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First insights into the biochemistry of Sabella spallanzanii (Annelida: Polychaeta) mucus: a potentially unexplored resource for applicative purposes

Published online by Cambridge University Press:  14 July 2010

Loredana Stabili ,
Roberto Schirosi ,
Angela Di Benedetto ,
Alessandro Merendino ,
Luciano Villanova  and
Adriana Giangrande
Loredana Stabili*
Affiliation:
Istituto per l'Ambiente Marino Costiero, Sezione di Taranto Dipartimento di Scienze e Tecnologie Biologiche ed Ambientali, Università del Saliento, 73100 (Lecce), Italy
Roberto Schirosi
Affiliation:
Istituto per l'Ambiente Marino Costiero, Sezione di Taranto
Angela Di Benedetto
Affiliation:
Dipartimento di Chimica e CIRCC, Università degli Studi di Bari, Campus Universitario, 70126 Bari, Italy
Alessandro Merendino
Affiliation:
Lachifarma s.r.l. Laboratorio Chimico Farmaceutico, Dipartimento Ricerca & Sviluppo S.S. 16 Zona Industriale, 73010 Zollino (Lecce), Italy
Luciano Villanova
Affiliation:
Lachifarma s.r.l. Laboratorio Chimico Farmaceutico, Dipartimento Ricerca & Sviluppo S.S. 16 Zona Industriale, 73010 Zollino (Lecce), Italy
Adriana Giangrande
Affiliation:
Dipartimento di Scienze e Tecnologie Biologiche ed Ambientali, Università del Saliento, 73100 (Lecce), Italy
*
Correspondence should be addressed to: L. Stabili, Dipartimento di Scienze e Tecnologie Biologiche ed Ambientali, Università del Salento, 73100 (Lecce), Italy email: [email protected]
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Abstract

Although mucus plays many different roles among marine invertebrates, relatively little is known about the link between biochemical structure and function. In the present study we focused on some physical and chemical properties of the polychaete Sabella spallanzanii's mucus such as viscosity, osmolarity, electrical conductivity, elemental composition, the protein and carbohydrate content, the total lipids and fatty acid composition, and polychlorinated biphenyls (PCBs) contamination. Moreover, an antimicrobial activity of the mucus was investigated. The water content of S. spallanzanii mucus was 96.2±0.3%. By dry weight 26±1.2% was protein, 8±0.21% was carbohydrate and only 0.1% lipid, much of the remainder of the dry weight was inorganic (about 65.2%). The estimated PCBs content was <0.005 μg g−1. The mucus of S. spallanzanii exerted a natural lysozyme-like activity and produced in vitro the growth inhibition of Vibrio anguillarum, Vibrio harveyi, Pseudomonas aeruginosa and Candida albicans. The findings from this study contribute to improve the limited knowledge available on the mucus composition in invertebrates and have implications for future investigations related to employment of S. spallanzanii mucus as a source of compounds of pharmaceutical and marine technological interest.

Keywords

mucusproteinscarbohydrateslipidsPCBslysozymeantimicrobial activity
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 91 , Issue 1 , February 2011 , pp. 199 - 208
Copyright
Copyright © Marine Biological Association of the United Kingdom 2010

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References

REFERENCES

Baier, R.E., Gucinski, H., Meenaghan, M.A., Wirth, J. and Glantz, P.Q. (1985) Biophysical studies of mucosal surfaces. In Glantz, P.-O., Leach, S.A. and Ericson, T. (eds) Oral interfacial reactions of bone, soft tissue and saliva. Oxford: IRL Press, pp. 83–95.Google Scholar
Barg, U. and Phillips, M.J. (1998) Environment and sustainability. Rome: FAO, 163 pp. [FAO Fisheries Circular, no. 886.]Google Scholar
Bavington, C.D., Lever, R., Mulloy, B., Grundy, M.M., Page, C.P., Richardson, N.V. and McKenzie, J.D. (2004) Anti-adhesive glycoproteins in echinoderm mucus secretions. Comparative Biochemistry and Physiology B139, 607–617.CrossRefGoogle Scholar
