Early development and molecular plasticity in the Mediterranean sea urchin Paracentrotus lividus exposed to CO2-driven acidification

SUMMARY Ocean acidification is predicted to have significant effects on benthic calcifying invertebrates, in particular on their early developmental stages. Echinoderm larvae could be particularly vulnerable to decreased pH, with major consequences for adult populations. The objective of this study was to understand how ocean acidification would affect the initial life stages of the sea urchin Paracentrotus lividus, a common species that is widely distributed in the Mediterranean Sea and the NE Atlantic. The effects of decreased pH (elevated PCO2) were investigated through physiological and molecular analyses on both embryonic and larval stages. Eggs and larvae were reared in Mediterranean seawater at six pH levels, i.e. pHT 8.1, 7.9, 7.7, 7.5, 7.25 and 7.0. Fertilization success, survival, growth and calcification rates were monitored over a 3 day period. The expression of genes coding for key proteins involved in development and biomineralization was also monitored. Paracentrotus lividus appears to be extremely resistant to low pH, with no effect on fertilization success or larval survival. Larval growth was slowed when exposed to low pH but with no direct impact on relative larval morphology or calcification down to pHT 7.25. Consequently, at a given time, larvae exposed to low pH were present at a normal but delayed larval stage. More surprisingly, candidate genes involved in development and biomineralization were upregulated by factors of up to 26 at low pH. Our results revealed plasticity at the gene expression level that allows a normal, but delayed, development under low pH conditions.

[1]  C. Ettensohn,et al.  The genomic regulatory control of skeletal morphogenesis in the sea urchin , 2012, Development.

[2]  K. Lotterhos,et al.  Elevated pCO2 increases sperm limitation and risk of polyspermy in the red sea urchin Strongylocentrotus franciscanus , 2011 .

[3]  S. Dupont,et al.  What meta-analysis can tell us about vulnerability of marine biodiversity to ocean acidification? , 2010 .

[4]  S. Dupont,et al.  Near future ocean acidification increases growth rate of the lecithotrophic larvae and juveniles of the sea star Crossaster papposus. , 2010, Journal of experimental zoology. Part B, Molecular and developmental evolution.

[5]  A. Poustka,et al.  Proteomic analysis of sea urchin (Strongylocentrotus purpuratus) spicule matrix , 2010, Proteome Science.

[6]  M. Byrne,et al.  Fertilization in a suite of coastal marine invertebrates from SE Australia is robust to near-future ocean warming and acidification , 2010 .

[7]  M. Byrne,et al.  Sea urchin fertilization in a warm, acidified and high pCO2 ocean across a range of sperm densities. , 2010, Marine environmental research.

[8]  S. Dupont,et al.  Impact of near-future ocean acidification on echinoderms , 2010, Ecotoxicology.

[9]  M. O'Donnell,et al.  Ocean acidification alters skeletogenesis and gene expression in larval sea urchins , 2010 .

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

[11]  C. Harley,et al.  Elevated water temperature and carbon dioxide concentration increase the growth of a keystone echinoderm , 2009, Proceedings of the National Academy of Sciences.

[12]  Maria Byrne,et al.  Temperature, but not pH, compromises sea urchin fertilization and early development under near-future climate change scenarios , 2009, Proceedings of the Royal Society B: Biological Sciences.

[13]  D. Clark,et al.  Response of sea urchin pluteus larvae (Echinodermata: Echinoidea) to reduced seawater pH: a comparison among a tropical, temperate, and a polar species , 2009 .

[14]  L. Peck,et al.  Near-future level of CO2-driven ocean acidification radically affects larval survival and development in the brittlestar Ophiothrix fragilis , 2008 .

[15]  H. Pörtner.  Ecosystem effects of ocean acidification in times of ocean warming: a physiologist’s view , 2008 .

[16]  M. Mann,et al.  In-depth, high-accuracy proteomics of sea urchin tooth organic matrix , 2008 .

[17]  O. Hoegh-Guldberg,et al.  Ocean acidification causes bleaching and productivity loss in coral reef builders , 2008, Proceedings of the National Academy of Sciences.

[18]  A. Farrell,et al.  Physiology and Climate Change , 2008, Science.

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

[20]  M. Mann,et al.  The sea urchin (Strongylocentrotus purpuratus) test and spine proteomes , 2008, Proteome Science.

[21]  Stephen Widdicombe,et al.  Ocean acidification may increase calcification rates, but at a cost , 2008, Proceedings of the Royal Society B: Biological Sciences.

[22]  M. Thorndyke,et al.  Near-future levels of ocean acidificat ion reduce fert ilizat ion success in a sea urchin , 2018 .

[23]  Michael O'Donnell,et al.  Gene expression in the intertidal mussel Mytilus californianus: physiological response to environmental factors on a biogeographic scale , 2008 .

[24]  D. McClay,et al.  FGF signals guide migration of mesenchymal cells, control skeletal morphogenesis and regulate gastrulation during sea urchin development , 2007 .

[25]  H. Kurihara,et al.  Effects of increased seawater pCO2 on early development of the oyster Crassostrea gigas , 2007 .

[26]  C. Heip,et al.  Impact of elevated CO2 on shellfish calcification , 2007 .

[27]  David Epel,et al.  Embryo stability and vulnerability in an always changing world , 2007, Proceedings of the National Academy of Sciences.

[28]  J. Morse,et al.  Calcium carbonate formation and dissolution. , 2007, Chemical reviews.

[29]  Andrew R. Jackson,et al.  The Genome of the Sea Urchin Strongylocentrotus purpuratus , 2006, Science.

[30]  M. Tare.  CO2 and ocean acidification , 2006 .

[31]  E. Maier‐Reimer,et al.  Anthropogenic ocean acidification over the twenty-first century and its impact on calcifying organisms , 2005, Nature.

