Skip to main content
Log in

Nutritional status affects the capacity of the snail Concholepas concholepas to synthesize Hsp70 when exposed to stressors associated with tidal regimes in the intertidal zone

  • Original Paper
  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

Synthesis of the heat shock protein Hsp70 is one of the most important physiological mechanisms that intertidal organisms possess to counteract damage to macromolecules caused by stressors associated with the tidal cycle. However, the synthesis and activity of Hsp70 involves an elevated energetic cost. We evaluated the effect of the nutritional status (fed vs. starved for 2 weeks) of juvenile Concholepas concholepas mollusc on their capacity to synthesize Hsp70 during emersion (i.e. low tide) and immersion (i.e. high tide) at high temperatures (24 °C, e.g. summer conditions) and at low temperatures (7 °C, e.g. winter conditions). In addition, we evaluated whether Hsp70 is induced directly upon exposure to stress (emersion) or during recovery (re-immersion). Starvation decreased the content of stored energy substrates of juveniles as well as their ability to synthesize Hsp70 during emersion under thermal stress, especially at high temperatures. Additionally, analysis of environmental factors associated with laboratory simulation of tidal regimes indicated that juveniles in starvation, in contrast to fed juveniles, did not significantly increase their levels of Hsp70 during cold emersion (7 °C) or warm emersion (24 °C) or upon re-immersion. Induction of Hsp70 occurred during exposure to stress (low-tide conditions) and not when juveniles returned to “normal” conditions (high-tide conditions). Thus, the synthesis of Hsp70 for the juveniles of this intertidal snail species was coordinated and adapted to the tidal cycle, and the species responds in a similar way to hot and cold emersion conditions. The observed levels of Hsp70 reflect the ability of the individual to synthesize these proteins, which is dependent on the nutritional status of the individual.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Baird NA, Turnbull DW, Johnson EA (2006) Induction of the heat shock pathway during hypoxia requires regulation of heat shock factor by hypoxia-inducible factor-1. J Biol Chem 281:38675–38681

    Article  CAS  Google Scholar 

  • Broitman B, Navarrete S, Smith F, Gaines S (2001) Geographic variation in southern Pacific intertidal communities. Mar Ecol Prog Ser 224:21–34

    Article  Google Scholar 

  • Brokordt K, Leiva N, Jeno K, Martínez G, Winkler F (2009) Effect of allozyme heterozygosity on basal and induced levels of heat shock protein (Hsp70), in juveniles Concholepas concholepas (Mollusca). J Exp Mar Biol Ecol 370:18–26

    Article  CAS  Google Scholar 

  • Brun N, Bricelj V, Macrae T, Ross N (2008) Heat shock protein responses in thermally stressed bay scallops, Argopecten irradians, and sea scallops, Placopecten magellanicus. J Exp Mar Biol Ecol 358:151–162

    Article  CAS  Google Scholar 

  • Byrne R, Gnaiger E, McMahon R, Dietz T (1990) Behavioral and metabolic responses to emersion and subsequent reimmersion in the freshwater bivalve, Corbicula fluminea. Bio Bull 178:251–259

    Article  Google Scholar 

  • Castilla J (1982) Gastropod mollusk fisheries in Chile: Concholepas concholepas, a case study. Monogr Biol 2:199–212

    Google Scholar 

  • Castilla J (1999) Coastal marine communities: trends and perspectives from human-exclusion experiments. Trends Ecol Evol 14:280–283

    Article  Google Scholar 

  • Castilla J, Cancino J (1979) Principales depredadores de Concholepas concholepas (Mollusca: Gastropoda: Muricidae) y observaciones preliminares sobre mecanismos conductuales de escape y defensa [Principal predators of Concholepas concholepas (Mollusca: Gastropoda: Muricidae) and preliminary observations of behavioral mechanisms of escape and defense]. Biol Pesq 12:115–123

    Google Scholar 

  • Castilla J, Durán L (1985) Human exclusion from the rocky intertidal zone of central of central Chile: the effects on Concholepas concholepas (Gastropoda). Oikos 45:391–399

    Article  Google Scholar 

  • Castilla J, Guisado C, Cancino J (1979) Aspectos Ecológicos y Conductuales Relacionados con la alimentación de Concholepas concholepas (Mollusca, Gastropoda, Muricidae) [Ecological and behavioral aspects related to feeding in Concholepas concholepas (Mollusca, Gastropoda, Muricidae)]. Biol Pesq 12:99–114