Bonar, D.B. (1972) Feeding and tube construction in Chone mollis Bush (Polychaeta, Sabellidae). Journal of Experimental Marine Biology and Ecology B9, 1–18.CrossRefGoogle Scholar
Bradford, M. (1976) A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of proteins dye binding. Analytical Biochemistry 72, 248.CrossRefGoogle Scholar
Brown, B.E. and Bythell, J.C. (2005) Perspectives on mucus secretion in reef corals. Marine Ecology Progress Series 296, 291–309.CrossRefGoogle Scholar
Bucolo, G. and David, H. (1973) Quantitative determination of serum triglycerides by the use of enzymes. Clinical Chemistry 19, 476–482.CrossRefGoogle ScholarPubMed
Budge, S.M. and Parrish, C.C. (2003) FA determination in cold water marine samples. Lipids 38, 781–791.CrossRefGoogle ScholarPubMed
Canicatti, C. (1989) Evolution of the lytic system in echinoderms. 2. Naturally occurring haemolytic activity in Marthasterias glacialis (Asteroidea) coelomic fluid. Comparative Biochemistry and Physiology 93A, 587–591.CrossRefGoogle Scholar
Canicatti, C. and d'Ancona, G. (1990) Biological protective substances in Marthasterias glacialis (Asteroidea) epidermal secretion. Journal of Zoology 222, 445–454.CrossRefGoogle Scholar
Canicattì, C., Ville, P., Pagliara, P. and Roch, P. (1992) Hemolysins from the mucus of Spirographis spallanzanii (Polychaeta: Sabellidae). Marine Biology 114, 453–458.CrossRefGoogle Scholar
Carsten, T. and Schupp, P.J. (2008) Activated chemical defense in marine sponges—a case study on Aplysinella rhax. Journal of Chemical Ecology 34, 1242–1252.Google Scholar
Charman, J. and Reid, L. (1973) The effect of freezing and thawing on the viscosity of sputum. Biorheology 10, 295–301.CrossRefGoogle ScholarPubMed
Clare, A.S. (1995) Marine natural product antifoulants: status and potential. Biofouling 9, 211–229.CrossRefGoogle Scholar
Coffroth, M.A. (1990) Mucus sheet formation on poritid corals: an evaluation of coral mucus as a nutrient source on reefs. Marine Biology 105, 39–49.CrossRefGoogle Scholar
Cone, R.A. (1999) Mucus. In Ogra, P.L., Mestecky, J., Lamm, M.E., Strober, W., Bienenstock, J. and McGhee, J.R. (eds) Mucosal immunology. San Diego: Academic Press, pp. 43–64.Google Scholar
Connor, V.M. (1986) The use of mucous trails by intertidal limpets to enhance food resources. Biological Bulletin. Marine Biological Laboratory, Woods Hole 171, 548–564.CrossRefGoogle ScholarPubMed
Dales, R.P. (1961) The coelomic and peritoneal cell systems of some sabellid polychaetes. Quarterly Journal of Microscopical Science 102, 327–346.Google Scholar
Davies, M.S., Jones, H.D. and Hawkins, S.J. (1990) Seasonal variation in the composition of pedal mucus from Patella vulgata L. Journal of Experimental Marine Biology and Ecology 144, 101–112.CrossRefGoogle Scholar
Davis, J.M. and Viney, C. (1998) Water–mucin phases: conditions for mucus liquid crystallinity. Thermochimica Acta 315, 39–49.CrossRefGoogle Scholar
DeMoor, S., Waite, H., Jangoux, M. and Patrick, P. (2003) Characterization of the adhesive from Cuvierian tubules of the sea cucumber Holothuria forskali (Echinodermata, Holothuroidea). Marine Biotechnology 5, 45–57.CrossRefGoogle ScholarPubMed
Dubois, M., Gilles, K.A., Hamilton, J.K., Rebers, P.A. and Smith, F. (1956) Colorimetric method for determination of sugars and related substances. Analytical Chemistry 28, 350–356.CrossRefGoogle Scholar
Ebran, N., Julien, S., Orange, N., Auperin, B. and Molle, G. (2000) Isolation and characterization of novel glycoproteins from fish epidermal mucus: correlation between their pore-forming properties and their antibacterial activities. Biochimica et Biophysica Acta 1467, 271–280.CrossRefGoogle ScholarPubMed
