Effects of hypoxia in the gills of the Manila clam Ruditapes philippinarum using NMR-based metabolomics

Zhang, Ying; Wu, Huifeng; Wei, Lei; Xie, Zeping; Guan, Bo

doi:10.1016/j.marpolbul.2016.08.066

Cited by 31 publications

(21 citation statements)

References 51 publications

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“…Here, the choline and betaine contents decreased in the hepatopancreas after hypoxic stress, suggesting that hypoxia may affect molecular pathways of the methionine cycle (Bertolo and McBreairty, 2013 ). Similar to the results of the present study, a higher flux toward the methionine cycle after environmental stress was demonstrated for gilthead sea bream Sparus aurata (Richard et al, 2016 ), the Manila clam Ruditapes philippinarum (Zhang et al, 2017 ), and rainbow smelt Osmerus mordax (Richards and Short, 2010 ). Choline and betaine are among several methyl-donors in the methionine cycle.…”

Section: Discussionsupporting

confidence: 89%

Based on the Metabolomic Approach the Energy Metabolism Responses of Oriental River Prawn Macrobrachium nipponense Hepatopancreas to Acute Hypoxia and Reoxygenation

Sun

Guo

et al. 2018

Front. Physiol.

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Hypoxia represents a major physiological challenge for prawns and is a problem in aquaculture. Therefore, an understanding of the metabolic response mechanism of economically important prawn species to hypoxia and re-oxygenation is essential. However, little is known about the intrinsic mechanisms by which the oriental river prawn Macrobrachium nipponense copes with hypoxia at the metabolic level. In this study, we conducted gas chromatography-mass spectrometry-based metabolomics studies and assays of energy metabolism-related parameters to investigate the metabolic mechanisms in the hepatopancreas of M. nipponense in response to 2.0 O2/L hypoxia for 6 and 24 h, and reoxygenation for 6 h following hypoxia for 24 h. Prawns under hypoxic stress displayed higher glycolysis-related enzyme activities and lower mRNA expression levels of aerobic respiratory enzymes than those in the normoxic control group, and those parameters returned to control levels in the reoxygenated group. Our results showed that hypoxia induced significant metabolomic alterations in the prawn hepatopancreas within 24 h. The main metabolic alterations were depletion of amino acids and 2-hydroxybutanoic acid and accumulation of lactate. Further, the findings indicated that hypoxia disturbed energy metabolism and induced antioxidant defense regulation in prawns. Surprisingly, recovery from hypoxia (i.e., reoxygenation) significantly affected 25 metabolites. Some amino acids (valine, leucine, isoleucine, lysine, glutamate, and methionine) were markedly decreased compared to the control group, suggesting that increased degradation of amino acids occurred to provide energy in prawns at reoxygenation conditions. This study describes the acute metabolomic alterations that occur in prawns in response to hypoxia and demonstrates the potential of the altered metabolites as biomarkers of hypoxia.

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Section: Discussionsupporting

confidence: 89%

Based on the Metabolomic Approach the Energy Metabolism Responses of Oriental River Prawn Macrobrachium nipponense Hepatopancreas to Acute Hypoxia and Reoxygenation

Sun

Guo

et al. 2018

Front. Physiol.

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“…The global water surface temperature has increased by approximately 0.7 C during the last century (Hansen et al, 2006) and a continued increase has been predicted . In response to environmental changes, organisms typically adjust their metabolic physiology to adapt to new energy requirements (Cheung & Lam, 1995;Lagerspetz, 2006;Zhang et al, 2017). It has been reported that temperature can affect the metabolic rates of marine invertebrates, thus influencing the energy available for growth (González et al, 2002).…”

Section: Introductionmentioning

confidence: 99%

Metabolic response of Scapharca subcrenata to heat stress using GC/MS-based metabolomics

Jiang

Jiao

Sun

et al. 2020

PeerJ

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Marine mollusks are commonly subjected to heat stress. To evaluate the effects of heat stress on the physiological metabolism of the ark shell Scapharca subcrenata, clams were exposed to different high temperatures (24, 28 and 32 °C) for 72 h. The oxygen consumption and ammonia excretion rates were measured at 2, 12, 24, 48 and 72 h. The results indicated that the metabolic rates of the ark shell significantly increased with increasing heat stress, accompanied by mortalities in response to prolonged exposure. A metabolomics approach based on gas chromatography coupled with mass spectrometry was further applied to assess the changes of metabolites in the mantle of the ark shell at 32 °C. Moreover, multivariate and pathway analyses were conducted for the different metabolites. The results showed that the heat stress caused changes in energy metabolism, amino acid metabolism, osmotic regulation, carbohydrate metabolism and lipid metabolism through different metabolic pathways. These results are consistent with the significant changes of oxygen consumption rate and ammonia excretion rate. The present study contributes to the understanding of the impacts of heat stress on intertidal bivalves and elucidates the relationship between individual-level responses and underlying molecular metabolic dynamics.

