Effect of prolonged starvation on nutrition utilization and transcriptional responses in Pacific oyster (Crassostrea gigas)
Emaciation syndrome due to starvation is a significant cause of mortality in marine animals, yet the underlying mechanisms in non-feeding and weak/no-mobility marine bivalves remain poorly understood. This study investigated nutrient utilization and transcriptional responses in oysters subjected to...
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Elsevier
2025-03-01
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| Series: | Aquaculture Reports |
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| Online Access: | http://www.sciencedirect.com/science/article/pii/S2352513425000353 |
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| author | Mingkun Liu Chenchen Wei Wenwen Xu Lintao Tan Li Li Guofan Zhang |
| author_facet | Mingkun Liu Chenchen Wei Wenwen Xu Lintao Tan Li Li Guofan Zhang |
| author_sort | Mingkun Liu |
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| description | Emaciation syndrome due to starvation is a significant cause of mortality in marine animals, yet the underlying mechanisms in non-feeding and weak/no-mobility marine bivalves remain poorly understood. This study investigated nutrient utilization and transcriptional responses in oysters subjected to a 44-day starvation period. Nutrient analysis revealed a distinct three-phase pattern in nutrient utilization. During the early stage (days 0–10), glycogen was rapidly consumed, with no mobilization of lipids, proteins, or fatty acids. In the late stage (days 23–44), glycogen was depleted, and there was significant consumption of lipids, proteins, fatty acids, and free amino acids. A newly identified ''transition metabolism'' phase, occurring between the two typical phases (days 10–23), was characterized by a slight compensatory increase in glycogen and lipids, alongside continued protein consumption and depletion of five fatty acids. This phase may represent ''the point of no return'' in starvation tolerance. Transcriptomic analysis revealed that the amino acid and lipid metabolism increased over starvation, while carbohydrate metabolism initially rose and then declined, with a notable tipping point on day 10. This pattern strongly supported the stepped change pattern identified by nutrient utilization. In contrast, immunological functions initially decreased before increasing, whereas functions related to cell growth and survival showed a consistent downward trend. Combined with the correlation between gene expression and symbiotic microbiota, these findings indicated that oysters, due to limited energy, activated insufficient immune responses, leading to increased pathogen abundance and higher mortality during prolonged starvation. This study refined the starvation stress tolerance limits (SSTL) model to better characterize oyster performance under prolonged starvation, offering valuable insights into emaciation syndrome and potential indicators for assessing health status and mortality risk in marine bivalves. |
| format | Article |
| id | doaj-art-b493e0a11fd740ab9a6263a97e7aa9bc |
| institution | Kabale University |
| issn | 2352-5134 |
| language | English |
| publishDate | 2025-03-01 |
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| spelling | doaj-art-b493e0a11fd740ab9a6263a97e7aa9bc2025-02-06T05:12:26ZengElsevierAquaculture Reports2352-51342025-03-0140102649Effect of prolonged starvation on nutrition utilization and transcriptional responses in Pacific oyster (Crassostrea gigas)Mingkun Liu0Chenchen Wei1Wenwen Xu2Lintao Tan3Li Li4Guofan Zhang5School of Marine Sciences, Ningbo University, Ningbo 315832, China; Shandong Province Key Laboratory of Experimental Marine Biology, Institute of Oceanology, Chinese Academy of Sciences, Qingdao 266071, China; Laboratory for Marine Biology and Biotechnology, Qingdao Marine Science and Technology Center, Qingdao 266237, China; Shandong Center of Technology Innovation for Oyster Seed Industry, Qingdao 266071, China; Southern Marine Science and Engineering Guangdong Laboratory (Zhanjiang), Zhanjiang 524006, China; National and Local Joint Engineering Laboratory of Ecological Mariculture, Qingdao 266071, ChinaShandong Province Key Laboratory of Experimental Marine Biology, Institute of Oceanology, Chinese Academy of Sciences, Qingdao 266071, China; National and Local Joint Engineering Laboratory of Ecological Mariculture, Qingdao 266071, ChinaRushan Marine Economy and Development Center, Rushan 264599, ChinaRushan Marine Economy and Development Center, Rushan 264599, China; Correspondence to: Rushan Marine Economy and Development Center, Rushan, China.Shandong Province Key Laboratory of Experimental Marine