    Google Scholar 

  • Cheetham M, Caplan A (1998) Structure function and revolution of DnaJ: conservation and adaptation of chaperone function. Cell Stress Chaperones 3:28–36

    Article  CAS  Google Scholar 

  • Clark MS, Worland MR (2008) How insects survive the cold: molecular mechanisms—a review. J Comp Physiol B 278:917–933

    Article  CAS  Google Scholar 

  • Colinet H, Lee SF, Hoffmann A (2010) Temporal expression of heat shock genes during cold stress and recovery from chill coma in adult Drosophila melanogaster. FEBS J 277:174–185

    Article  CAS  Google Scholar 

  • Currie S, Tufts BL, Moyes CD (1999) Influence of bioenergetic stress on heat shock protein gene expression in nucleated red blood cells of fish. Am J Physiol 276:990–996

    Google Scholar 

  • Dahlhoff E, Buckley B, Menge B (2001) Physiology of the rocky intertidal predator Nucella ostrina along an environmental stress gradient. Ecology 82:2816–2829

    Article  Google Scholar 

  • Dahlhoff E, Stillman J, Menge B (2002) Physiological community ecology: variation in metabolic activity of ecologically important rocky intertidal invertebrates along environmental gradients. Integ Comp Biol 42:862–871

    Article  Google Scholar 

  • David E, Tanguy A, Pichavant K, Moraga D (2005) Response of the Pacific oyster Crassostrea gigas to hypoxia exposure under experimental conditions. FEBS J 272:5635–5652

    Article  CAS  Google Scholar 

  • Dong Y, Yu S, Wang Q, Dong S (2011) Physiological responses in a variable environment: relationships between metabolism, Hsp and thermotolerance in an intertidal species. PLoS One 6:e26446

    Article  CAS  Google Scholar 

  • Dorsey TE, McDonald PW, Roels OA (1977) A heated biuret-Folin protein assay which gives equal absorbance with different proteins. Anal Biochem 78:156–164

    Article  CAS  Google Scholar 

  • Dubois M, Gilles KA, Hamilton JK, Rebers PA, Smith F (1956) Colorimetric method for determination of sugars and related substances. Anal Chem 28:350–356

    Article  CAS  Google Scholar 

  • Durán L, Castilla J (1989) Variation and persistence of the middle intertidal community of central Chile, with and without human harvesting. Mar Biol 103:555–562

    Article  Google Scholar 

  • Dye A (1991) Feed preferences of Nucella crassilabrum and juvenile Concholepas concholepas (Gastropoda: Muricidae) from a rocky shore in southern Chile. J Moll Stud 57:301–307

    Article  Google Scholar 

  • Fan C, Lee S, Cyr D (2003) Mechanisms for regulation of Hsp70 function by Hsp40. Cell Stress Chaperones 8:309–316

    Article  CAS  Google Scholar 

  • Feder M, Hofmann G (1999) Heat shock proteins, molecular chaperones and the stress response: evolutionary and ecological physiology. Ann Rev Physiol 61:243–282

    Article  CAS  Google Scholar 

  • Fink A (1999) Chaperone-mediated protein folding. Physiol Rev 79:425–449

    CAS  Google Scholar 

  • Frydman J, Nimmesgern E, Ohtsuka K, Hartl F (1994) Folding of nascent polypeptide chains in a high molecular mass assembly with molecular chaperones. Nature 370:111–117

    Article  CAS  Google Scholar 

  • Gäde G (1988) Energy metabolism during anoxia and recovery in shell adductor and foot muscle of the gastropod mollusc Haliotis lamellosa: formation of the novel anaerobic end product tauropine. Biol Bull 175:1221–1231

    Article  Google Scholar 

  • Gething M, Sambrook J (1992) Protein folding in the cell. Nature 355:33–45

    Article  CAS  Google Scholar 

  • Goto SG, Kimura MT (1998) Heat- and cold-shock responses and temperature adaptations in subtropical and temperate species of Drosophila. J Insect Physiol 44:1233–1239

    Article  CAS  Google Scholar 

  • Guisado C, Castilla J (1983) Aspects of the ecology and growth of an intertidal juvenile population of Concholepas concholepas (Mollusca: Gastropoda: Muricidae) at Las Cruces, Chile. Mar Biol 78:99–103

    Article  Google Scholar 

  • Gutiérrez R, Gallardo C (1999) Prey attack, food preference and growth in juveniles of the edible muricid snail, Chorus giganteus. Aquaculture 174:69–79

    Article  Google Scholar 

  • Hartl FU (1996) Molecular chaperones in cellular protein folding. Nature 38:571–579

