Heat-shock response in Patagonian gastropods

Rocío Nieto-Vilela, Federico Márquez, Gregorio Bigatti, Sebastian Giulianelli

Resumen


The physiological process to counteract environmental stress are extremely diverse in marine species that inhabit intertidal zones. Ecological approaches have demonstrated a variety of adaptations among narrowly distributed species. The present study is focused on physiological responses of two key marine gastropods from Atlantic Patagonia, living in one of the most stressful intertidal rocky shores of the world: Tegula patagonica and Trophon geversianus. We evaluated the body temperature and its heat-shock response by Hsp70 expression. Our results suggest that T. geversianus, inhabiting the mid-intertidal zone and exposed for longer to aerial conditions, presents better physiological and behavioral adaptations to temperature than T. patagonica, living in the low intertidal with less physical stress. Tegula patagonica seems to have an inefficient thermal defense, an inability to upregulate Hsp70 expression against water temperature increase. Contrariwise, a significant upregulation of Hsp70 was registered in T. geversianus added to a protective behavior of hiding during periods of high temperature. These results will be useful as a reference for monitoring sentinel species to assess real-time changes in coastal intertidal communities due to global warming.


Palabras clave


Thermal stress; Patagonian gastropods; strategies; rocky shores; Hsp70

Texto completo:

PDF (English)

Referencias


Arribas, L.P., J.E. Alfaya, M.G. Palomo, S. Giulianelli, R.A. Nieto-Vilela & G. Bigatti 2021. Ocean warming lead to heat shock protein expression and decrease in the feeding rate of the Patagonian sea star Anasterias minuta. Journal of Experimental Marine Biology and Ecology 546:151661.

Acker, J.G. & G. Leptoukh. 2007. Online analysis enhances use of NASA earth science data. Transactions American Geophysical Union 88:14-17.

Andrade, C. & C. Ríos. 2007. Experimental Study on the Feeding Habits of Trophon geversianus (Pallas 1774) (Gastropoda: Muricidae): prey selection and manipulation. Anales del Instituto de la Patagonia 35:45-54.

Avaca, M.A., A. Roche, M. Maggioni, J. Coronel & N. Cetra. 2021 Effects of epiphytic Ulva spp. on the marine snail Tegula patagonica (D'Orbigny, 1840) in a coastal Patagonian Bay. Estuarine, Coastal and Shelf Science 252:107275.

Bazterrica, M.C., B.R. Silliman, F.J. Hidalgo, C.M. Crain & M.D. Bertness. 2007. Limpet grazing on a physically stressful Patagonian rocky shore. Journal of Experimental Marine Biology and Ecology 353:22-34.

Bertness, M.D., S.D. Gaines & M.E. Hay. 2001. Marine community ecology 3 edn. Sinauer Associates Sunderland: Massachusetts, 369 pp.

Bertness, M.D., C.M. Crain, B.R. Silliman, M.C. Bazterrica, M.V. Reyna, F. Hildago & J. Farina. 2006. The community structure of western atlantic patagonian rocky shores. Ecolology Monographs 76:439-460.

Boraso de Zaixso, A.L., & H.E. Zaixso. 2015. La zona costera patagónica argentina. Universidad Nacional de la Patagonia San Juan Bosco-Intituto de Desarrollo. Chapter 2, El Bentos Costero Patagónico; pp. 43-138

Choi, Y.H., E.Y. Kim & T.J. Nam. 2018. Involvement of insulin-like growth factor in intraspecific variation in growth of Pacific oyster Crassostrea gigas during winter. Fisheries science 84:1017-1024.

Crespi, A.C., G. Soria, A. De Cian & C. López-Moreno. 2018. Roaring forties: An analysis of a decadal series of data of dust in Northern Patagonia. Atmospheric Environment 177:111-119.

Cumplido, M., A. Averbuj & G. Bigatti. 2010. Reproductive seasonality and oviposition induction in Trophon geversianus (Gastropoda: Muricidae) from Golfo Nuevo, Argentina. Journal Shellfish Research 29:423-428.

Dellatorre, F.G., J.P. Pisoni, P.J. Barón & A.L. Rivas. 2012. Tide and wind forced nearshore dynamics in Nuevo Gulf (Northern Patagonia, Argentina): Potential implications for cross-shore transport. Journal of Marine Systems 96:82-89.

