control in the cytosol and the endoplasmic reticulum: brothers in arms. Molecular Cell 40, 238–252.CrossRefGoogle Scholar
Cárdenas, P. and Rapp, H.T. (2012) A review of Norwegian streptaster-bearing Astrophorida (Porifera: Demospongiae: Tetractinellida), new records and a new species. Zootaxa 3253, 1–53.CrossRefGoogle Scholar
Cárdenas, P., Xavier, J.R., Reveillaud, J., Schander, C. and Rapp, H.T. (2011) Molecular phylogeny of the Astrophorida (Porifera, Demospongiae(p)) reveals an unexpected high level of spicule homoplasy. PLoS ONE 6, e18318.CrossRefGoogle ScholarPubMed
Cebrian, E., Agell, G., Martí, R. and Uriz, M.J. (2006) Response of the Mediterranean sponge Chondrosia reniformis Nardo to copper pollution. Environmental Pollution 141, 452–458.CrossRefGoogle ScholarPubMed
Conaco, C., Neveu, P., Zhou, H., Arcila, M.L., Degnan, S.M., Degnan, B.M. and Kosik, K.S. (2012) Transcriptome profiling of the demosponge Amphimedon queenslandica reveals genome-wide events that accompany major life cycle transitions. BMC Genomics 13, 209.CrossRefGoogle ScholarPubMed
Dereeper, A., Guignon, V., Blanc, G., Audic, S., Buffet, S., Chevenet, F., Dufayard, J.F., Guindon, S., Lefort, V., Lescot, M., Claverie, J.M. and Gascuel, O. (2008) Phylogeny.fr: robust phylogenetic analysis for the non-specialist. Nucleic Acids Research 36, W465–W469.CrossRefGoogle ScholarPubMed
Efremova, S.M., Margulis, B.A., Guzhova, I.V., Itskovich, V.B., Lauenroth, S., Müller, W.E.G. and Schröder, H.C. (2002) Heat shock protein Hsp70 expression and DNA damage in Baikalian sponges exposed to model pollutants and wastewater from Baikalsk Pulp and Paper Plant. Aquatic Toxicology 57, 267–280.CrossRefGoogle ScholarPubMed
Fan, L., Liu, M., Simister, R., Webster, N.S. and Thomas, T. (2013) Marine microbial symbiosis heats up: the phylogenetic and functional response of a sponge holobiont to thermal stress. ISME Journal 7, 991–1002.CrossRefGoogle ScholarPubMed
Fan, L., Reynolds, D., Liu, M., Stark, M., Kjelleberg, S., Webster, N. and Thomas, T. (2012) Functional equivalence and evolutionary convergence in complex communities of microbial sponge symbionts. Proceedings of the National Academy of Sciences USA 109, E1878–1887.CrossRefGoogle ScholarPubMed
Feder, M.E. and Hofmann, G.E. (1999) Heat-shock proteins, molecular chaperones, and the stress response: evolutionary and ecological physiology. Annual Review of Physiology 61, 243–282.CrossRefGoogle ScholarPubMed
Filiciotto, F., Vazzana, M., Celi, M., Maccarrone, V., Ceraulo, V.M., Buffa, C., Di Stefano, V., Mazzola, S. and Buscaino, G. (2014) Behavioural and biochemical stress responses of Palinurus elephas after exposure to boat noise pollution in tank. Marine Pollution Bulletin 84, 104–114.CrossRefGoogle ScholarPubMed
Gupta, R.S., Aitken, K., Falah, M. and Singh, B. (1994) Cloning of Giardia lamblia heat shock protein HSP70 homologs: implications regarding origin of eukaryotic cells and of endoplasmic reticulum. Proceedings of the National Academy of Sciences USA 91, 2895–2899.CrossRefGoogle ScholarPubMed
Hendrick, J.P. and Hartl, F. (1993) Molecular chaperone functions of heat-shock proteins. Annual Review of Biochemistry 62, 349–384.CrossRefGoogle ScholarPubMed
Koziol, C., Kobayashi, N., Müller, I.M. and Müller, W.E.G. (1998) Cloning of sponge heat shock proteins: evolutionary relationships between the major kingdoms. Journal of Zoological Systematics and Evolutionary Research 36, 101–109.CrossRefGoogle Scholar