    Article  Google Scholar 

  • Helmuth B, Broitman B, Blanchette C, Gilman S, Halpin P et al (2006) Mosaic patterns of thermal stress in the rocky intertidal zone: implications for climate change. Ecol Monogr 76:461–479

    Article  Google Scholar 

  • Hochachka PW, Buck LT, Doll CJ, Land SC (1996) Unifying theory of hypoxia tolerance: molecular/metabolic defence and rescue mechanisms for surviving oxygen lack. Biochemistry 93:9493–9498

    CAS  Google Scholar 

  • Hofmann G, Somero G (1995) Evidence for protein damage at environmental temperatures: seasonal changes in levels of ubiquitina conjugates and Hsp70 in the intertidal mussel Mytilus trossulus. J Exp Biol 198:1509–1518

    CAS  Google Scholar 

  • Hong M, Kwon J, Shim J, Lee J (2004) Differential hypoxia response of Hsp-16 genes in the nematode. J Mol Biol 344:369–381

    Article  CAS  Google Scholar 

  • Hu MH, Wang Y, Tsang ST, Cheung SG, Shin PKS (2011) Effect of starvation on the energy budget of two Asian horseshoe crab species: Tachypleus tridentatus and Carcinoscorpius rotundicauda (Chelicerata: Xiphosura). Mar Biol 158:1591–1600

    Article  Google Scholar 

  • Iba K (2002) Acclimative response to temperature stress in higher plants: approaches of gene engineering for temperature tolerance. Ann Rev Plant Biol 53:225–245

    Article  CAS  Google Scholar 

  • Larade K, Storey KB (2002) Reversible suppression of protein synthesis in concert with polysome disaggregation during anoxia exposure in Littorina littorea. Mol Cell Biochem 232:121–127

    Article  CAS  Google Scholar 

  • Leiva G, Castilla J (2002) A review of world marine gastropod fishery: evolution of catches, management and the Chilean experience. Rev Fish Biol Fish 11:283–303

    Article  Google Scholar 

  • Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:262–265

    Google Scholar 

  • Lyytinen A, Mappes J, Lindström L (2012) Variation in Hsp70 levels after cold shock: signs of evolutionary responses to thermal selection among Leptinotarsadecem lineata populations. PLoS One 7:e31446

    Article  CAS  Google Scholar 

  • Madeira D, Narciso L, Cabral HN, Vinagre C, Diniz MS (2012) HSP70 production patterns in coastal and estuarine organisms facing increasing temperatures. J Sea Res 73:137–147

    Article  CAS  Google Scholar 

  • Maĭsov A, Podlipaeva Y, Kipyatkov V (2007) Expression of stress proteins of HSP70 family in response to cold in Myrmica ants from various geographic populations. Cell Tissue Biol 1:434–438

    Article  Google Scholar 

  • Mann R, Gallager SM (1985) Physiological and biochemical energetics of larvae of Teredo navalis L. and Namkia gouldi (Bartsch) (Bivalvia: Teredinidae). J Exp Mar Biol Ecol 85:211–228

    Article  CAS  Google Scholar 

  • Martínez P, Navarrete S (2002) Temporal and spatial variation in settlement of the gastropod Concholepas concholepas in natural and artificial substrata. J Mar Biol Assoc UK 82:257–264

    Article  Google Scholar 

  • Martínez J, Perez-Serrano J, Bernadina WE, Rodríguez-Caabeiro F (2001) Stress response to cold in Trichinella species. Cryobiology 43:293–302

    Article  CAS  Google Scholar 

  • McGaw IJ (2003) Behavioral thermoregulation in Hemigrapsus nudus, the amphibious purple shore crab. Biol Bull 204:38–49

    Article  CAS  Google Scholar 

  • Menge B, Farrell T (1989) Community structure and interaction webs in shallow marine hard-bottom communities: tests of an environmental stress model. Adv Ecol Res 19:189–262

    Article  Google Scholar 

  • Monaco C, Brokordt K, Gaymer C (2010) Latitudinal thermal gradient effects on the cost of living of the intertidal porcelain crab Petrolisthes granulosus. Aquat Biol 9:23–33

    Article  Google Scholar 

  • Moreno C, Ascencio G, Ibáñez S (1993) Patrones de asentamiento de Concholepas concholepas (Bruguière) (Mollusca: Muricidae) en la zona intermareal rocosa de Valdivia, Chile [Settlement patterns of Concholepas concholepas (Bruguière) (Mollusca: Muricidae) in the rocky intertidal zone of Valdivia, Chile]. Rev Chil Hist Nat 66:93–101