Denny, M.W. & D.S. Wethey. 2001. Physical processes that generate patterns in marine communities. Chapter 1 in: M.D. Bertness, S.D. Gaines & M.E. Hay (ed.), Marine Community Ecology, pp. 3-37, Sunderland: Sinauer Associates Inc.

Dong, Y., L.P. Miller, J.G. Sanders & G. Somero. 2008. Heat-Shock Protein 70 (Hsp70) expression in four limpets of the genus Lottia: interspecific variation in constitutive and inducible synthesis correlates with in situ exposure to heat stress. The Biological Bulletin 215:173-181.

EMA Frumento, O. 1982. Estación Meteorlógica Autónoma. [accessed 2019].

Evans, T.G. & G.N. Somero. 2010. Phosphorylation events catalyzed by major cell signaling proteins differ in response to thermal and osmotic stress among native (Mytilus californianus and Mytilus trossulus) and invasive (Mytilus galloprovincialis) species of mussels. Physiological and Biochemical Zoology, 83:984-996.

Feder, M.E. & G.E. Hofmann. 1999. Heat-shock proteins, molecular chaperones, and the stress response: Evolutionary and Ecological Physiology. Annual review of physiology 61:243-282.

Giulianelli, S., M. Riggio, T. Guillardoy, C. Pérez Piñero, M.A. Gorostiaga, G. Sequeira & C. Lanari. 2019. FGF2 induces breast cancer growth through ligand‐independent activation and recruitment of ERα and PRBΔ4 isoform to MYC regulatory sequences. International journal of cancer 145:1874-1888.

Griffin, M. & G. Pastorino. 2005 The genus Trophon Monfort, 1810 (Gastropoda: Muricidae) in the Tertiary of Patagonia. Journal Paleontology 79:296-311.

Hofmann, G.E. 1999. Ecologically relevant variation in induction and function of heat shock proteins in marine organisms. American Zoologist 39:889-900.

Jeno, K. & K. Brokordt. 2014. 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. Marine Biology 161:1039-1049.

Nakano, K. & G.K. Iwama. 2002. The 70-kDa heat shock protein response in two intertidal sculpins, Oligocottus maculosus and O. snyderi: relationship of hsp70 and thermal tolerance. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology 133:79-94.

Lima, F.P., F. Gomes, R. Seabra, D.S. Wethey, M.l. Seabra, T. Cruz, A.M. Santos & T.J. Hilbish, 2016. Loss of thermal refugia near equatorial range limits. Global change biology 22:254-263.

Lindquist, S. 1986 The heat-shock response. Annual Review of Biochemistry 55:1151-1191.

Long, L.L., Y.L. Han, Z. Sheng, C. Du, Y.F. Wang & J.Q. Zhu. 2015. Expression analysis of HSP70 in the testis of Octopus tankahkeei under thermal stress. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology 187:150-159.

Lowry, O.H., A.L. Farr, N.J. Rosebrough & R.J. Ryall. 1951. Protein measurement of emulsifying capacity by electrical resistance. Food Science 193, 265-275.

Menge, B.A. & G.M. Branch. 2001. Rocky intertidal communities. Chapter 13 In: M.D. Bertness, S.D. Gaines& M.E. Hay (ed). Marine Community Ecology, pp. 211-254, Sunderland: Sinauer Associates, Inc.

Miloslavich, P., J.J. Cruz-Motta, A. Hernández, C. Herrera, E. Klein, F. Barros, G. Bigatti, M. Cárdenas, A. Carranza & A. Flores. 2016. Marine Benthos. Chapter 3 in: Benthic assemblages in South American intertidal rocky shores: biodiversity, services, and threats, pp.83-138.

Mizrahi, T., J. Heller, S. Goldenberg & Z. Arad. 2011. Heat shock protein expression in relation to reproductive cycle in land snails: Implications for survival. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology 160, 149-155.

Nieto-Vilela, R.A. 2014. Thesis: Composición proximal y Toxina Paralizante de Moluscos en los gasterópodos con potencial pesquero Nacella magellanica y Tegula patagonica de Norpatagonia. In: Facultad de Ciencias Naturales. Universidad de la Patagonia San Juan Bosco Puerto Madryn.

Nieto-Vilela, R.A. 2020. PhD. Thesis: Efecto del estrés físico y el calentamiento global sobre gasterópodos marinos de costas rocosas patagónicas. In: Departamento de Biología y Ambiente. Universidad Nacional de la Patagonia San Juan Bosco Comodoro Rivadavia, p. 174.