Biology, Institute of Oceanology, Chinese Academy of Sciences, Qingdao 266071, China; Laboratory for Marine Fisheries Science and Food Production Processes, Qingdao Marine Science and Technology Center, Qingdao 266237, China; University of Chinese Academy of Sciences, Beijing 100049, China; Shandong Center of Technology Innovation for Oyster Seed Industry, Qingdao 266071, China; Southern Marine Science and Engineering Guangdong Laboratory (Zhanjiang), Zhanjiang 524006, China; National and Local Joint Engineering Laboratory of Ecological Mariculture, Qingdao 266071, China; Correspondence to: Institute of Oceanology, Chinese Academy of Sciences, Qingdao, China.Shandong Province Key Laboratory of Experimental Marine Biology, Institute of Oceanology, Chinese Academy of Sciences, Qingdao 266071, China; Laboratory for Marine Biology and Biotechnology, Qingdao Marine Science and Technology Center, Qingdao 266237, China; Shandong Center of Technology Innovation for Oyster Seed Industry, Qingdao 266071, China; Southern Marine Science and Engineering Guangdong Laboratory (Zhanjiang), Zhanjiang 524006, China; National and Local Joint Engineering Laboratory of Ecological Mariculture, Qingdao 266071, ChinaEmaciation syndrome due to starvation is a significant cause of mortality in marine animals, yet the underlying mechanisms in non-feeding and weak/no-mobility marine bivalves remain poorly understood. This study investigated nutrient utilization and transcriptional responses in oysters subjected to a 44-day starvation period. Nutrient analysis revealed a distinct three-phase pattern in nutrient utilization. During the early stage (days 0–10), glycogen was rapidly consumed, with no mobilization of lipids, proteins, or fatty acids. In the late stage (days 23–44), glycogen was depleted, and there was significant consumption of lipids, proteins, fatty acids, and free amino acids. A newly identified ''transition metabolism'' phase, occurring between the two typical phases (days 10–23), was characterized by a slight compensatory increase in glycogen and lipids, alongside continued protein consumption and depletion of five fatty acids. This phase may represent ''the point of no return'' in starvation tolerance. Transcriptomic analysis revealed that the amino acid and lipid metabolism increased over starvation, while carbohydrate metabolism initially rose and then declined, with a notable tipping point on day 10. This pattern strongly supported the stepped change pattern identified by nutrient utilization. In contrast, immunological functions initially decreased before increasing, whereas functions related to cell growth and survival showed a consistent downward trend. Combined with the correlation between gene expression and symbiotic microbiota, these findings indicated that oysters, due to limited energy, activated insufficient immune responses, leading to increased pathogen abundance and higher mortality during prolonged starvation. This study refined the starvation stress tolerance limits (SSTL) model to better characterize oyster performance under prolonged starvation, offering valuable insights into emaciation syndrome and potential indicators for assessing health status and mortality risk in marine bivalves.http://www.sciencedirect.com/science/article/pii/S2352513425000353Emaciation syndromeStarvationNutrientTranscriptomeOyster mortality |
| spellingShingle | Mingkun Liu Chenchen Wei Wenwen Xu Lintao Tan Li Li Guofan Zhang Effect of prolonged starvation on nutrition utilization and transcriptional responses in Pacific oyster (Crassostrea gigas) Aquaculture Reports Emaciation syndrome Starvation Nutrient Transcriptome Oyster mortality |
| title | Effect of prolonged starvation on nutrition utilization and transcriptional responses in Pacific oyster (Crassostrea gigas) |
| title_full | Effect of prolonged starvation on nutrition utilization and transcriptional responses in Pacific oyster (Crassostrea gigas) |
| title_fullStr | Effect of prolonged starvation on nutrition utilization and transcriptional responses in Pacific oyster (Crassostrea gigas) |
| title_full_unstemmed | Effect of prolonged starvation on nutrition utilization and transcriptional responses in Pacific oyster (Crassostrea gigas) |
| title_short | Effect of prolonged starvation on nutrition utilization and transcriptional responses in Pacific oyster (Crassostrea gigas) |
| title_sort | effect of prolonged starvation on nutrition utilization and transcriptional responses in pacific oyster crassostrea gigas |
| topic | Emaciation syndrome Starvation Nutrient Transcriptome Oyster mortality |
| url | http://www.sciencedirect.com/science/article/pii/S2352513425000353 |
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