Integrated application of transcriptomics and metabolomics provides insights into glycogen content regulation in the Pacific oyster Crassostrea gigas

Busu Li,Jie Meng,Kai Song,Guofan Zhang,Li Li

doi:10.1186/s12864-017-4069-8

Abstract

BackgroundThe Pacific oyster Crassostrea gigas is an important marine fishery resource, which contains high levels of glycogen that contributes to the flavor and the quality of the oyster. However, little is known about the molecular and chemical mechanisms underlying glycogen content differences in Pacific oysters. Using a homogeneous cultured Pacific oyster family, we explored these regulatory networks at the level of the metabolome and the transcriptome.ResultsOysters with the highest and lowest natural glycogen content were selected for differential transcriptome and metabolome analysis. We identified 1888 differentially-expressed genes, seventy-five differentially-abundant metabolites, which are part of twenty-seven signaling pathways that were enriched using an integrated analysis of the interaction between the differentially-expressed genes and the differentially-abundant metabolites. Based on these results, we found that a high expression of carnitine O-palmitoyltransferase 2 (CPT2), indicative of increased fatty acid degradation, is associated with a lower glycogen content. Together, a high level of expression of phosphoenolpyruvate carboxykinase (PEPCK), and high levels of glucogenic amino acids likely underlie the increased glycogen production in high-glycogen oysters. In addition, the higher levels of the glycolytic enzymes hexokinase (HK) and pyruvate kinase (PK), as well as of the TCA cycle enzymes malate dehydrogenase (MDH) and pyruvate carboxylase (PYC), imply that there is a concomitant up-regulation of energy metabolism in high-glycogen oysters. High-glycogen oysters also appeared to have an increased ability to cope with stress, since the levels of the antioxidant glutathione peroxidase enzyme 5 (GPX5) gene were also increased.ConclusionOur results suggest that amino acids and free fatty acids are closely related to glycogen content in oysters. In addition, oysters with a high glycogen content have a greater energy production capacity and a greater ability to cope with stress. These findings will not only provide insights into the molecular mechanisms underlying oyster quality, but also promote research into the molecular breeding of oysters.

Highlights

The Pacific oyster Crassostrea gigas is an important marine fishery resource, which contains high levels of glycogen that contributes to the flavor and the quality of the oyster
Glycogen metabolism is highly conserved across species, with glycogen phosphorylase and glycogen synthase being the key enzymes in glycogen degradation and glycogen synthesis, respectively
To compare the metabolite composition of the two oyster groups having either high- or low-glycogen content, both hierarchical cluster analysis (HCA) and principal component analysis (PCA) models were tested using the data obtained from GC-TOF-MS analysis

Summary

Introduction

The Pacific oyster Crassostrea gigas is an important marine fishery resource, which contains high levels of glycogen that contributes to the flavor and the quality of the oyster. Hata’s group has reported the extraction and purification of glycogen phosphorylase from the adductor muscles of oysters [8], whereas Bacca’s group reported the cloning of the oyster glycogen synthase gene, and that the expression level of glycogen synthase changed in a pattern consistent with seasonal variation in glycogen content [9] In other mollusks, such as Crassostrea angulata, glycogen synthase and its regulator glycogen synthase kinase 3 have been characterized, and it was found that their expression depends on the reproductive cycle [10]. Several recent studies have described the molecular regulation of enzymes involved in glycogen metabolism in C. gigas [11, 12] In this regard, a quantitative trait loci (QTL) analysis identified two SNPs in the glycogen debranching enzyme and one SNP in glycogen phosphorylase that are associated with glycogen content [11]. In oysters, little is known about the genetic mechanisms that determine glycogen content and a significant amount of work remains to be done

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