Metabolomics and biochemical assays reveal the metabolic responses to hypo-salinity stress and osmoregulatory role of cAMP-PKA pathway in Mercenaria mercenaria
Hypo-salinity events frequently occur in marine ecosystem due to persistent rainfall and freshwater inflow, reducing the cytosol osmolarity and triggering cellular stress responses in aquatic organisms. Euryhaline bivalves have developed sophisticated regulatory mechanisms to adapt to salinity fluct...
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Elsevier
2022-01-01
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| Series: | Computational and Structural Biotechnology Journal |
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| Online Access: | http://www.sciencedirect.com/science/article/pii/S2001037022003385 |
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| author | Cong Zhou Hao Song Jie Feng Zhi Hu Mei-jie Yang Pu Shi Yong-ren Li Yong-jun Guo Hai-zhou Li Tao Zhang |
| author_facet | Cong Zhou Hao Song Jie Feng Zhi Hu Mei-jie Yang Pu Shi Yong-ren Li Yong-jun Guo Hai-zhou Li Tao Zhang |
| author_sort | Cong Zhou |
| collection | DOAJ |
| description | Hypo-salinity events frequently occur in marine ecosystem due to persistent rainfall and freshwater inflow, reducing the cytosol osmolarity and triggering cellular stress responses in aquatic organisms. Euryhaline bivalves have developed sophisticated regulatory mechanisms to adapt to salinity fluctuations over a long period of evolution. In this study, we performed multiple biochemical assays, widely targeted metabolomics, and gene expression analysis to investigate the comprehensive metabolic responses to hypo-salinity stress and osmoregulation mechanisms in hard clam Mercenaria mercenaria, which is a euryhaline bivalve species widely cultured in China. During hypo-salinity stress, increased vacuoles appeared in gill filaments. The Na+ and Cl- concentrations in gills significantly decreased because of the up-regulation of Na+/K+-ATPase (NKA) activity. The cAMP content dramatically decreased at 5 d post hypo-salinity stress. Meanwhile, the gene expression levels of adenylate cyclase, proteinkinase A, and sodium and calcium channel proteins were evidently down-regulated, suggesting that cAMP-PKA pathway was inhibited to prevent ambient inorganic ions from entering the gill cells. Antioxidant metabolites, such as serine and Tyr-containing dipeptides, were significantly up-regulated to resist oxidative stress. Glycerolipid metabolism was strengthened to stabilize membrane structure when hypo-salinity stress was prolonged to 5 days. At 1 d post hypo-salinity stress, an increase in alanine and lactate contents marked the initiation of anaerobic metabolism. Acylcarnitines accumulation indicated that fatty acids β-oxidation was promoted to provide energy for osmoregulation. The potential biomarkers of hypo-salinity stress were identified in hard clams. This study provides novel insights into the metabolic regulatory mechanisms to hypo-salinity stress in euryhaline bivalves. |
| first_indexed | 2024-04-11T05:19:18Z |
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| language | English |
| last_indexed | 2024-04-11T05:19:18Z |
| publishDate | 2022-01-01 |
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| series | Computational and Structural Biotechnology Journal |
| spelling | doaj.art-34917abc01584d65b13948aaf549c86f2022-12-24T04:53:46ZengElsevierComputational and Structural Biotechnology Journal2001-03702022-01-012041104121Metabolomics and biochemical assays reveal the metabolic responses to hypo-salinity stress and osmoregulatory role of cAMP-PKA pathway in Mercenaria mercenariaCong Zhou0Hao Song1Jie Feng2Zhi Hu3Mei-jie Yang4Pu Shi5Yong-ren Li6Yong-jun Guo7Hai-zhou Li8Tao Zhang9CAS Key Laboratory of Marine Ecology and Environmental Sciences, Institute of Oceanology, Chinese Academy of Sciences, Qingdao 266071, China; Laboratory for Marine Ecology and Environmental Science, Qingdao National Laboratory for Marine Science and Technology, Qingdao 266237, China; Center for Ocean Mega-Science, Chinese