Abstract
Hydrothermal vent environments, particularly those associated with the vestimentiferan Riftia pachyptila, are believed to be among the highest chitin-producing systems. In order to elucidate the chitin cycle in these environments, we estimate the in situ chitin degradation rates of tube-worm exoskeletons. Our in situ experiments show that the tubes of Riftia are highly stable structures. Comparative measurements of the degradation rates of Riftia tubes and crab shells immersed at deep-sea vents show that the tubes would be degraded within 2.5 years, whereas the time for the total degradation of the vent crab (Bythograea thermydron) carapaces would not exceed 36 days. The importance of the microbial participation in this degradation was estimated for Riftia tubes. Based on previous work, we calculated chitin production by a population of Riftia tubes of about 750 g m-2 year-1 (763). From our in situ experiments, we estimated a microbial chitinolysis rate of about 500 g m-2 year-1 (496) (65% of the chitin produced).Exoskeletons containing β-chitin appear more stable in natural environments than those containing α-chitin and would thus be less available as carbon and nitrogen sources. In contrast, isolated β-chitin was hydrolysed faster than α-chitin during in vitro degradation experiments; for instance, Riftia β-chitin was degraded about 3- to 4-fold faster than Bythograea α-chitin. A stabilization process by disulfide bonds of the proteins-chitin link, rather than the crystalline form of the chitin (α/β), accounts for the resistance of Riftia tubes to enzymatic attacks.
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References
Fretter V (1988) New archaeogastropod limpets from hydrothermal vent: superfamily Lepetodrilacea. II. Anatomy. Philos Trans R Soc Lond B 318:33–82
Fustec A, Desbruyères D, Juniper K (1987) Deep-sea hydrothermal vent communities at 13°N on the east pacific rise: microdistribution and temporal variations. Biol Oceanogr 4:121–163
Gaill F, Hunt S (1986) Tubes of deep sea hydrothermal vent worms Riftia pachyptila (Vestimentifera) and Alvinella pompejana (Annelida). Mar Ecol Prog Ser 34:267–274
Gaill F, Hunt S (1991) The biology of annelid worms from high temperature hydrothermal vent regions. Rev Aquat Sci 4:107–137
Gaill F, Shillito B, Ménard F. Goffinet G, Childress JJ (1997) Rate and process of tube production by the deep-sea hydrothermal vent tubeworm Riftia pachyptila. Mar Ecol Prog Ser 148:135–143
Goffinet G (1996) Production and biodegradation of chitin in marine environments. In: Giraud-Guille MM (ed) Chitin in life sciences. 1st Summer school European Chitin Society. Jacques André, Lyon, pp 53–65
Goffinet G, Jeuniaux C (1994) Le tégument: morphologie et biochimie. In: Grassé PP (ed) Traité de zoologie, vol VII. Crustacés. Morphologie, physiologie, reproduction, embryologie. Masson, Paris
Jeuniaux C (1963) Chitine et chitinolyse, un chapitre de la biologie moléculaire. Masson, Paris
Jeuniaux C (1982) La chitine dans le règne animal. Bull Soc Zool France 107:363–386
Lechaire JP, Shillito B, Frébourg G, Gaill F (2002) Elemental characterization of microorganism granules by EFTEM in the tube wall of a deep-sea vent invertebrate. Biol Cell 94:243–249
Locke M, Huie P (1980) Cuticle techniques in arthropods. Springer, New York Heidelberg Berlin
Lopez-Garcia P, Gaill F, Moreira D (2002) Wide bacterial diversity associated to tubes of the vent worm Riftia pachyptila. Env Microbiol 4:204–215
Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Proteins measurement with the folin phenol reagent. J Biol Chem 193:265–275
Poulicek M, Goffinet G, Voss-Foucart MF, Jaspar-Versali MF, Bussers JC, Toussaint C (1985) Chitin degradation in natural environment (mollusk shells and crab carapaces). In: Muzzarelli RAA, Jeuniaux C, Gooday GW (eds) Chitin in nature and technology. Plenum, New York, pp 547–550
Poulicek M, Gaill F, Goffinet G (1998) Chitin biodegradation in marine environments. In: Stankiewicz BA, van Bergen PF (eds) Nitrogen-containing macromolecules in the bio- and geosphere. American Chemical Society, Washington, DC, pp 163–210
Ravaux J, Gay L, Voss-Foucart MF, Gaill F (1998) Tube growth process in the deep-sea hydrothermal vent tube-worm Riftia pachyptila : synthesis and degradation of chitin. Cah Biol Mar 39: 99–107
Roux M, Rio M, Schein E, Lutz RA, Fritz LW, Ragone LM (1989) Mesures in situ de la croissance des bivalves et des vestimentifères et de la corrosion des coquilles au site hydrothermal de 13°N (dorsale du Pacifique oriental). C R Acad Sci Paris 308:121–127
Sadosky F, Thiébaut E, Jollivet D, Shillito B (2002) Recruitement and population structure of the vetigastropod Lepetodrilus elevatus at 13°N hydrothermal vent sites on East Pacific Rise. Cah Biol Mar 43:399–402
Sarradin PM, Caprais JC, Briand P, Gaill F, Shillito B, Desbruyères D (1998) Chemical and thermal description of the environment of the Genesis hydrothermal vent community (13°N, EPR). Cah Biol Mar 39:159–167
Shillito B, Lechaire JP, Goffinet G, Gaill F (1995) Composition and morphogenesis of the tubes of vestimentiferan worms. In: Parson LM, Walker CL, Dixon DR (eds) Hydrothermal vents and processes. Geological Society Special Publication, pp 295–302
Shillito B, Ravaux J, Gaill F, Delachambre J, Thiébaut E, Childress JJ (1999) Preliminary data on carbon production of deep-sea vent tubeworms. Mar Ecol Prog Ser 183:275–279
Voss-Foucart MF, Bussers JC, Goffinet G, Poulicek M, Toussaint C, Jeuniaux C (1984) Etude préliminaire de la diagenèse précoce des carapaces de Carcinus maenas dans un sédiment marin. Altération structurale et chimique. Ann Soc R Zool Belg 114:145–146
Acknowledgements
We gratefully acknowledge chief scientists D. Desbruyères, J. Childress and C. Fisher. We thank the captain, pilots and crew of Atalante and Nautile; Atlantis and Alvin and those from Harbor Branch Oceanographic Institute's RV Edwin Link and DSRV Johnson Sea Link. We also thank C. Toussaint for her technical assistance; and B. Shillito and J.P. Lechaire for their help in chitin production calculations. This work was funded by the CNRS program Geomex, the French program Dorsales and the CEE program VENTOX (n°EVK3CT1999–00003).
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Communicated by S.A. Poulet, Roscoff
J. Ravaux and M. Zbinden contributed equally to this work
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Ravaux, J., Zbinden, M., Voss-Foucart, M.F. et al. Comparative degradation rates of chitinous exoskeletons from deep-sea environments. Marine Biology 143, 405–412 (2003). https://doi.org/10.1007/s00227-003-1086-8
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DOI: https://doi.org/10.1007/s00227-003-1086-8