Seasonal variability of prooxidant pressure and antioxidant adaptation to symbiosis in the Mediterranean demosponge Petrosia ficiformis

In symbioses between invertebrates and microalgae, host tissues are exposed to increased levels of photosynthetically produced oxygen. The biochemical consequences of symbioses have been poorly investigated in Mediterranean species, but a general increase in antioxidant defences has been recently reported in the demosponge Petrosia ficiformis as an adaptive response to the cyanobacterium Aphanocapsa feldmanni. Since Mediterranean symbioses naturally experi- ence marked seasonal variations in symbiont content, light intensity and seawater temperature, the aim of this work was to investigate if these fluctuations modulate the prooxidant challenge to sponge tissues. Antioxidant efficiency was characterised on a monthly basis by combining an analysis of the main antioxidants (superoxide dismutase, catalase, glutathione S-transferases, glutathione reduc- tase, glutathione peroxidases) with measurements of the total oxyradical scavenging capacity (TOSC), thus achieving a more holistic assessment of the capacity of sponge tissues to absorb differ- ent forms of reactive oxygen species. Symbiotic sponges showed significant seasonal changes in antioxidant efficiency, with more marked variations in tissues directly exposed to photosynthetically produced reactive oxygen species. The greatest variations were observed during the summer months, with the highest seasonal values for some defences (i.e. catalase) and the lowest for others (i.e. glutathione peroxidases). The marked increase in catalase and TOSC in summer suggests greater production of H2O2 in the symbioses during this period, supporting the hypothesis that sea- water temperature can significantly modulate the prooxidant challenge in Mediterranean symbioses. The results suggest that species with lower antioxidant efficiency may be less tolerant of conditions effecting oxidative damage; e.g. increases in temperature during the summer months.

[1]  S. Bompadre,et al.  Total oxidant scavenging capacity (TOSC) of microsomal and cytosolic fractions from Antarctic, Arctic and Mediterranean scallops: differentiation between three potent oxidants. , 2000, Aquatic toxicology.

[2]  P. Glynn,et al.  Bleaching and Recovery of Five Eastern Pacific Corals in an El Niño-Related Temperature Experiment , 2001 .

[3]  Regoli.  Total oxyradical scavenging capacity (TOSC) in polluted and translocated mussels: a predictive biomarker of oxidative stress. , 2000, Aquatic toxicology.

[4]  C. Downs,et al.  Exploring the basis of thermotolerance in the reef coral Goniastrea aspera , 2002 .

[5]  G. Bavestrello,et al.  Are diatoms a food source for Antarctic sponges? , 2004 .

[6]  M. Lesser.  Elevated temperatures and ultraviolet radiation cause oxidative stress and inhibit photosynthesis in ymbiotic dinoflagellates , 1996 .

[7]  J. J. Gilbert,et al.  Chlorophyll and Primary Productivity of Some Green, Freshwater Sponges , 1973 .

[8]  C. Downs,et al.  A Molecular Biomarker System for Assessing the Health of Coral (Montastraea faveolata) During Heat Stress , 2000, Marine Biotechnology.

[9]  F. Regoli,et al.  Applications of a new method for measuring the total oxyradical scavenging capacity in marine invertebrates , 1998 .

[10]  C. Usai,et al.  ABA- and cADPR-mediated effects on respiration and filtration downstream of the temperature-signaling cascade in sponges , 2003, Journal of Cell Science.

[11]  E. Stackebrandt,et al.  Vibrio shiloi sp. nov., the causative agent of bleaching of the coral Oculina patagonica. , 2001, International journal of systematic and evolutionary microbiology.

[12]  B. Rajagopalan,et al.  Mass Coral Reef Bleaching: A Recent Outcome of Increased El Niño Activity? , 1999, Ecology letters.

[13]  C. Wilkinson.  Global and local threats to coral reef functioning and existence: review and predictions , 1999 .

[14]  W. Dunlap,et al.  REVIEW—ULTRAVIOLET RADIATION‐ABSORBING MYCOSPORINE‐LIKE AMINO ACIDS IN CORAL REEF ORGANISMS: A BIOCHEMICAL AND ENVIRONMENTAL PERSPECTIVE , 1998 .

[15]  M. P. Lesser,et al.  Bleaching in coral reef anthozoans: effects of irradiance, ultraviolet radiation, and temperature on the activities of protective enzymes against active oxygen , 1990, Coral Reefs.

[16]  S. Focardi,et al.  Integrating enzymatic responses to organic chemical exposure with total oxyradical absorbing capacity and dna damage in the european eel Anguilla anguilla , 2003, Environmental toxicology and chemistry.