Academy of Sciences, Qingdao 266071, China; CAS Engineering Laboratory for Marine Ranching, Institute of Oceanology, Chinese Academy of Sciences, Qingdao 266071, China; University of Chinese Academy of Sciences, Beijing 100049, China; Shandong Province Key Laboratory of Experimental Marine Biology, Qingdao 266071, ChinaCAS Key Laboratory of Marine Ecology and Environmental Sciences, Institute of Oceanology, Chinese Academy of Sciences, Qingdao 266071, China; Laboratory for Marine Ecology and Environmental Science, Qingdao National Laboratory for Marine Science and Technology, Qingdao 266237, China; Center for Ocean Mega-Science, Chinese Academy of Sciences, Qingdao 266071, China; CAS Engineering Laboratory for Marine Ranching, Institute of Oceanology, Chinese Academy of Sciences, Qingdao 266071, China; Shandong Province Key Laboratory of Experimental Marine Biology, Qingdao 266071, ChinaCAS Key Laboratory of Marine Ecology and Environmental Sciences, Institute of Oceanology, Chinese Academy of Sciences, Qingdao 266071, China; Laboratory for Marine Ecology and Environmental Science, Qingdao National Laboratory for Marine Science and Technology, Qingdao 266237, China; Center for Ocean Mega-Science, Chinese Academy of Sciences, Qingdao 266071, China; CAS Engineering Laboratory for Marine Ranching, Institute of Oceanology, Chinese Academy of Sciences, Qingdao 266071, China; Shandong Province Key Laboratory of Experimental Marine Biology, Qingdao 266071, ChinaCAS Key Laboratory of Marine Ecology and Environmental Sciences, Institute of Oceanology, Chinese Academy of Sciences, Qingdao 266071, China; Laboratory for Marine Ecology and Environmental Science, Qingdao National Laboratory for Marine Science and Technology, Qingdao 266237, China; Center for Ocean Mega-Science, Chinese Academy of Sciences, Qingdao 266071, China; CAS Engineering Laboratory for Marine Ranching, Institute of Oceanology, Chinese Academy of Sciences, Qingdao 266071, China; University of Chinese Academy of Sciences, Beijing 100049, China; Shandong Province Key Laboratory of Experimental Marine Biology, Qingdao 266071, ChinaCAS Key Laboratory of Marine Ecology and Environmental Sciences, Institute of Oceanology, Chinese Academy of Sciences, Qingdao 266071, China; Laboratory for Marine Ecology and Environmental Science, Qingdao National Laboratory for Marine Science and Technology, Qingdao 266237, China; Center for Ocean Mega-Science, Chinese Academy of Sciences, Qingdao 266071, China; CAS Engineering Laboratory for Marine Ranching, Institute of Oceanology, Chinese Academy of Sciences, Qingdao 266071, China; University of Chinese Academy of Sciences, Beijing 100049, China; Shandong Province Key Laboratory of Experimental Marine Biology, Qingdao 266071, ChinaCAS Key Laboratory of Marine Ecology and Environmental Sciences, Institute of Oceanology, Chinese Academy of Sciences, Qingdao 266071, China; Laboratory for Marine Ecology and Environmental Science, Qingdao National Laboratory for Marine Science and Technology, Qingdao 266237, China; Center for Ocean Mega-Science, Chinese Academy of Sciences, Qingdao 266071, China; CAS Engineering Laboratory for Marine Ranching, Institute of Oceanology, Chinese Academy of Sciences, Qingdao 266071, China; University of Chinese Academy of Sciences, Beijing 100049, China; Shandong Province Key Laboratory of Experimental Marine Biology, Qingdao 266071, ChinaTianjin Key Laboratory of Aqua-ecology and Aquaculture, Fisheries College, Tianjin Agricultural University, Tianjin 300384, ChinaTianjin Key Laboratory of Aqua-ecology and Aquaculture, Fisheries College, Tianjin Agricultural University, Tianjin 300384, ChinaShandong Fu Han Ocean Sci-Tech Co., Ltd, Haiyang 265100, ChinaCAS Key Laboratory of Marine Ecology and Environmental Sciences, Institute of Oceanology, Chinese Academy of Sciences, Qingdao 266071, China; Laboratory for Marine Ecology and Environmental Science, Qingdao National Laboratory for Marine Science and Technology, Qingdao 266237, China; Center for Ocean Mega-Science, Chinese Academy of Sciences, Qingdao 