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Impacts of seawater acidification on mantle gene expression patterns of the Baltic Sea blue mussel: implications for shell formation and energy metabolism

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Abstract

Marine organisms have to cope with increasing CO2 partial pressures and decreasing pH in the oceans. We elucidated the impacts of an 8-week acclimation period to four seawater pCO2 treatments (39, 113, 243 and 405 Pa/385, 1,120, 2,400 and 4,000 μatm) on mantle gene expression patterns in the blue mussel Mytilus edulis from the Baltic Sea. Based on the M. edulis mantle tissue transcriptome, the expression of several genes involved in metabolism, calcification and stress responses was assessed in the outer (marginal and pallial zone) and the inner mantle tissues (central zone) using quantitative real-time PCR. The expression of genes involved in energy and protein metabolism (F-ATPase, hexokinase and elongation factor alpha) was strongly affected by acclimation to moderately elevated CO2 partial pressures. Expression of a chitinase, potentially important for the calcification process, was strongly depressed (maximum ninefold), correlating with a linear decrease in shell growth observed in the experimental animals. Interestingly, shell matrix protein candidate genes were less affected by CO2 in both tissues. A compensatory process toward enhanced shell protection is indicated by a massive increase in the expression of tyrosinase, a gene involved in periostracum formation (maximum 220-fold). Using correlation matrices and a force-directed layout network graph, we were able to uncover possible underlying regulatory networks and the connections between different pathways, thereby providing a molecular basis of observed changes in animal physiology in response to ocean acidification.

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Acknowledgments

We would like to thank Ulrike Panknin and Katja Trübenbach for tissue sampling, as well as UP for her help with RNA isolation and cDNA synthesis. This study is part of the German joint project “Biological Impact of Ocean Acidification (BIOACID)” (3.1.3) and funded by the Federal Ministry of Education and Research (BMBF, FKZ 03F0608B). It is a contribution to the PACES research program (work package 1.6) of the Alfred Wegener Institute funded by the Helmholtz Association. The Excellence Cluster ‘Future Ocean’ awarded grants to F.M., E.P., M.A.G. and P.R.

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227_2012_1930_MOESM1_ESM.pdf

Fig. 1 supplement Correlation network of genes in a) inner mantle tissue and b) outer mantle tissue based on the R-script after removing pCO2 dependent correlations. Line width of vertices corresponds to correlation. Genes were set as correlated when Spearman’s |ρ| ≥ 0.5. (PDF 299 kb)

227_2012_1930_MOESM2_ESM.pdf

Fig. 2 supplement Comparison of Copper-binding site CuA from several tyrosinases and one hemocyanin. Essential histidines, responsible for copper-binding are denoted with arrows. MeTYRs: Mytilus edulis putative tyrosinases from our transcriptome, LgTYR1: Lottia gigantea tyrosinase (ID: 166196 on JGI), PmTYR: Pinctada maxima tyrosinase (GH280185), PfOT47: P. fucata tyrosinase (DQ112679), PfTYR2: P. fucata tyrosinase (AB254133), PfTYR1: P. fucata tyrosinase (AB254132), CfTYR: Clamys farreri tyrosinase (ACF25906.1), LgTYR2: L. gigantea tyrosinase (ID: 160808 on JGI), IaTYR1: Illex argentinus tyrosinase (AB107880.1), IaTYR2: I. argentinus tyrosinase (AB107881.1), SoTYR: Sepia officinalis tyrosinase (AJ297474.1), HtHem: Haliotis tuberculata hemocyanin (CAC82192.1), GgTYR: Gallus gallus tyrosinase (AAB36375.1), MmTYR: Mus musculus tyrosinase (P11344.3), HsTYR: Homo sapiens (P14679.3). (PDF 1116 kb)

227_2012_1930_MOESM3_ESM.pdf

Fig. 3 supplement Phylogenetic tree of protein sequences including CuA sites of several tyrosinases and one hemocyanin. The length of the used sequences varied between 77 and 111 amino acids. The tree was constructed with the neighbor-joining method (Saitou and Nei 1987). Distances between the roots were un-corrected. For abbreviations see Fig. 2 supplement. (PDF 418 kb)

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Hüning, A.K., Melzner, F., Thomsen, J. et al. Impacts of seawater acidification on mantle gene expression patterns of the Baltic Sea blue mussel: implications for shell formation and energy metabolism. Mar Biol 160, 1845–1861 (2013). https://doi.org/10.1007/s00227-012-1930-9

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