Koziol, C., Leys, S.P., Müller, I.M. and Müller, W.E.G. (1997) Cloning of Hsp70 genes from the marine sponges Sycon raphanus (Calcarea) and Rhabdocalyptus dawsoni (Hexactinellida). An approach to solve the phylogeny of sponges. Biological Journal of the Linnean Society 62, 581–592.Google Scholar
Koziol, C., Wagner-Hülsmann, C., Mikoc, A., Gamulin, V., Kruse, M., Pancer, Z., Schäcke, H. and Müller, W.E.G. (1996) Cloning of a heat-inducible biomarker, the cDNA encoding the 70 kDa heat shock protein, from the marine sponge Geodia cydonium: response to natural stressors. Marine Ecology Progress Series 136, 153–161.CrossRefGoogle Scholar
Kregel, K.C. (2002) Heat shock proteins: modifying factors in physiological stress responses and acquired thermotolerance. Journal of Applied Physiology 92, 2177–2186.CrossRefGoogle ScholarPubMed
Laemmli, U.K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680–685.CrossRefGoogle ScholarPubMed
Lafferty, K.D., Porter, J.W. and Ford, S.E. (2004) Are diseases increasing in the ocean? Annual Reviews in Ecology, Evolution and Systematics 35, 31–54.CrossRefGoogle Scholar
Lee, A.S. (2014) Glucose-regulated proteins in cancer: molecular mechanisms and therapeutic potential. Nature Reviews Cancer 14, 263–276.CrossRefGoogle ScholarPubMed
López-Legentil, S., Song, B., McMurray, S.E. and Pawlik, J.R. (2008) Bleaching and stress in coral reef ecosystems: hsp70 expression by the giant barrel sponge Xestospongia muta. Molecular Ecology 17, 1840–1849.CrossRefGoogle ScholarPubMed
Lopp, A., Reintamm, T., Kuusksalu, A., Tammiste, I., Pihlak, A. and Kelve, M. (2010) Natural occurrence of 2′,5′-linked heteronucleotides in marine sponges. Marine Drugs 8, 235–254.CrossRefGoogle ScholarPubMed
Mayer, M.P. and Bukau, B. (2005) Hsp70 chaperones: cellular functions and molecular mechanism. Cellular and Molecular Life Sciences 62, 670–684.CrossRefGoogle ScholarPubMed
Müller, W.E.G., Batel, R., Lacorn, M., Steinhart, H., Simat, T., Lauenroth, S., Hassanein, H. and Schröder, H.C. (1998) Accumulation of cadmium and zinc in the marine sponge Suberites domuncula and its potential consequences on single-strand breaks and on expression of heat-shock protein: a natural field study. Marine Ecology Progress Series 167, 127–135.CrossRefGoogle Scholar
Müller, W.E.G., Koziol, C., Dapper, J., Kurelec, B., Batel, R. and Rinkevich, B. (1995) Combinatory effects of temperature stress and nonionic organic pollutants on stress protein (hsp70) gene expression in the freshwater sponge Ephydatia fluviatilis. Environmental Toxicology and Chemistry 14, 1203–1208.Google Scholar
Munro, S. and Pelham, H.R.B. (1987) A C-terminal signal prevents secretion of luminal ER proteins. Cell 48, 899–907.CrossRefGoogle ScholarPubMed
Rensing, S.A. and Maier, U.G. (1994) Phylogenetic analysis of the stress-70 protein family. Journal of Molecular Evolution 39, 80–86.CrossRefGoogle ScholarPubMed
Rossi, S. and Snyder, M.J. (2001) Competition for space among sessile marine invertebrates: changes in HSP70 expression in two Pacific cnidarians. Biological Bulletin 201, 385–393.CrossRefGoogle ScholarPubMed
Sambrook, J. and Russell, D.W. (2001) Preparation of plasmid DNA by alkaline lysis with SDS: minipreparation. In Argentine, J., Irwin, N. et al. (eds) Molecular cloning: a laboratory manual. Volume 1. 3rd edition. New York, NY: Cold Spring Harbor Laboratory Press, pp. 1.32–1.34.Google Scholar
Sanders, B.M. (1993) Stress proteins in aquatic organisms: an environmental perspective. Critical Reviews in Toxicology 23, 49–75.CrossRefGoogle ScholarPubMed