266071, China; CAS Engineering Laboratory for Marine Ranching, Institute of Oceanology, Chinese Academy of Sciences, Qingdao 266071, China; Shandong Province Key Laboratory of Experimental Marine Biology, Qingdao 266071, China; Corresponding author at: 7 Nanhai Road, Shinan District, Qingdao City, Shandong Province, China.Hypo-salinity events frequently occur in marine ecosystem due to persistent rainfall and freshwater inflow, reducing the cytosol osmolarity and triggering cellular stress responses in aquatic organisms. Euryhaline bivalves have developed sophisticated regulatory mechanisms to adapt to salinity fluctuations over a long period of evolution. In this study, we performed multiple biochemical assays, widely targeted metabolomics, and gene expression analysis to investigate the comprehensive metabolic responses to hypo-salinity stress and osmoregulation mechanisms in hard clam Mercenaria mercenaria, which is a euryhaline bivalve species widely cultured in China. During hypo-salinity stress, increased vacuoles appeared in gill filaments. The Na+ and Cl- concentrations in gills significantly decreased because of the up-regulation of Na+/K+-ATPase (NKA) activity. The cAMP content dramatically decreased at 5 d post hypo-salinity stress. Meanwhile, the gene expression levels of adenylate cyclase, proteinkinase A, and sodium and calcium channel proteins were evidently down-regulated, suggesting that cAMP-PKA pathway was inhibited to prevent ambient inorganic ions from entering the gill cells. Antioxidant metabolites, such as serine and Tyr-containing dipeptides, were significantly up-regulated to resist oxidative stress. Glycerolipid metabolism was strengthened to stabilize membrane structure when hypo-salinity stress was prolonged to 5 days. At 1 d post hypo-salinity stress, an increase in alanine and lactate contents marked the initiation of anaerobic metabolism. Acylcarnitines accumulation indicated that fatty acids β-oxidation was promoted to provide energy for osmoregulation. The potential biomarkers of hypo-salinity stress were identified in hard clams. This study provides novel insights into the metabolic regulatory mechanisms to hypo-salinity stress in euryhaline bivalves.http://www.sciencedirect.com/science/article/pii/S2001037022003385MetabolomicsOsmoregulationOxidative stressEnergy metabolismHypo-salinity tolerance |
| spellingShingle | Cong Zhou Hao Song Jie Feng Zhi Hu Mei-jie Yang Pu Shi Yong-ren Li Yong-jun Guo Hai-zhou Li Tao Zhang Metabolomics and biochemical assays reveal the metabolic responses to hypo-salinity stress and osmoregulatory role of cAMP-PKA pathway in Mercenaria mercenaria Computational and Structural Biotechnology Journal Metabolomics Osmoregulation Oxidative stress Energy metabolism Hypo-salinity tolerance |
| title | Metabolomics and biochemical assays reveal the metabolic responses to hypo-salinity stress and osmoregulatory role of cAMP-PKA pathway in Mercenaria mercenaria |
| title_full | Metabolomics and biochemical assays reveal the metabolic responses to hypo-salinity stress and osmoregulatory role of cAMP-PKA pathway in Mercenaria mercenaria |
| title_fullStr | Metabolomics and biochemical assays reveal the metabolic responses to hypo-salinity stress and osmoregulatory role of cAMP-PKA pathway in Mercenaria mercenaria |
| title_full_unstemmed | Metabolomics and biochemical assays reveal the metabolic responses to hypo-salinity stress and osmoregulatory role of cAMP-PKA pathway in Mercenaria mercenaria |
| title_short | Metabolomics and biochemical assays reveal the metabolic responses to hypo-salinity stress and osmoregulatory role of cAMP-PKA pathway in Mercenaria mercenaria |
| title_sort | metabolomics and biochemical assays reveal the metabolic responses to hypo salinity stress and osmoregulatory role of camp pka pathway in mercenaria mercenaria |
| topic | Metabolomics Osmoregulation Oxidative stress Energy metabolism Hypo-salinity tolerance |
| url | http://www.sciencedirect.com/science/article/pii/S2001037022003385 |
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