[17]  J. Shick.  Diffusion Limitation and Hyperoxic Enhancement of Oxygen Consumption in Zooxanthellate Sea Anemones, Zoanthids, and Corals. , 1990, The Biological bulletin.

[18]  M. Lesser.  Oxidative stress causes coral bleaching during exposure to elevated temperatures , 1997, Coral Reefs.

[19]  F. Regoli,et al.  Quantification of total oxidant scavenging capacity of antioxidants for peroxynitrite, peroxyl radicals, and hydroxyl radicals. , 1999, Toxicology and applied pharmacology.

[20]  B. Halliwell,et al.  Free radicals in biology and medicine , 1985 .

[21]  J. Dykens,et al.  Oxygen radical production in the sea anemone Anthopleura elegantissima and its endosymbiotic algae , 1992 .

[22]  M. Badger.  Photosynthetic Oxygen Exchange , 1985 .

[23]  E. Gaino,et al.  Necrosis in a population of Petrosia ficiformis (Porifera, Demospongiae) in relation with environmental stress , 2001 .

[24]  S. Bompadre,et al.  Susceptibility to oxidative stress of the Mediterranean demosponge Petrosia ficiformis : role of endosymbionts and solar irradiance , 2000 .

[25]  P. Picco,et al.  A catastrophic mass‐mortality episode of gorgonians and other organisms in the Ligurian Sea (North‐western Mediterranean), summer 1999 , 2000 .

[26]  A. Penna,et al.  Diatom invasion in the antarctic hexactinellid sponge Scolymastra joubini , 2000, Polar Biology.

[27]  M. Lesser,et al.  Depth-dependent responses to solar ultraviolet radiation and oxidative stress in the zooxanthellate coral Acropora microphthalma , 1995 .

[28]  F. Regoli,et al.  DNA integrity and total oxyradical scavenging capacity in the Mediterranean mussel, Mytilus galloprovincialis: a field study in a highly eutrophicated coastal lagoon. , 2001, Aquatic toxicology.

[29]  M. Havaux.  Stress Tolerance of Photosystem II in Vivo: Antagonistic Effects of Water, Heat, and Photoinhibition Stresses. , 1992, Plant physiology.

[30]  M. Lesser,et al.  Effects of ultraviolet radiation on corals and other coral reef organisms , 1996 .

[31]  J. Vacelet,et al.  Mortalité massive d'invertébrés marins : un événement sans précédent en Méditerranée nord-occidentale , 2000 .

[32]  O. H. Lowry,et al.  Protein measurement with the Folin phenol reagent. , 1951, The Journal of biological chemistry.

[33]  Raymond L. Hayes,et al.  Coral Bleaching and Ocean "Hot Spots" , 1994 .

[34]  A. Douglas,et al.  Experience shapes the susceptibility of a reef coral to bleaching , 2002, Coral Reefs.

[35]  F. Regoli,et al.  A rapid gas chromatographic assay for determining oxyradical scavenging capacity of antioxidants and biological fluids. , 1998, Free radical biology & medicine.

[36]  C. Usai,et al.  The temperature-signaling cascade in sponges involves a heat-gated cation channel, abscisic acid, and cyclic ADP-ribose , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[37]  M. Richter,et al.  Studies on the mechanism of photosystem II photoinhibition II. The involvement of toxic oxygen species , 1990, Photosynthesis Research.

[38]  A. Douglas.  Coral bleaching--how and why? , 2003, Marine pollution bulletin.

[39]  C. Downs,et al.  Oxidative stress and seasonal coral bleaching. , 2002, Free radical biology & medicine.

[40]  C. Bianchi,et al.  Coral mortality in NW Mediterranean , 2000, Coral Reefs.

[41]  Solar global radiation and climate at Genova, Italy , 1981 .

[42]  S. Heckathorn,et al.  Heat-shock proteins and thermotolerance: linking molecular and ecological perspectives. , 1995, Trends in ecology & evolution.

[43]  M. Lesser,et al.  Effects of irradiance and ultraviolet radiation on photoadaptation in the zooxanthellae of Aiptasia pallida: primary production, photoinhibition, and enzymic defenses against oxygen toxicity , 1989 .

[44]  J. Dykens,et al.  Oxygen detoxification in algal-invertebrate symbioses from the Great Barrier Reef , 1985, Oecologia.

[45]  Barbara E. Brown,et al.  Adaptations of Reef Corals to Physical Environmental Stress , 1997 .

[46]  B. Chance,et al.  The relation of free radical production to hyperoxia. , 1986, Annual review of physiology.

[47]  A. Mehler.  Studies on reactions of illuminated chloroplasts. I. Mechanism of the reduction of oxygen and other Hill reagents. , 1951, Archives of biochemistry and biophysics.