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“…8a&b, the level of dissolved oxygen in the water is insufficient with the hypoxia exposure time increased, and the clams may depend on anaerobic respiration to supply the metabolic energy, which is strongly reducing their energy requirement, so the activity of SDH and LDH decreases with prolonged hypoxia challenge. The different changes in the activities of key enzymes involved in glycolysis may indicate a diverse strategy of shellfish under hypoxia [29].…”

Section: Discussionmentioning

confidence: 99%

“…However, mussels are able to sustain their life at anoxic conditions for weeks by reducing energy requirement [40]. The Manila clam exhibited strong tolerance to hypoxia as the 20-day LC 50 for dissolved oxygen (DO) was estimated to be 0.57 mg L − 1 , and the LT 50 at 0.5 mg L − 1 DO was 422 h [29]. In this study, AKP activity in hepatopancreas was significantly increased at 5 d in response to hypoxia stress, indicating that the hepatopancreas is an important organ that involved in the immune response and hypoxia regulation in R. philippinarum.…”

Section: Discussionmentioning

confidence: 99%

“…Hence, the tolerance of the bivalves for hypoxia and/or anoxic conditions has been investigated by a number of researchers [1,26,27]. More recently, the effects of hypoxia on survival, behavior, metabolism and cellular and tissue damage of R. philippinarum were conducted, suggesting that severe hypoxia significantly affects the physiology of R. philippinarum [28,29]. Until now, however, little effort has been put towards elucidating the molecular mechanisms combined with physiological and biochemical response of clams to the hypoxia resistance and acclimations.…”

Section: Introductionmentioning

confidence: 99%

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Transcriptome analysis reveals differential immune related genes expression in Ruditapes philippinarum under hypoxia stress: potential HIF and NF-κB crosstalk in immune responses in clam

et al. 2020

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Background: Hypoxia is an important environmental stressor in aquatic ecosystems, with increasingly impacts on global biodiversity. Benthic communities are the most sensitive parts of the coastal ecosystem to eutrophication and resulting hypoxia. As a filter-feeding organism living in the seafloor sediment, Ruditapes philippinarum represents an excellent "sentinel" species to assess the quality of marine environment. In order to gain insight into the molecular response and acclimatization mechanisms to hypoxia stress in marine invertebrates, we examined hypoxia-induced changes in immune-related gene expression and gene pathways involved in hypoxia regulation of R. philippinarum. Results: We investigated the response of the Manila clam R. philippinarum to hypoxia under experimental conditions and focused on the analysis of the differential expression patterns of specific genes associated with hypoxia response by RNA-seq and time course qPCR analysis. A total of 75 genes were captured significantly differentially expressed, and were categorized into antioxidant/oxidative stress response, chaperones/heat shock proteins, immune alteration, and cell proliferation/apoptosis. Fourteen hypoxia responsive genes were validated significantly up/down regulated at different time 0, 2, 5, and 8 d in gills of R. philippinarum in hypoxia challenged group. Functional enrichment analysis revealed the HIF signaling pathway and NF-κB signaling pathway play pivotal roles in hypoxia tolerance and resistance in R. philippinarum. Conclusion: The HIF signaling pathway and NF-κB signaling pathway play a critical role in hypoxia tolerance and resistance in Manila clam. The immune and defense related genes and pathways obtained here gain a fundamental understanding of the hypoxia stress in marine bivalves and provide important insights into the physiological acclimation, immune response and defense activity under hypoxia challenge. The reduced metabolism is a consequence of counterbalancing investments in immune defense against other physiological processes.

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Effects of hypoxia in the gills of the Manila clam Ruditapes philippinarum using NMR-based metabolomics

Cited by 31 publications

References 51 publications

Based on the Metabolomic Approach the Energy Metabolism Responses of Oriental River Prawn Macrobrachium nipponense Hepatopancreas to Acute Hypoxia and Reoxygenation

Based on the Metabolomic Approach the Energy Metabolism Responses of Oriental River Prawn Macrobrachium nipponense Hepatopancreas to Acute Hypoxia and Reoxygenation

Metabolic response of Scapharca subcrenata to heat stress using GC/MS-based metabolomics

Transcriptome analysis reveals differential immune related genes expression in Ruditapes philippinarum under hypoxia stress: potential HIF and NF-κB crosstalk in immune responses in clam

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