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Identification of Differentially Expressed Genes involved in Thermal Adaptation of the Hong Kong Oyster by Digital Gene Expression Profiling

ABSTRACT: Thermal exposure of sessile marine animals inhabiting estuarine intertidal regions is a matter of serious concern. The Hong Kong oyster, Crassostrea hongkongensis is one of the dominant sessile inhabitants of marine intertidal region which undergoes large seasonal temperature fluctuations every year. The oyster has developed several adaptation mechanisms to cope with acute thermal stress. However, the genetic basis of these mechanisms remain largely unclear. To better understand how acute thermal exposure affects the biology of the oyster, two cDNA libraries obtained from the gill of oysters exposed to thermal stress and ambient temperature were sequenced using the Digital Gene Expression (DGE) tag profiling strategy. In total, 5.9 and 6.2 million reads were obtained for thermal stress and control libraries respectively, with approximately 74.25% and 75.02 % of the reads mapping to the C. hongkongensis reference sequence. A total of 605 differentially expressed transcripts could be detected in the thermal stress group as compared to the control group, of which 378 are up-regulated and 227 are down-regulated. Gene Ontology (GO) and Kyoto Encyclopedia of Genes and Genomes (KEGG) pathway analysis indicated that these Differentially Expressed Genes (DEGs) were enriched with a broad spectrum of biological processes and pathways, including those associated with chaperones, antioxidants, immunity, apoptosis and cytoskeletal reorganization. Among these significantly enriched pathways, protein processing in the endoplasmic reticulum was the most affected metabolic pathway, which plays an important role in the unfolded protein response (UPR) and ER-associated degradation (ERAD) processes. Our results demonstrate the complex multi-modal cellular response to thermal stress in C. hongkongensis.

ORGANISM(S): Crassostrea hongkongensis

PROVIDER: GSE85707 | GEO | 2016/10/11

SECONDARY ACCESSION(S): PRJNA339141

REPOSITORIES: GEO

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Project description:Intermittent hypoxia is a common stressor in estuarine and coastal habitats due to the diurnal and tidal cycles of oxygen availability. Oxygen deficiency results in energy stress by limiting aerobic ATP production, while reoxygenation may lead to oxidative injury due to the excessive production of reactive oxygen species (ROS) in mitochondria. Mitochondria are a key intracellular target of hypoxia-reoxygenation (H/R) stress due to their central role in ATP production, ROS generation and stress signaling. Marine intertidal bivalves such as the Pacific oyster Crassostrea gigas are adapted to frequent H/R cycles in the intertidal zone and maintain mitochondrial integrity and aerobic function despite frequent oxygen fluctuations. To gain insight into the molecular responses of mitochondria of the hypoxia-tolerant Pacific oyster to H/R stress, we studied changes in oxidative phosphorylation (OXPHOS) capacity, proton leak and activity of the electron transport system enzymes (ETS) in gill mitochondria of C. gigas. We furthermore investigated shifts in mitochondrial proteome and phosphoproteome after 24 h of hypoxia and 1 h of post-hypoxic recovery. Oyster mitochondria maintained normal ETS and OXPHOS capacity during H/R stress, despite a slight but significant decline in cytochrome c oxidase (Complex IV) activity after reoxygenation. Fifty total proteins and 36 phosphoproteins were differentially abundant in mitochondria of H/R exposed oysters compared with the controls. Rearrangements of the mitochondrial (phospho)proteome during H/R stress involved upregulation of mitochondrial ETS (most notably Complexes I and IV) and iron-binding proteins (frataxin and ferrochelatase) as well as suppression of the metabolic pathways that channel electrons to ubiquinone, possibly as a mechanism to limit ROS production due to the iron overload and reverse flow of electrons through ETS. H/R stress also led to upregulation of a mitophagic activator serine/threonine protein phosphatase PGAM5 and dephosphorylation of metalloendopeptidase OMA1 indicating stimulation of mitochondrial quality control mechanisms during reoxygenation. Changes in the overall abundance and phosphorylation levels of several key proteins involved in the mitochondrial protein homeostasis (including subunits of the mitochondrial ribosome, mitochondrial inner membrane translocase and elongation factor G) are consistent with the suppression of the protein synthesis during hypoxia, likely as an energy-saving mechanism. Overall, our study indicates that shifts in the mitochondrial (phospho-)proteome play an important role in responses of oysters to H/R stress and might complement adaptations of anaerobic metabolism and metabolic rate depression in ensuring hypoxic survival and rapid recovery in this hypoxia-tolerant intertidal species.

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Identification of Differentially Expressed Genes involved in Thermal Adaptation of the Hong Kong Oyster by Digital Gene Expression Profiling

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