    Google Scholar 

  • Morris JP, Thatje S, Hauton C (2013) The use of stress-70 proteins in physiology: a re-appraisal. Mol Ecol 22:1494–1502

    Article  CAS  Google Scholar 

  • Muñoz J, Finke GR, Camus PA, Bozinovic F (2005) Thermoregulatory behavior, heat gain and thermal tolerance in the periwinkle Echinolittorina peruviana in central Chile. Comp Biochem Physiol A Physiol 142:92–98

    Article  CAS  Google Scholar 

  • Newell R (1979) Biology of intertidal animals. Marine Ecological Surveys, Faversham

    Google Scholar 

  • Olivares A (2003) Inanición forzada de Concholepas concholepas Bruguiére, 1789 (Gastropoda, Muricidae): efecto sobre crecimiento, composición bioquímica, índice de condición y capacidad de recuperación [Forced starvation of Concholepas concholepas Bruguiére, 1789 (Gastropoda, Muricidae): the effect on growth, biochemical composition, condition index and resilience. Universidad Católica del Norte

  • Oliveira G, Eichler P, Rossi I, Da Silva R (2004) Hepatopancreas gluconeogenesis during anoxia and post-anoxia recovery in Chasmagnathus granulata crabs maintained on high-protein or carbohydrate-rich diets. J Exp Zool 301:240–248

    Article  CAS  Google Scholar 

  • Paine R (1977) Controlled manipulations in the marine intertidal zone and their contributions to ecological theory (special publication). Acad Nat Sci Phila 12:245–270

    Google Scholar 

  • Paine R, Castilla J, Cancino J (1985) Perturbation and recovery patterns of starfish-dominated intertidal assemblages in Chile, New Zealand, and Washington State. Am Nat 125:679–691

    Article  Google Scholar 

  • Parsell D, Lindquist S (1994) Heat shock proteins and stress tolerance. In: Morimoto RI, Tissieres A, Georgopoulos C (eds) The Biology of heat shock proteins and molecular chaperones. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, pp 457–494

    Google Scholar 

  • Samples BL, Pool GL, Lumb RH (1999) Polyunsaturated fatty acids enhance the heat induced stress response in rainbow trout (Oncorhynchus mykiss) leukocytes. Comp Biochem Physiol 123:389–397

    Article  CAS  Google Scholar 

  • SAS Institute (1999) SAS/STAT user’s guide, release 8.02 ed. SAS Institute Press, Cary

    Google Scholar 

  • Sejerkilde M, Sørensen JG, Loeschcke V (2003) Effects of cold- and heat-hardening on thermal resistance and Hsp70 expression in Drosophila melanogaster. J Insect Physiol 49:719–726

    Article  CAS  Google Scholar 

  • Sharma SK, De Los Rios P, Christen P, Lustig A, Goloubinoff P (2010) The kinetic parameters and energy cost of the Hsp70 chaperone as a polypeptide unfoldase. Nat Chem Biol 6:914–920

    Article  CAS  Google Scholar 

  • Simon M, Reikerstorfer A, Schwarz A, Krone C, Luger T (1995) Heat shock protein 70 overexpression affects the response to ultraviolet light in murine fibroblasts: evidence for increased cell viability and suppression of cytokine release. J Clin Invest 95:926–933

    Article  CAS  Google Scholar 

  • Snedecor GW, Cochran WG (1989) Statistical methods. Iowa State University Press, Ames

    Google Scholar 

  • Sokal R, Rohlf J (1981) Biometry, 2nd edn. WH Freeman and Company, New York

    Google Scholar 

  • Sokolova I, Pörtner H (2001) Temperature effects on key metabolic enzymes in Littorina saxatilis and L. obtusata from different latitudes and shore levels. Mar Biol 139:113–126

    Article  CAS  Google Scholar 

  • Sokolova M, Pörtner H (2003) Metabolic plasticity and critical temperatures for aerobic scope in a eurythermal marine invertebrate (Littorina saxatilis, gastropoda: Littorinidae) from different latitudes. J Exp Biol 206:195–207

    Article  Google Scholar 

  • Somero G (2002) Thermal physiology and vertical zonation of intertidal animals: optima, limits, and costs of living. Integr Comp Biol 42:780–789

    Article  Google Scholar 

  • Sonna LA, Fujita J, Gaffin SL, Lilly CM (2002) Effects of heat and cold stress on mammalian gene expression. J Appl Physiol 92:1725–1742

