Improved survival under heat stress in intertidal embryos (Fucus spp.) simultaneously exposed to hypersalinity and the effect of parental thermal history

Intertidal organisms exposed to thermal stress normally experience other stresses simultaneously, but how these combined stresses modify tolerance to heat, especially for embryos, is poorly understood. Tolerance of fucoid algal embryos to heat, with and without acclimation to a sublethal temperature and with simultaneous exposure to hypersaline media, was examined. Embryos of Fucus vesiculosus L. (mid-intertidal zone) were less tolerant than embryos of Fucus spiralis L. (upper intertidal zone); without acclimation and with a growth temperature of 14°C, about half of the embryos survived 3 h exposure to 33°C in F. vesiculosus and of 35°C in F. spiralis. Conditions experienced by parental thalli (4°C versus 14°C storage) significantly affected the heat tolerance of embryos grown for 24 h post-fertilization at 14°C in F. vesiculosus, a result that is important for biologists using fucoid algae as model systems. Acclimation to a sublethal temperature (29°C) or exposure to the LT50 (33°C, F. vesiculosus; 35°C, F. spiralis) in 100 psu seawater (2850 mmol kg−1 osmolality) resulted in 30–50% higher levels of embryonic survival. Higher levels of HSP60s were found in embryos exposed to 29–33°C than to 14°C; lower levels of HSP60s were present in embryos exposed to the LT50 under hypersaline conditions than in normal seawater. Contemporaneous studies in 1995–1996 of substratum temperature and desiccation levels were made at Schoodic Point, Maine (USA) underneath F. spiralis and F. vesiculosus canopies and in Semibalanus balanoides patches. This study extends the bioindicator utility of heat-shock proteins in studies of intertidal organisms and demonstrates the importance of integrated stress responses in survival of a single stress factor (e.g. temperature).

[1]  S. Kirchhoff,et al.  Cytosolic Heat Shock Protein 60, Apoptosis, and Myocardial Injury , 2002, Circulation.

[2]  S. Brawley The fast block against polyspermy in fucoid algae is an electrical block. , 1991, Developmental biology.

[3]  J. Pearse,et al.  Spatial segregation of four species of turban snails (Gastropoda:Tegula) in central California , 1981 .

[4]  Y. Kanesaki,et al.  Salt stress and hyperosmotic stress regulate the expression of different sets of genes in Synechocystis sp. PCC 6803. , 2002, Biochemical and biophysical research communications.

[5]  J. Lubchenco Littornia and Fucus: Effects of Herbivores, Substratum Heterogeneity, and Plant Escapes During Succession , 1983 .

[6]  Y. Loya,et al.  The 60-kDa Heat Shock Protein (HSP60) of the Sea Anemone Anemonia viridis: A Potential Early Warning System for Environmental Changes , 2001, Marine Biotechnology.

[7]  U. K. Laemmli,et al.  Cleavage of Structural Proteins during the Assembly of the Head of Bacteriophage T4 , 1970, Nature.

[8]  S. Brawley Fertilization in natural populations of the dioecious brown alga Fucus ceranoides and the importance of the polyspermy block , 1992 .

[9]  G. Somero,et al.  The threshold induction temperature of the 90-kDa heat shock protein is subject to acclimatization in eurythermal goby fishes (genus Gillichthys). , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[10]  J. Maul,et al.  Retracted: The Chlamydomonas reinhardtii Organellar Genomes Respond Transcriptionally and Post-Transcriptionally to Abiotic Stimuli , 2002, The Plant Cell Online.

[11]  Winfrid Schramm Ökologisch-physiologische Untersuchungen zur Austrocknungs- und Temperaturresistenz an Fuaus vesiculosus L. der westlichen Ostsee , 1968 .

[12]  L. Johnson,et al.  PREDICTING DESICCATION STRESS IN MICROSCOPIC ORGANISMS THE USE OF AGAROSE BEADS TO DETERMINE EVAPORATION WITHIN AND BETWEEN INTERTIDAL MICROHABITATS 1 , 1993 .

[13]  G O Kirst,et al.  Salinity Tolerance of Eukaryotic Marine Algae , 1990 .

[14]  S. Brawley,et al.  Reproductive ecology, of Fucus distichus (Phaeophyceae): an intertidal alga with successful external fertilization , 1996 .

[15]  A. Mathieson,et al.  Physiological Studies of Intertidal Fucoid Algae , 1978 .

[16]  G. Somero,et al.  Heat-Shock Protein Expression in Mytilus californianus: Acclimatization (Seasonal and Tidal-Height Comparisons) and Acclimation Effects. , 1997, The Biological bulletin.

[17]  G. Somero,et al.  Evidence for protein damage at environmental temperatures: seasonal changes in levels of ubiquitin conjugates and hsp70 in the intertidal mussel Mytilus trossulus , 1995, The Journal of experimental biology.

[18]  E. Girvetz,et al.  Induction of Marine Mollusc Stress Proteins by Chemical or Physical Stress , 2001, Archives of environmental contamination and toxicology.

[19]  P. Rinne,et al.  Dehydrins in cold-acclimated apices of birch (Betula pubescens Ehrh.): production, localization and potential role in rescuing enzyme function during dehydration , 1999, Planta.

[20]  T. Close,et al.  PROTEINS IMMUNOLOGICALLY RELATED TO DEHYDRINS IN FUCOID ALGAE , 1998 .

[21]  S. Brawley,et al.  Calmodulin-binding proteins are developmentally regulated in gametes and embryos of fucoid algae. , 1989, Developmental biology.

[22]  S. Gullans,et al.  Immediate early gene and HSP70 expression in hyperosmotic stress in MDCK cells. , 1991, The American journal of physiology.