Flammang, P. (2006) Adhesive secretions in echinoderms: an overview. In Smith, A.M. and Callow, J.A. (eds) Biological adhesives. Berlin: Springer, pp. 183–206.CrossRefGoogle Scholar
Flammang, P., Ribesse, J. and Jangoux, M.M. (2002) Biomechanics of adhesion in sea cucumber Cuvierian tubules (Echinodermata, Holothuroidea). Integrative and Comparative Biology 42, 1107–1115.CrossRefGoogle ScholarPubMed
Flammang, P. and Walker, G. (1997) Measurement of the adhesion of the podia in the asteroid Asterias rubens (Echinodermata). Journal of the Marine Biological Association of the United Kingdom 77, 1251–1254.CrossRefGoogle Scholar
Flammang, P.A., Van Cauwenberge, M.A., Alexandre, H. and Jangoux, M. (1998) A study of temporary adhesion of the podia in the sea star Asterias rubens (Echinodermata, Asteroidea) through their footprints. Journal of Experimental Biology 201, 2383–2395.CrossRefGoogle ScholarPubMed
Folch, J., Less, M. and Stone Stanley, G.H. (1957) A simple method for the isolation and purification of total lipids from animal tissues. Journal of Biological Chemistry 226, 497–508.CrossRefGoogle ScholarPubMed
Giangrande, A., Licciano, M., Pagliara, P. and Gambi, M.C. (2000) Gametogenesis and larval development in Sabella spallanzanii (Polychaeta: Sabellidae) from the Mediterranean Sea. Marine Biology 136, 847–861.CrossRefGoogle Scholar
Graham, L.D. (2008) Biological adhesives from nature. In Wnek, G. and Bowlin, G. (eds) Encyclopedia of biomaterials and biomedical engineering, 2nd edition.New York & London: Informa Healthcare, pp. 236–253.Google Scholar
Gupta, B.J. (1989) The relationship of mucoid substances and ion and water transport, with new data on intestinal goblet cells and a model for gastric secretion. Symposia of the Society for Experimental Biology. Cambridge 43, 81–110.Google Scholar
Guzman-Murillo, M.A. and Ascencio, F. (2000) Anti-adhesive activity of sulphated exopolysaccharides of microalgae on attachment of red shore disease-associated bacteria and Helicobacter pylori to tissue culture cells. Letters in Applied Microbiology 30, 473–478.CrossRefGoogle Scholar
Hamwood, T.E., Cribb, B.W., Halliday, J.A., Kearn, G.C. and Whittington, I.D. (2002) Preliminary characterization and extraction of anterior adhesive secretion in monogean (plathelminth) parasites. Folia Parasitologica 49, 39–49.CrossRefGoogle Scholar
Hames, B.D. (1990) One-dimensional polyacrylamide gel electrophoresis. In Hames, B.D. and Rickwood, D. (eds) Gel electrophoresis of proteins: a practical approach. Oxford: IRL, pp. 1–147.Google Scholar
Hellio, C., Berge, J.P., Beaupoil, C., Gal, Y.L. and Bougougnon, N. (2002) Screening of marine algal extracts for anti-settlement activities against microalgae and maroalgae. Biofouling 18, 205–215.CrossRefGoogle Scholar
Jelic-Mrcelic, G., Sliskovic, M. and Antolic, B. (2006) Biofouling communities on test panels coated with TBT and TBT-free copper-based antifouling paints. Biofouling 22, 293–302.CrossRefGoogle ScholarPubMed
Ibrahim, H.R., Aoki, T. and Pellegrini, A. (2002) Strategies for new antimicrobial proteins and peptides: lysozyme and aprotinin as model molecules. Current Pharmaceutical Design 8, 671–693.CrossRefGoogle ScholarPubMed
Iwanaga, S. and Lee, B.L. (2005) Recent advances in the innate immunity of invertebrate animals. Journal of Biochemistry and Molecular Biology 38, 128–150.Google ScholarPubMed
Jones, K.C. and de Voogt, P. (1999) Persistent organic pollutants (POPs): state of the science. Environmental Pollution 100, 209–221.CrossRefGoogle ScholarPubMed
Kamino, K. (2006) Barnacle underwater attachment. In Smith, A.M. and Callow, J.A. (eds) Biological adhesives. Berlin: Springer, pp. 145–166.CrossRefGoogle Scholar
