Effects of seawater temperature increase on economically relevant native and introduced clam species.

As a consequence of climate change, global warming is expected to increase during the 21st century. Taking this into account, the impact of rising temperatures on the native Ruditapes decussatus and introduced R. philippinarum bivalve species was assessed, through biochemical and mRNA transcription analyses. Our findings showed that at 21 °C the electron transport system and antioxidant enzyme activity, as well as the expression of Hsp70 gene were induced in R. decussatus when compared with 17 °C. On the other hand, at 25 °C results suggested that R. decussatus closed their valves during short periods, as a behavioral strategy, down-regulating the expression of genes associated with mitochondrial metabolism (Cox-1 and 16S) and chaperone function (Hsp70) compared with organisms at 17 °C. In addition, the introduced species (R. philippinarum) increased the electron transport system and antioxidant activities, as well as gene expression of antioxidant enzymes and molecular chaperone (Hsp70) at 21 °C. However, antioxidant mechanisms were not enough to prevent lipid membrane damages at 21 °C. At 25 °C R. philippinarum presented increased electron transport system and antioxidant activity, as well as the expression of genes associated with apoptosis regulation and molecular chaperone. Overall, the present findings indicate that in a global warming scenario both species are able to induce different mechanisms to mitigate the impacts of temperature increase.

[1]  A. Hamdoun,et al.  Phenotypic Plasticity of HSP70 and HSP70 Gene Expression in the Pacific Oyster (Crassostrea gigas): Implications for Thermal Limits and Induction of Thermal Tolerance , 2003, The Biological Bulletin.

[2]  B. Maher,et al.  Establishing metal exposure - dose - response relationships in marine organisms: illustrated with a case study of cadmium toxicity in tellina deltoidalis , 2010 .

[3]  C. Choi,et al.  Characterization and mRNA expression of Mn-SOD and physiological responses to stresses in the Pacific oyster Crassostrea gigas , 2009 .

[4]  D. Abele,et al.  From bivalves to birds : oxidative stress and longevity , 2010 .

[5]  Jacqueline de Chazal,et al.  Climate change 2007 : impacts, adaptation and vulnerability : Working Group II contribution to the Fourth Assessment Report of the IPCC Intergovernmental Panel on Climate Change , 2014 .

[6]  B. Hoffman,et al.  Gadd45 in stress signaling , 2008, Journal of molecular signaling.

[7]  A. Tanguy,et al.  Identification of differentially expressed genes of the Pacific oyster Crassostrea gigas exposed to prolonged thermal stress , 2007, The FEBS journal.

[8]  M. Pardal,et al.  Latitudinal gradients in Scrobicularia plana reproduction patterns, population dynamics, growth, and secondary production , 2011 .

[9]  G. Chainy,et al.  Biochemical markers of oxidative stress in Perna viridis exposed to mercury and temperature. , 2007, Chemico-biological interactions.

[10]  Jianshi Lin,et al.  Seawater Acidification and Elevated Temperature Affect Gene Expression Patterns of the Pearl Oyster Pinctada fucata , 2012, PloS one.

[11]  R. Lanciotti,et al.  Depuration of striped venus clam (Chamelea gallina L.): effects on microorganisms, sand content, and mortality. , 2009, Journal of food science.

[12]  H. Pörtner,et al.  Temperature-dependence of mitochondrial function and production of reactive oxygen species in the intertidal mud clam Mya arenaria. , 2002, The Journal of experimental biology.

[13]  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.

[14]  S. Arnold,et al.  Inducers of Chemical Hypoxia Act in a Gender- and Brain Region-Specific Manner on Primary Astrocyte Viability and Cytochrome c Oxidase , 2011, Neurotoxicity Research.

[15]  Dario Savini,et al.  Monitoring marine invasive species in Mediterranean marine protected areas (MPAs) : a strategy and practical guide for managers , 2013 .

[16]  M. Pardal,et al.  Long‐term monitoring of a mercury contaminated estuary (Ria de Aveiro, Portugal): the effect of weather events and management in mercury transport , 2014 .

[17]  G. Hofmann,et al.  Transcriptomic response of sea urchin larvae Strongylocentrotus purpuratus to CO2-driven seawater acidification , 2009, Journal of Experimental Biology.