[23]  M. Dring,et al.  Photosynthesis of Intertidal Brown Algae During and After Periods of Emersion: A Renewed Search for Physiological Causes of Zonation , 1982 .

[24]  A. Chapman Functional ecology of fucoid algae: twenty-three years of progress , 1995 .

[25]  S. Lindquist The heat-shock response. , 1986, Annual review of biochemistry.

[26]  Wilhelm Gruissem,et al.  Biochemistry & Molecular Biology of Plants , 2002 .

[27]  L. Johnson,et al.  Sublethal stress in the intertidal zone: tidal emersion inhibits photosynthesis and retards development in embryos of the brown alga Pelvetia fastigiata , 1993, Oecologia.

[28]  L. Kautsky,et al.  Successful external fertilization in turbulent environments. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[29]  H. Köhler,et al.  Daily stress protein (hsp70) cycle in chitons (Acanthopleura granulata Gmelin, 1791) which inhabit the rocky intertidal shoreline in a tropical ecosystem. , 2002, Comparative biochemistry and physiology. Toxicology & pharmacology : CBP.

[30]  I. Davison,et al.  STRESS TOLERANCE IN INTERTIDAL SEAWEEDS , 1996 .

[31]  T. Strömgren Short-term effects of temperature upon the growth of intertidal fucales , 1977 .

[32]  J. Collén,et al.  SEASONALITY AND THERMAL ACCLIMATION OF REACTIVE OXYGEN METABOLISM IN FUCUS VESICULOSUS (PHAEOPHYCEAE) , 2001 .

[33]  S. Baker ON THE CAUSES OF THE ZONING OF BROWN SEAWEEDS ON THE SEASHORE , 1909 .

[34]  K. Lüning,et al.  Seaweeds: Their Environment, Biogeography, and Ecophysiology , 1990 .

[35]  B. Menge,et al.  PHYSIOLOGY OF THE ROCKY INTERTIDAL PREDATOR NUCELLA OSTRINA ALONG AN ENVIRONMENTAL STRESS GRADIENT , 2001 .

[36]  G. Somero,et al.  Biochemical Adaptation: Mechanism and Process in Physiological Evolution , 1984 .

[37]  C. Paavola,et al.  Chlamydomonas transcripts encoding three divergent plastid chaperonins are heat-inducible , 1995, Plant Molecular Biology.

[38]  K. Oparka,et al.  The use of fluorescent probes for studies of living plant cells , 1994 .

[39]  T. Norton,et al.  Factors controlling the lower limits of fucoid algae on the shore , 1978 .

[40]  C. Harley,et al.  Climate Change and Latitudinal Patterns of Intertidal Thermal Stress , 2002, Science.

[41]  E. Serrão,et al.  Suppression subtractive hybridization for studying gene expression during aerial exposure and desiccation in fucoid algae , 2001 .

[42]  J. Mclachlan,et al.  Cold-hardiness of zygotes and embryos of Fucus (Phaeophyceae, Fucales)* , 1974 .

[43]  D. Wethey Biogeography, Competition, and Microclimate: The Barnacle Chthamalus fragilis in New England1 , 2002, Integrative and comparative biology.

[44]  H. Ruan,et al.  Effect of freezing on seaweed photosynthesis , 1989 .

[45]  J. Huang,et al.  Salt tolerance of Hordeum and Brassica species during germination and early seedling growth , 1995 .

[46]  H. Bode,et al.  Thermotolerance and synthesis of heat shock proteins: these responses are present in Hydra attenuata but absent in Hydra oligactis. , 1988, Proceedings of the National Academy of Sciences of the United States of America.

[47]  J. Callow,et al.  Gamete concentrations and timing and success of fertilization in a rocky shore seaweed , 2002 .

[48]  G. Somero,et al.  Evolutionary and acclimation-induced variation in the heat-shock responses of congeneric marine snails (genus Tegula) from different thermal habitats: implications for limits of thermotolerance and biogeography. , 1999, The Journal of experimental biology.

[49]  G. Hofmann,et al.  Adjusting the thermostat: the threshold induction temperature for the heat-shock response in intertidal mussels (genus Mytilus) changes as a function of thermal history. , 2001, The Journal of experimental biology.

[50]  L. Johnson,et al.  SURVIVAL OF FUCOID EMBRYOS IN THE INTERTIDAL ZONE DEPENDS UPON DEVELOPMENTAL STAGE AND MICROHABITAT 1 , 1991 .

[51]  L. Johnson,et al.  Dispersal and recruitment of a canopy-forming intertidal alga: the relative roles of propagule availability and post-settlement processes , 1998, Oecologia.

[52]  S. Brawley,et al.  CRYOANALYTICAL STUDIES OF FREEZING DAMAGE AND RECOVERY IN FUCUS VESICULOSUS (PHAEOPHYCEAE) , 1999 .

[53]  M. Feder,et al.  Heat-shock proteins, molecular chaperones, and the stress response: evolutionary and ecological physiology. , 1999, Annual review of physiology.

[54]  B. Helmuth,et al.  Microhabitats, Thermal Heterogeneity, and Patterns of Physiological Stress in the Rocky Intertidal Zone , 2001, The Biological Bulletin.

[55]  I. Davison,et al.  Freezing rate and duration determine the physiological response of intertidal fucoids to freezing , 1993 .

[56]  K. Lüning Temperature tolerance and biogeography of seaweeds: The marine algal flora of Helgoland (North Sea) as an example , 1984, Helgoländer Meeresuntersuchungen.

[57]  J. Buchner,et al.  Functional Characterization of the Higher Plant Chloroplast Chaperonins (*) , 1995, The Journal of Biological Chemistry.

[58]  M. M. Bradford A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. , 1976, Analytical biochemistry.