Kennedy, J.F. and Pagliuca, G. (1994) Chapter 2. Oligosaccharides. In Chapling, M.F. and Kennedy, J.F. (eds) Carbohydrate analysis: a practical approach, 2nd edition.New York: Oxford University Press, Inc., pp. 43–72.CrossRefGoogle Scholar
Kitson, R.E. and Mellon, M.G. (1944) Colorimetric determination of phosphorus as molybdivanadophosphoric acid. Industrial and Engineering Chemistry, Analytical Edition. Easton, Pa. 16, pp. 379.CrossRefGoogle Scholar
Konstantinou, I.K. and Albanis, T.A. (2004) Worldwide occurrence and effects of antifouling paint booster biocides in the aquatic environment: a review. Environmental International 30, 235–248.CrossRefGoogle ScholarPubMed
Laemmli, V.H. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680–682.CrossRefGoogle ScholarPubMed
Lewis, D.B. (1968) Feeding and tube building in the Fabriciinae (Annelida, Polychaeta). Proceedings of the Linnean Society of London 179, 37–49.CrossRefGoogle Scholar
Lopez-Vidriero, M.T., Jones, R. and Reid, L. (1980) Analysis of skin mucus of plaice Pleuronectes platessa L. Journal of Comparative Pathology 90, 415–420.CrossRefGoogle ScholarPubMed
Mastrodonato, M., Lepore, E., Gherardi, M., Zizza, S., Sciscioli, M. and Ferri, D. (2005) Histochemical and ultrastructural analysis of the epidermal gland cells of Branchioma luctuosum (Polichaeta, Sabellidae). Invertebrate Biology 124, 303–309.CrossRefGoogle Scholar
McKenzie, J.D. and Grigovala, I.V. (1996) The echinoderm surface and its role in preventing microfouling. Biofouling 10, 261–272.CrossRefGoogle ScholarPubMed
Meikle, P. (1986) Chemical and biochemical studies on the mucus from Acropora formosa and preliminary investigations of mucus from five other coral species. PhD thesis. James Cook University of North Queensland, Townsville, Australia.Google Scholar
Meikle, P., Richards, G.N. and Yellowlees, D. (1987) Structural characterisation of the oligosaccharide side chains from a glycoprotein isolated from the mucus of the coral Acropora formosa. Journal of Biological Chemistry 262, 16941–16947.CrossRefGoogle Scholar
Meikle, P., Richards, G.N. and Yellowlees, D. (1988) Structural investigations on the mucus from six species of coral. Marine Biology 99, 187–193.CrossRefGoogle Scholar
Mouneyrac, C., Mastain, O., Amiard, J.C., Amiard-Triquet, C., Beaunier, P., Jeantet, A.Y., Smith, B.D. and Rainbow, P.S. (2003) Trace-metal detoxication and tolerance of the estuarine worm Hediste diversicolor chronically exposed in their environment. Marine Biology 143, 731–744.CrossRefGoogle Scholar
Ostroumov, S.A. (2008) On the concepts of biochemical ecology and hydrobiology: ecological chemomediators. Contemporary Problems of Ecology 1, 238–244.CrossRefGoogle Scholar
Paul, J.H., DeFlaun, M.F. and Jeffrey, W.H. (1986) Elevated levels of microbial activity in the coral surface microlayer. Marine Ecology Progress Series 33, 29–40.CrossRefGoogle Scholar
Pawlicki, J.M., Pease, L.B., Pierce, C.M., Startz, T.P., Zhang, Y. and Smith, A.M. (2004) The effect of molluscan glue proteins on gel mechanics. Journal of Experimental Biology 207, 1127–1135.CrossRefGoogle ScholarPubMed
Pomponi, S.A., Willoughby, R., Wright, A.E., Pecorella, C., Sennet, S.H., Lopez, J. and Samples, G. (1998) In vitro production of marine-derived antitumor compounds. In Le Gal, Y. and Halvorson, H.O. (eds) New developments in marine biotechnology. New York: Plenum Press, p. 43.Google Scholar
Quinlan, K.P. and Desesa, M.A. (1955) Spectrophotometric determination of phosphorus as molybdovanadophosphoric acid. Analytical Chemistry 27, 1626–1629.CrossRefGoogle Scholar
Quinnell, S., Hulsman, K. and Davie, P.J.F. (2004) Protein model for pollutant uptake and elimination by living organisms and its implications for ecotoxicology. Marine Ecology Progress Series 274, 1–16.CrossRefGoogle Scholar