[18]  I. Fridovich,et al.  Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. , 1971, Analytical biochemistry.

[19]  P. Luttikhuizen,et al.  Seasonal variability in somatic and reproductive investment of the bivalve Scrobicularia plana (da Costa, 1778) along a latitudinal gradient , 2011 .

[20]  Chhandak Basu,et al.  Real‐time PCR (qPCR) primer design using free online software , 2011, Biochemistry and molecular biology education : a bimonthly publication of the International Union of Biochemistry and Molecular Biology.

[21]  G. Somero,et al.  Rhythms of Gene Expression in a Fluctuating Intertidal Environment , 2008, Current Biology.

[22]  T. Nalepa,et al.  Seasonal changes in the respiratory electron transport system (ETS) and respiration of the zebra mussel, Dreissena polymorpha in Saginaw Bay, Lake Huron , 2001, Hydrobiologia.

[23]  M. Marin,et al.  Effects of high temperatures on functional responses of haemocytes in the clam Chamelea gallina. , 2007, Fish & shellfish immunology.

[24]  P. Blier,et al.  Thermal sensitivity of metabolic enzymes in subarctic and temperate freshwater mussels (Bivalvia: Unionoida) , 2010 .

[25]  Doris Schiedek,et al.  Interactions between climate change and contaminants. , 2007, Marine pollution bulletin.

[26]  G. Somero,et al.  Invasive and native blue mussels (genus Mytilus) on the California coast: the role of physiology in a biological invasion. , 2011 .

[27]  S. Aust,et al.  Microsomal lipid peroxidation. , 1978, Methods in enzymology.

[28]  F. D. King,et al.  Respiration and the activity of the respiratory electron transport system in marine zooplankton1 , 1975 .

[29]  S. Haldar,et al.  The relationship between BcI2, Bax and p53: consequences for cell cycle progression and cell death. , 1998, Molecular human reproduction.

[30]  F. Spaccesi.  Abundance, recruitment, and shell growth of the exotic mussel Limnoperna fortunei in the Río de la Plata (Argentina) , 2013, Zoological Studies.

[31]  J. Widdows,et al.  Effects of elevated temperatures on the scope for growth and resistance to air exposure of the clam Ruditapes decussatus (L.), from southern Portugal* , 1997 .

[32]  H. W. Robinson,et al.  THE BIURET REACTION IN THE DETERMINATION OF SERUM PROTEINS I. A STUDY OF THE CONDITIONS NECESSARY FOR THE PRODUCTION OF A STABLE COLOR WHICH BEARS A QUANTITATIVE RELATIONSHIP TO THE PROTEIN CONCENTRATION , 1940 .

[33]  G. Somero,et al.  Thermal limits and adaptation in marine Antarctic ectotherms: an integrative view , 2007, Philosophical Transactions of the Royal Society B: Biological Sciences.

[34]  R. Freitas,et al.  Spatial distribution and bioaccumulation patterns in three clam populations from a low contaminated ecosystem , 2015 .

[35]  A. Scorilas,et al.  Alterations in mRNA Expression of Apoptosis‐Related Genes BCL2, BAX, FAS, Caspase‐3, and the Novel Member BCL2L12 after Treatment of Human Leukemic Cell Line HL60 with the Antineoplastic Agent Etoposide , 2006, Annals of the New York Academy of Sciences.

[36]  Corinne Le Quéré,et al.  Climate Change 2013: The Physical Science Basis , 2013 .

[37]  W. S. Lakra,et al.  Molecular identification and phylogenetic relationships of seven Indian Sciaenids (Pisces: Perciformes, Sciaenidae) based on 16S rRNA and cytochrome c oxidase subunit I mitochondrial genes , 2009, Molecular Biology Reports.

[38]  Thomas D. Schmittgen,et al.  Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. , 2001, Methods.

[39]  A. Ivanina,et al.  Interactive effects of elevated temperature and CO(2) levels on metabolism and oxidative stress in two common marine bivalves (Crassostrea virginica and Mercenaria mercenaria). , 2013, Comparative biochemistry and physiology. Part A, Molecular & integrative physiology.