Nieto-Vilela, R.A., M. Cumplido, S. Zabala & G. Bigatti. 2021. Biochemical composition during the reproductive cycle of a novel gastropod resource from Atlantic Patagonia. Marine and Freshwater Research.

Palomo, M.G., M. Bagur, S. Calla, M. Cecilia, S.A.S. Dalton & S.J. Hawkins. 2019. Biodiversity and interactions on the intertidal rocky shores of Argentina (South-West Atlantic). Chapter 7 in: Hawkins SJ, Bohn K, Williams GA. Interactions in the Marine Benthos. Oxford, p 164-189.

Pastorino, G. 2005. A revision of the genus Trophon montfort, 1810 (Gastropoda: Muricidae) from southern south America. The Nautilus 119:55-82.

Pastorino, G. 1994 Moluscos costeros recientes de Puerto Piramide, Chubut, Argentina. Academia Nacional de Ciencias, Córdoba.

Pöhlmann, K., S. Koenigstein, K. Alter, D. Abele & C. Held. 2011. Heat-shock response and antioxidant defense during air exposure in patagonian shallow-water limpets from different climatic habitats. Cell Stress and Chaperones 16: 621-632.

Porter, W.P. & D.M. Gates. 1969. Thermodynamic equilibria of animals with environment. Ecology Monographs 39:227-244.

Raffaelli, D. & S.J. Hawkins. 2012. Intertidal ecology. London: Springer Science & Business Media, 356 pp.

Rechimont, M.E., D. Galván, M.C. Sueiro, G. Casas, M.L. Piriz, M.E. Diez, M. Primost, S. Zabala, F. Márquez, M.M. Brogger, J.E. Fernández Alfaya & G. Bigatti. 2013. Benthic diversity and community structure of a north patagonian rocky shore. Journal of the Marine Biological Association of the United Kingdom 93: 2049-2058.

Silliman, B.R., M.D. Bertness, A.H. Altieri, J.N. Griffin, M.C. Bazterrica, F.J. Hidalgo, C.M. Crain & M.V. Reyna. 2011. Whole-community facilitation regulates biodiversity on patagonian rocky shores. PLoS ONE 6: 10.

Smolina, I., S. Kollias, A. Jueterbock, J.A. Coyer & G. Hoarau. 2016. Variation in thermal stress response in two populations of the brown seaweed, Fucus distichus, from the Arctic and subarctic intertidal. Royal Society Open Science 3:150429.

Somero, G. 2002. Thermal physiology and vertical zonation of intertidal animals: Optima, limits, and costs of living. Integrative and Comparative Biology 42:780-789.

Sorte, C.J.B. & G.E. Hofmann. 2004. Changes in latitudes, changes in aptitudes: Nucella canaliculata (Mollusca: Gastropoda) is more stressed at its range edge. Marine Ecology Progress Series 274:263-268.

Sukhan, Z.P., M. Sharker, Y. Cho, S. Hossen, K.S. Choi & K.H. Kho. 2021. Thermal stress affects gonadal maturation by regulating GnRH, GnRH receptor, APG Wamide, and serotonin receptor gene expression in male pacific abalone, Haliotis discus hannai during breeding season. Frontiers in Marine Science 8:664426

Teso, S.V., G. Bigatti, G.N. Casas, L. Piriz & P.E. Penchaszadeh. 2009. Do native grazers from Patagonia, Argentina, consume the invasive kelp Undaria pinnatifida? Revista del Museo Argentino de Ciencias Naturales 11:7-14.

Tomanek, L. & G. Somero. 2000. Time course and magnitude of synthesis of heat‐shock proteins in congeneric marine snails (genus Tegula) from different tidal heights. Journal of Physiology and Biochemistry Zoology 73:249-256.

Tomanek, L. & E. Sanford. 2003. Heat-Shock Protein 70 (Hsp70) as a biochemical stress indicator: An experimental field test in two congeneric intertidal gastropods (Genus: Tegula). Biological Bulleting 205:276-284.

Tomanek, L. & M.L. Zuzow. 2010. The proteomic response of the mussel congeners Mytilus galloprovincialis and M. trossulus to acute heat stress: implications for thermal tolerance limits and metabolic costs of thermal stress. Journal of Experimental Biology 213:3559-3574.


Enlaces refback

  • No hay ningún enlace refback.


Creative Commons License
This work is licensed under a Creative Commons Attribution 3.0 License.