Ritchie, K.B. (2006) Regulation of microbial populations by coral surface mucus and mucus-associated bacteria. Marine Ecology Progress Series 322, 1–14.CrossRefGoogle Scholar
Rosen, M.W. and Cornford, N.E. (1971) Fluid friction of fish slimes. Nature 234, 49–51.CrossRefGoogle Scholar
Sagert, J., Sun, C. and Waite, J.H. (2006) Chemical subtleties of mussel and polychaete holdfasts. In Smith, A.M. and Callow, J.A. (eds) Biological adhesives. Berlin: Springer, pp. 124–140.Google Scholar
Santos, R., Costa, G. da, Franco, C., Gomes-Alves, P., Flammang, P. and Coelho, A.V. (2009) First insights into the biochemistry of tube foot adhesive from the sea urchin Paracentrotus lividus (Echinoidea, Echinodermata). Marine Biotechnology 11, 686–698.CrossRefGoogle ScholarPubMed
Smith, A.M. (2006) The biochemistry and mechanics of gastropod adhesive gels. In Smith, A.M. and Callow, J.A. (eds) Biological adhesives. Berlin: Springer, pp. 167–182.CrossRefGoogle Scholar
Smith, A.M. and Morin, M.M. (2002) Biochemical differences between trail mucus and adhesive mucus from marsh periwinkle snails. Biological Bulletin. Marine Biological Laboratory, Woods Hole 203, 338–346.CrossRefGoogle ScholarPubMed
Smith, A.M., Quick, T.J. and Peter, S.T.R.L. (1999) Differences in the composition of adhesive and non-adhesive mucus from the limpet Lottia zimatula. Biological Bulletin. Marine Biological Laboratory, Woods Hole 196, 34–44.CrossRefGoogle Scholar
Stabili, L., Schiros', R., Licciano, M. and Giangrande, A. (2009) The mucus of Sabella spallanzanii (Annelida, Polychaota): its involvement in chemical defence and fertilization success. Journal of Experimental Marine Biology and Ecology 374, 144–149.CrossRefGoogle Scholar
Statsoft Inc. (2001) Electronic statistics textbook. Tulsa, OK: Statsoft.Google Scholar
Storch, V. (1988) The ultrastructure of Polychaeta. I. Integument. In Westheide, W. and Hermans, C.O. (eds) Microfauna marina, Volume 4. Stuttgart: Verlag, pp. 13–36.Google Scholar
Stupak, M.E., Garcia, M.T. and Perez, M.C. (2003) Non-toxic alternative compounds for marine antifouling paints. International Biodeterioration and Biodegradation 52, 49–52.CrossRefGoogle Scholar
Suzuki, Y., Tasumi, S., Tsutsui, S., Okamoto, M. and Suetake, H. (2003) Molecular diversity of skin mucus lectins in fish. Comparative Biochemistry and Physiology B136, 723–730.CrossRefGoogle Scholar
Trinder, P. (1969) Simple turbidemetric method for the determination of serum cholesterol. Annals of Clinical Biochemistry 6, 165.CrossRefGoogle Scholar
Turley, P.A., Fenn, R.J., Ritter, J.C. and Callow, M.E. (2005) Pyrithiones as antifoulants: environmental fate and loss of toxicity. Biofouling 21, 31–40.CrossRefGoogle ScholarPubMed
Verdugo, P. (1984) Hydration kinetics of exocytosed mucins in cultured secretory cells of the rabbit trachea: a new model. In Nugent, J. and O'Conner, M. (eds) Mucus and mucosa. London: Pitman Publishing, pp. 212–222. [Ciba Foundation Symposium no. 109.]Google Scholar
Wainwright, S.A., Biggs, W.D., Currey, J.D. and Gosline, J.M. (1976) Mechanical design in organisms. Princeton: Princeton University Press, 423 pp.Google Scholar
Withers, P.C. (1992) Comparative animal physiology. Fort Worth: Saunders College Publishing, 669 pp.Google Scholar
Zöllner, N. and Kirsch, K. (1962) Determination of the total lipid concentration in serum. Zentralblatt für Gesamte Experimentelle Medizin 135, 545–549.CrossRefGoogle Scholar
Zuchelkowski, E.M., Pinkstaff, C.A. and Hinton, D.E. (1985) Mucosubstance histochemistry in control and acid-stressed epidermis of brown bullhead catfish, Ictalurus nebulosus (LeSueur). Anatomical Record 212, 327–335.CrossRefGoogle ScholarPubMed