    CAS  Google Scholar 

  • Sørensen JG (2010) Application of heat shock protein expression for detecting natural adaptation and exposure to stress in natural populations. Curr Zool 56:703–713

    Google Scholar 

  • Soto F (1996) Estructura gremial de un ensamble de depredadores de la zona intermareal rocosa en Chile central [Guild structure of an assembly of predators along the rocky intertidal zone of central Chile]. Invest Mar 24:97–105

    Article  Google Scholar 

  • Stillman JH, Somero GN (2000) A comparative analysis of the upper thermal tolerance limits of eastern Pacific porcelain crabs, Genus Petrolisthes: influences of latitude, vertical zonation, acclimation, and phylogeny. Physiol Biochem Zool 73:200–208

    Article  CAS  Google Scholar 

  • Stotz W, Amesti P, Martínez D, Pérez E (1991) Lugares de asentamiento y desarrollo de juveniles de Concholepas concholepas (Bruguière 1789) en ambientes inter y submareales de la IV Región, Coquimbo, Chile [Settlement areas and the development of Concholepas concholepas juveniles (Bruguière 1789) in the intertidal and subtidal environments of Region IV, Coquimbo, Chile]. Rev Biol Mar 26:351–361

    Google Scholar 

  • Stuardo J (1979) Sobre clasificación, distribución y variación de Concholepas concholepas (Bruguière, 1789): un estudio de taxonomía [On the classification, distribution and variation of Concholepas concholepas (Bruguière, 1789): a study of taxonomy]. Biol Pesq 12:5–38

    Google Scholar 

  • Teixeira T, Diniz M, Calado R, Rosa R (2013) Coral physiological adaptations to air exposure: heat shock and oxidative stress responses in Veretillum cynomorium. J Exp Mar Biol Ecol 439:35–41

    Article  CAS  Google Scholar 

  • Tomanek L (2002) The heat-shock response: its variation, regulation and ecological importance in intertidal gastropods (genus Tegula). Int Comp Biol 42:797–807

    Article  CAS  Google Scholar 

  • Tomanek L, Sanford E (2003) Heat-shock protein 70 (Hsp70) as a biochemical stress indicator: an experimental field test in two congeneric intertidal gastropods (genus Tegula). Biol Bull 205:276–284

    Article  CAS  Google Scholar 

  • Tomanek L, Somero G (1999) 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. J Exp Biol 202:2925–2936

    Google Scholar 

  • Tran D, Bourdineaud J, Massabuauy J, Garnier-Laplace J (2005) Modulation of uranium bioaccumulation by hypoxia in the freshwater clam Corbicula fluminea: induction of multi-xenobiotic resistance protein and heat shock protein 60 in gill tissues. Environ Toxicol Chem 24–9:2278–2284

    Article  Google Scholar 

  • Valle-Levinson A, Moraga-Opazo J (2006) Observations of bipolar residual circulation in two equatorward-facing semiarid bays. Cont Shelf Res 26:179–193

    Article  Google Scholar 

  • Valle-Levinson A, Moraga J, Olivares J, Blanco JL (2000) Tidal and residual circulation in a semi-arid bay: Coquimbo Bay, Chile. Cont Shelf Res 20:2009–2028

    Article  Google Scholar 

  • Wells RMG, Baldwin J (1995) A comparison of metabolic stress during air exposure in two species of New Zealand abalone, Haliotis iris and Haliotis australis: implications for the handling and shipping of live animals. Aquaculture 134:361–370

    Article  Google Scholar 

  • Williams GA, De Pirro M, Leung KMY, Morritt D (2005) Physiological responses to heat stress on a tropical shore: the benefits of mushrooming behaviour in the limpet Cellana grata. Mar Ecol Prog Ser 292:213–224

    Article  Google Scholar 

Download references

Acknowledgments

We are grateful to Nicolás Leiva and Gabriela Núñez for their help with animal manipulation during the experiments. We specially express thanks to Tatiana Manzur for her help with the data analyses and Mauricio Soler and Roxana González for their help with the figures. This study was supported by FONDECYT 1050291 funding to KB.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Katherina Brokordt.

Additional information

Communicated by H. Pörtner.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Jeno, K., Brokordt, K. Nutritional status affects the capacity of the snail Concholepas concholepas to synthesize Hsp70 when exposed to stressors associated with tidal regimes in the intertidal zone. Mar Biol 161, 1039–1049 (2014). https://doi.org/10.1007/s00227-014-2397-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00227-014-2397-7

Keywords

Navigation