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Penaeid shrimp counteract high ammonia stress by generating and using functional peptides from hemocyanin, such as HMCs27
Agricultural and anthropogenic activities release high ammonia levels into aquatic ecosystems, severely affecting aquatic organisms. Penaeid shrimp can survive high ammonia stress conditions, but the underlying molecular mechanisms are unknown. Here, total hemocyanin and oxyhemocyanin levels decreas...
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Published in: | The Science of the total environment 2023-12, Vol.905, p.167073-167073, Article 167073 |
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container_title | The Science of the total environment |
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creator | Zhao, Mingming Zheng, Zhihong Wang, Chuanqi Yao, Defu Lin, Zhongyang Zhao, Yongzhen Chen, Xiuli Li, Shengkang Aweya, Jude Juventus Zhang, Yueling |
description | Agricultural and anthropogenic activities release high ammonia levels into aquatic ecosystems, severely affecting aquatic organisms. Penaeid shrimp can survive high ammonia stress conditions, but the underlying molecular mechanisms are unknown. Here, total hemocyanin and oxyhemocyanin levels decreased in Penaeus vannamei plasma under high ammonia stress. When shrimp were subjected to high ammonia stress for 12 h, 24 hemocyanin (HMC) derived peptides were identified in shrimp plasma, among which one peptide, designated as HMCs27, was chosen for further analysis. Shrimp survival was significantly enhanced after treatment with the recombinant protein of HMCs27 (rHMCs27), followed by high ammonia stress. Transcriptome analysis of shrimp hepatopancreas after treatment with or without rHMCs27 followed by high ammonia stress revealed 973 significantly dysregulated genes, notable among which were genes involved in oxidation and metabolism, such as cytochrome C, catalase (CAT), isocitrate dehydrogenase, superoxide dismutase (SOD), trypsin, chymotrypsin, glutathione peroxidase, glutathione s-transferase (GST), and alanine aminotransferase (ALT). In addition, levels of key biochemical indicators, such as SOD, CAT, and total antioxidant capacity (T-AOC), were significantly enhanced, whereas hepatopancreas malondialdehyde levels and plasma pH, NH3, GST, and ALT levels were significantly decreased after rHMCs27 treatment followed by high ammonia stress. Moreover, high ammonia stress induced hepatopancreas tissue injury and apoptosis, but rHMCs27 treatment ameliorated these effects. Collectively, the current study revealed that in response to high ammonia stress, shrimp generate functional peptides, such as peptide HMCs27 from hemocyanin, which helps to attenuate the ammonia toxicity by enhancing the antioxidant system and the tricarboxylic acid cycle to decrease plasma NH3 levels and pH.
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•High ammonia stress decreases plasma hemocyanin and oxygenated hemocyanin levels.•Shrimp hemocyanin degrades into functional peptides during ammonia stress.•Hemocyanin-derived peptide HMCs27 helps shrimp counteract ammonia toxicity.•HMCs27 affects the antioxidant system to reduce plasma pH and NH3 levels.•Shrimp survival under ammonia stress is significantly improved by HMCs27. |
doi_str_mv | 10.1016/j.scitotenv.2023.167073 |
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[Display omitted]
•High ammonia stress decreases plasma hemocyanin and oxygenated hemocyanin levels.•Shrimp hemocyanin degrades into functional peptides during ammonia stress.•Hemocyanin-derived peptide HMCs27 helps shrimp counteract ammonia toxicity.•HMCs27 affects the antioxidant system to reduce plasma pH and NH3 levels.•Shrimp survival under ammonia stress is significantly improved by HMCs27.</description><identifier>ISSN: 0048-9697</identifier><identifier>EISSN: 1879-1026</identifier><identifier>DOI: 10.1016/j.scitotenv.2023.167073</identifier><language>eng</language><publisher>Elsevier B.V</publisher><subject>Ammonia toxicity ; Antioxidant system ; Hemocyanin peptides ; Penaeus vannamei ; Tissue damage ; Transcriptome analysis</subject><ispartof>The Science of the total environment, 2023-12, Vol.905, p.167073-167073, Article 167073</ispartof><rights>2023 Elsevier B.V.