[40]  V. Quintino,et al.  Effects of depuration on the element concentration in bivalves: Comparison between sympatric Ruditapes decussatus and Ruditapes philippinarum , 2012 .

[41]  J. Marques,et al.  The impact of estuarine salinity changes on the bivalves Scrobicularia plana and Cerastoderma edule, illustrated by behavioral and mortality responses on a laboratory assay , 2015 .

[42]  N. Bandarra,et al.  Effect of warming on protein, glycogen and fatty acid content of native and invasive clams. , 2014, Food research international.

[43]  Marco Munari,et al.  Combined effects of temperature and salinity on functional responses of haemocytes and survival in air of the clam Ruditapes philippinarum. , 2011, Fish & shellfish immunology.

[44]  M. Grieshaber,et al.  Energy metabolism and valve closure behaviour in the Asian clam Corbicula fluminea , 2003, Journal of Experimental Biology.

[45]  Vincent R. Gray.  Climate Change 2007: The Physical Science Basis Summary for Policymakers , 2007 .

[46]  C. Paillard,et al.  Effect of temperature on defense parameters in manila clam Ruditapes philippinarum challenged with Vibrio tapetis. , 2004, Diseases of aquatic organisms.

[47]  A. Eissa,et al.  The impact of global climatic changes on the aquatic environment , 2011 .

[48]  M. Delgado,et al.  Comparative study of gonadal development of Ruditapes philippinarum (Adams and Reeve) and Ruditapes decussatus (L.) (Mollusca: Bivalvia): Influence of temperature , 2007 .

[49]  Cascade J. B. Sorte,et al.  Geographic Variation in Temperature Tolerance as an Indicator of Potential Population Responses to Climate Change , 2011 .

[50]  H. Pörtner,et al.  Behavioral, metabolic, and molecular stress responses of marine bivalve Mytilus galloprovincialis during long-term acclimation at increasing ambient temperature. , 2007, American journal of physiology. Regulatory, integrative and comparative physiology.

[51]  S. Pouvreau,et al.  Metabolic adjustments in the oyster Crassostrea gigas according to oxygen level and temperature , 2007 .

[52]  S. Yum,et al.  Expressions of oxidative stress-related genes and antioxidant enzyme activities in Mytilus galloprovincialis (Bivalvia, Mollusca) exposed to hypoxia , 2013, Zoological Studies.

[53]  M. Marin,et al.  Can the combination of decreased pH and increased temperature values induce oxidative stress in the clam Chamelea gallina and the mussel Mytilus galloprovincialis? , 2013, Marine pollution bulletin.

[54]  G. Hofmann,et al.  Effect of pH on Gene Expression and Thermal Tolerance of Early Life History Stages of Red Abalone (Haliotis rufescens) , 2010 .

[55]  J. Lajtner,et al.  Differences in tolerance to anthropogenic stress between invasive and native bivalves. , 2016, The Science of the total environment.

[56]  M. Nunes,et al.  Ecophysiology of native and alien-invasive clams in an ocean warming context. , 2014, Comparative biochemistry and physiology. Part A, Molecular & integrative physiology.

[57]  N. C. Gomes,et al.  Short-term variability of abundance, diversity and activity of estuarine bacterioneuston and bacterioplankton , 2009 .

[58]  D. Posada,et al.  Gene expression analysis of clams Ruditapes philippinarum and Ruditapes decussatus following bacterial infection yields molecular insights into pathogen resistance and immunity. , 2012, Developmental and comparative immunology.

[59]  H. Pörtner,et al.  Metabolic and molecular stress responses of sublittoral bearded horse mussel Modiolus barbatus to warming sea water: implications for vertical zonation , 2008, Journal of Experimental Biology.

[60]  C. Paillard,et al.  Interactive effects of metal contamination and pathogenic organisms on the marine bivalve Cerastoderma edule. , 2010, Marine pollution bulletin.

[61]  C. Lambert,et al.  Brown muscle disease: impact on Manila clam Venerupis (=Ruditapes) philippinarum biology. , 2014, Fish & shellfish immunology.

[62]  Colin R. Janssen,et al.  The use of biomarkers in Daphnia magna toxicity testing. IV. Cellular Energy Allocation: a new methodology to assess the energy budget of toxicant-stressed Daphnia populations , 1997 .