Abstract
Marine bivalves secrete calcified shells to protect their soft bodies from predation and damages, which is of great importance for their survival, and for the safety of the coastal ecosystem. In recent years, larval shell formation of marine bivalves has been severely affected by ocean acidification (OA), and previous study indicated that OA might affect such process by disrupting endogenous energy metabolism. Developmental stages from trochophore to D-shape larvae are extremely important for initial shell formation in oyster since a calcified shell was formed to cover the chitin one. In the present study, metabolomic and transcriptomic approaches were employed to investigate the energy metabolism of oyster larvae during initial shell (prodissoconch I, PDI shell) formation and under experimental OA treatment. Totally 230 chemical compounds were identified from the present dataset, most of which were highly expressed in the “middle” stage (early D-shape larvae) which was critical for PDI shell formation since a calcified shell was formed to cover the chitin one. Several compounds such as glucose, glutarylcarnitine (C5), β-hydroxyisovaleroylcarnitine, 5-methylthioadenosine (MTA), myristoleate (14:1n5) and palmitoleate (16:1n7) were identified, which were involved in energy metabolic processes including amino acid oxidation, glycolysis, pentose phosphate pathway and fatty acid metabolism. In addition, mRNA expressions of genes related to protein metabolism, glycolysis, lipid degradation, calcium transport and organic matrix formation activities were significantly down-regulated upon experimental OA. These results collectively suggested that formation of the initial shell in oyster larvae required endogenous energy coming from amino acid oxidation, glycolysis, pentose phosphate pathway and fatty acid metabolism. These metabolic activities could be severely inhibited by experimental OA, which might alter the allocation of endogenous energy. Insufficient endogenous energy supply then suppressed the mobilization of calcium and resulted in a failure or delay in PDI shell formation.
Highlights
Marine bivalves secrete calcified shells to protect their soft bodies from predation and damages, which is of great importance for their survival, and for the safety of the coastal ecosystem
To test this hypothesis we explored the impact of experimental acidification treatments on larvae of the Pacific oyster Crassostrea gigas with metabolic and transcriptomic approaches, hoping to (1) identify metabolites related to lipid/carbohydrate/protein metabolism during PDI shell formation; (2) illustrate the influences of experimental ocean acidification (OA) on energy metabolism; and (3) reveal the negative effects of OA on PDI shell formation
By analyzing the transcriptomic data of oyster larvae under experimental OA, expressions of genes related to key processes in larvae shell formation were significantly inhibited, which included calcium transportation (CGI_10000261, CGI_10011110 and CGI_10008043), bicarbonate transport (CGI_10004992, CGI_10027742 and CGI_10020143), organic matrix (CGI_10011133, CGI_10003192 and CGI_10002674), glycolysis (CGI_10007559, CGI_10003670 and CGI_10025556), fatty acid metabolic process (CGI_10008805, CGI_10021437 and CGI_10001878), protein phosphorylation (CGI_10002840, CGI_10015358 and CGI_10015881), and ATP synthesis (CGI_10004070, CGI_10006577 and CGI_10005007) (Fig. 6, Table 1). Marine bivalves such as oysters and scallops secrete calcified shells as a supporting frame for their soft bodies and for protection from predators[1,2], which is thought to be one of the key factors that trigger the expansion of bivalves at the dawn of the Cambrian times[16]
Summary
Marine bivalves secrete calcified shells to protect their soft bodies from predation and damages, which is of great importance for their survival, and for the safety of the coastal ecosystem. MRNA expressions of genes related to protein metabolism, glycolysis, lipid degradation, calcium transport and organic matrix formation activities were significantly down-regulated upon experimental OA These results collectively suggested that formation of the initial shell in oyster larvae required endogenous energy coming from amino acid oxidation, glycolysis, pentose phosphate pathway and fatty acid metabolism. The energy cost of calcification was empirically derived to be no more than 1.1 μJ (ng CaCO3)−1 in oyster larvae, and larval families showed variation in response to ocean acidification, with loss of shell size ranging from no effect to 28%, which indicated that resilience to OA might exist among genotypes[14,15] These works evidenced that OA is likely to affect larval shell formation in marine bivalves by disrupting the balance of energy metabolism. To test this hypothesis we explored the impact of experimental acidification treatments on larvae of the Pacific oyster Crassostrea gigas with metabolic and transcriptomic approaches, hoping to (1) identify metabolites related to lipid/carbohydrate/protein metabolism during PDI shell formation; (2) illustrate the influences of experimental OA on energy metabolism; and (3) reveal the negative effects of OA on PDI shell formation
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