[32]  Ken Caldeira,et al.  Ocean model predictions of chemistry changes from carbon dioxide emissions to the atmosphere and ocean , 2005 .

[33]  H. Thornton,et al.  Effect of increased atmospheric CO2 on shallow water marine benthos , 2005 .

[34]  Y. Shirayama,et al.  Effects of increased atmospheric CO2 on sea urchin early development , 2004 .

[35]  Mark A. Green,et al.  Dissolution mortality of juvenile bivalves in coastal marine deposits , 2004 .

[36]  J. Kita,et al.  Acute CO2 tolerance during the early developmental stages of four marine teleosts , 2003, Environmental toxicology.

[37]  K. Caldeira,et al.  Oceanography: Anthropogenic carbon and ocean pH , 2003, Nature.

[38]  F. Wilt.  Biomineralization of the Spicules of Sea Urchin Embryos , 2002, Zoological science.

[39]  P. B. Duffy,et al.  Anthropogenic carbon and ocean pH , 2001 .

[40]  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.

[41]  H. Pörtner,et al.  Modulation of the cost of pHi regulation during metabolic depression: a (31)P-NMR study in invertebrate (Sipunculus nudus) isolated muscle. , 2000, The Journal of experimental biology.

[42]  M. Lamare,et al.  In situ estimates of larval development and mortality in the New Zealand sea urchin Evechinus chloroticus (Echinodermata: Echinoidea) , 1999 .

[43]  Denis Allemand,et al.  Photosynthesis and Calcification at Cellular, Organismal and Community Levels in Coral Reefs: A Review on Interactions and Control by Carbonate Chemistry , 1999 .

[44]  Yuichiro Yamada,et al.  Acute toxicity of lowered pH to some oceanic zooplankton , 1999 .

[45]  P. Leong,et al.  Metabolic importance of Na+/K+-ATPase activity during sea urchin development. , 1997, The Journal of experimental biology.

[46]  C. Ettensohn,et al.  Skeletal morphogenesis in the sea urchin embryo: regulation of primary mesenchyme gene expression and skeletal rod growth by ectoderm-derived cues. , 1997, Development.

[47]  M. Pedrotti,et al.  Effects of food diet on the survival, development and growth rates of two cultured echinoplutei (Paracentrotus lividus and Arbacia lixula) , 1993 .

[48]  A. Fujiwara,et al.  Change in the Activity of Na1, K+‐ATPase in Embryos of the Sea Urchin, Hemicentrotus pulcherrimus, during Early Development , 1992 .

[49]  C. Killian,et al.  Characterization and expression of a gene encoding a 30.6-kDa Strongylocentrotus purpuratus spicule matrix protein. , 1991, Developmental biology.

[50]  S. Rumrill,et al.  Natural mortality of marine invertebrate larvae , 1990 .

[51]  R. Raff,et al.  Antibodies to a fusion protein identify a cDNA clone encoding msp130, a primary mesenchyme-specific cell surface protein of the sea urchin embryo. , 1987, Developmental biology.

[52]  J. Cheung,et al.  Effects of metabolic acidosis on viability of cells exposed to anoxia. , 1985, The American journal of physiology.

[53]  W. Lennarz,et al.  A monoclonal antibody inhibits calcium accumulation and skeleton formation in cultured embryonic cells of the sea urchin , 1985, Cell.

[54]  B. Trump,et al.  Extracellular Acidosis Protects Ehrlich Ascites Tumor Cells and Rat Renal Cortex against Anoxic Injury , 1974, Science.

[55]  J. Messer,et al.  Heart Muscle Viability following Hypoxia: Protective Effect of Acidosis , 1973, Science.

[56]  P. L. Jørgensen,et al.  Preparation of highly active (Na+ + K+)-ATPase from the outer medulla of rabbit kidney. , 1969, Biochemical and biophysical research communications.

[57]  S. Goldhor.  Ecology , 1964, The Yale Journal of Biology and Medicine.

[58]  A. Dickson.  The carbon dioxide system in seawater : equilibrium chemistry and measurements 1 , 2011 .

[59]  K. Shimada,et al.  Effects of acidified seawater on early life stages of scleractinian corals (Genus Acropora) , 2009, Fisheries Science.

[60]  J. Hall‐Spencer,et al.  Effects of anthropogenic seawater acidification on acid-base balance in the sea urchin Psammechinus miliaris. , 2007, Marine pollution bulletin.

[61]  Stefano Schiavon,et al.  Climate Change 2007: The Physical Science Basis. , 2007 .

[62]  Andrew G. Dickson,et al.  Guide to best practices for ocean CO2 measurements , 2007 .

[63]  H. L. Miller,et al.  Climate Change 2007: The Physical Science Basis , 2007 .

[64]  J. Berge,et al.  Effects of increased sea water concentrations of CO2 on growth of the bivalve Mytilus edulis L. , 2006, Chemosphere.

[65]  C. Page,et al.  Ocean acidification due to increasing atmospheric carbon dioxide , 2005 .

[66]  B. Miner,et al.  Echinoid larval ecology , 2001 .

[67]  M. Verlaque,et al.  Ecology of Paracentrotus lividus , 2001 .

[68]  S. Bay,et al.  Status and Applications of Echinoid ( Phylum Echinodermata ) Toxicity Test Methods , 1993 .

[69]  L. Fenaux,et al.  Dispersal of echinoderm larvae in a geographical area marked by upwelling (Ligurian Sea, NW Mediterranean) , 1992 .

[70]  J. S. Gordon.  The Sea Urchin , 1870 .

[71]  Thomas D. Schmittgen,et al.  Analysis of Relative Gene Expression Data Using Real-Time Quantitative PCR and the 2 2 DD C T Method , 2022 .