Saraste, M., Sibbald, P.R. and Wittinghofer, A. (1990) The P-loop – a common motif in ATP- and GTP-binding proteins. Trends in Biochemical Sciences 15, 430–434.CrossRefGoogle ScholarPubMed
Schill, R.O., Pfannkuchen, M., Fritz, G., Köhler, H.R. and Brümmer, F. (2006) Quiescent gemmules of the freshwater sponge, Spongilla lacustris (Linnaeus, 1759), contain remarkably high levels of Hsp70 stress protein and hsp70 stress gene mRNA. Journal of Experimental Zoology Part A: Comparative Experimental Biology 305A, 449–457.CrossRefGoogle Scholar
Schippers, K.J., Sipkema, D., Osinga, R., Smidt, H., Pomponi, S.A., Martens, D.E. and Wijffels, R.H. (2012) Cultivation of sponges, sponge cells and symbionts: achievements and future prospects. Advantages in Marine Biology 62, 273–337.CrossRefGoogle ScholarPubMed
Schröder, H.C., Batel, R., Lauenroth, S., Hassanein, H.M.A., Lacorn, M., Simat, T., Steinhart, H. and Müller, W.E.G. (1999) Induction of DNA damage and expression of heat shock protein HSP70 by polychlorinated biphenyls in the marine sponge Suberites domuncula Olivi. Journal of Experimental Marine Biology and Ecology 233, 285–300.CrossRefGoogle Scholar
Srivastava, M., Simakov, O., Chapman, J., Fahey, B., Gauthier, M.E., Mitros, T., Richards, G.S., Conaco, C., Dacre, M., Hellsten, U., Larroux, C., Putnam, N.H., Stanke, M., Adamska, M., Darling, A., Degnan, S.M., Oakley, T.H., Plachetzki, D.C., Zhai, Y., Adamski, M., Calcino, A., Cummins, S.F., Goodstein, D.M., Harris, C., Jackson, D.J., Leys, S.P., Shu, S., Woodcroft, B.J., Vervoort, M., Kosik, K.S., Manning, G., Degnan, B.M. and Rokhsar, D.S. (2010) The Amphimedon queenslandica genome and the evolution of animal complexity. Nature 466, 720–726.CrossRefGoogle ScholarPubMed
Trannum, H.C., Nilsson, H.C., Schaanning, M.T. and Øxnevad, S. (2010) Effects of sedimentation from water-based drill cuttings and natural sediment on benthic macrofaunal community structure and ecosystem processes. Journal of Experimental Marine Biology and Ecology 383, 111–121.CrossRefGoogle Scholar
Trefry, J.H., Dunton, K.H., Trocine, R.P., Schonberg, S.V., McTigue, N.D., Hersh, E.S. and McDonald, T.J. (2013) Chemical and biological assessment of two offshore drilling sites in the Alaskan Arctic. Marine Environmental Research 86, 35–45.CrossRefGoogle ScholarPubMed
Tsukahara, F., Yoshioka, T. and Muraki, T. (2000) Molecular and functional characterization of HSC54, a novel variant of human heat-shock cognate protein 70. Molecular Pharmacology 58, 1257–1263.CrossRefGoogle ScholarPubMed
Webster, N., Pantile, R., Botté, E., Abdo, D., Andreakis, N. and Whalan, S. (2013) A complex life cycle in a warming planet: gene expression in thermally stressed sponges. Molecular Ecology 22, 1854–1868.CrossRefGoogle Scholar
Witte, U. and Graf, G. (1996) Metabolism of deep-sea sponges in the Greenland-Norwegian Sea. Journal of Experimental Marine Biology and Ecology 198, 223–235.CrossRefGoogle Scholar
Supplementary material: File

Vallmann supplementary material

Appendix 1

Download Vallmann supplementary material(File)
File 133.1 KB
Supplementary material: File

Vallmann supplementary material

Appendix 2

Download Vallmann supplementary material(File)
File 26.6 KB
Supplementary material: File

Vallmann supplementary material

Appendix 3

Download Vallmann supplementary material(File)
File 365.6 KB
Supplementary material: File

Vallmann supplementary material

Appendix 4

Download Vallmann supplementary material(File)
File 35.8 KB