</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c348t-d2f135f4ffebc032d63276cabad591bac37b052acdefe15eaabf4ec80866f6243</citedby><cites>FETCH-LOGICAL-c348t-d2f135f4ffebc032d63276cabad591bac37b052acdefe15eaabf4ec80866f6243</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>314,780,784,27924,27925</link.rule.ids></links><search><creatorcontrib>Zhao, Mingming</creatorcontrib><creatorcontrib>Zheng, Zhihong</creatorcontrib><creatorcontrib>Wang, Chuanqi</creatorcontrib><creatorcontrib>Yao, Defu</creatorcontrib><creatorcontrib>Lin, Zhongyang</creatorcontrib><creatorcontrib>Zhao, Yongzhen</creatorcontrib><creatorcontrib>Chen, Xiuli</creatorcontrib><creatorcontrib>Li, Shengkang</creatorcontrib><creatorcontrib>Aweya, Jude Juventus</creatorcontrib><creatorcontrib>Zhang, Yueling</creatorcontrib><title>Penaeid shrimp counteract high ammonia stress by generating and using functional peptides from hemocyanin, such as HMCs27</title><title>The Science of the total environment</title><description>Agricultural and anthropogenic activities release high ammonia levels into aquatic ecosystems, severely affecting aquatic organisms. Penaeid shrimp can survive high ammonia stress conditions, but the underlying molecular mechanisms are unknown. Here, total hemocyanin and oxyhemocyanin levels decreased in Penaeus vannamei plasma under high ammonia stress. When shrimp were subjected to high ammonia stress for 12 h, 24 hemocyanin (HMC) derived peptides were identified in shrimp plasma, among which one peptide, designated as HMCs27, was chosen for further analysis. Shrimp survival was significantly enhanced after treatment with the recombinant protein of HMCs27 (rHMCs27), followed by high ammonia stress. Transcriptome analysis of shrimp hepatopancreas after treatment with or without rHMCs27 followed by high ammonia stress revealed 973 significantly dysregulated genes, notable among which were genes involved in oxidation and metabolism, such as cytochrome C, catalase (CAT), isocitrate dehydrogenase, superoxide dismutase (SOD), trypsin, chymotrypsin, glutathione peroxidase, glutathione s-transferase (GST), and alanine aminotransferase (ALT). In addition, levels of key biochemical indicators, such as SOD, CAT, and total antioxidant capacity (T-AOC), were significantly enhanced, whereas hepatopancreas malondialdehyde levels and plasma pH, NH3, GST, and ALT levels were significantly decreased after rHMCs27 treatment followed by high ammonia stress. Moreover, high ammonia stress induced hepatopancreas tissue injury and apoptosis, but rHMCs27 treatment ameliorated these effects. Collectively, the current study revealed that in response to high ammonia stress, shrimp generate functional peptides, such as peptide HMCs27 from hemocyanin, which helps to attenuate the ammonia toxicity by enhancing the antioxidant system and the tricarboxylic acid cycle to decrease plasma NH3 levels and pH.
[Display omitted]
•High ammonia stress decreases plasma hemocyanin and oxygenated hemocyanin levels.•Shrimp hemocyanin degrades into functional peptides during ammonia stress.•Hemocyanin-derived peptide HMCs27 helps shrimp counteract ammonia toxicity.•HMCs27 affects the antioxidant system to reduce plasma pH and NH3 levels.•Shrimp survival under ammonia stress is significantly improved by HMCs27.</description><subject>Ammonia toxicity</subject><subject>Antioxidant system</subject><subject>Hemocyanin peptides</subject><subject>Penaeus vannamei</subject><subject>Tissue damage</subject><subject>Transcriptome analysis</subject><issn>0048-9697</issn><issn>1879-1026</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2023</creationdate><recordtype>article</recordtype><recordid>eNqFkE9rGzEQxUVpoW7az1Ade8i6-rMrrY_BpE0hITmkZ6GVRraMV9potAF_-6xx6LVzmYF578H7EfKdszVnXP08rNHFmiuk17VgQq650kzLD2TFe71pOBPqI1kx1vbNRm30Z_IF8cCW0T1fkdMTJAvRU9yXOE7U5TlVKNZVuo-7PbXjmFO0FGsBRDqc6A7S8q8x7ahNns54vsKcXI052SOdYKrRA9JQ8kj3MGZ3simma4qzWwKR3j1sUeiv5FOwR4Rv7_uK_P11-7y9a-4ff__Z3tw3TrZ9bbwIXHahDQEGx6TwSgqtnB2s7zZ8sE7qgXXCOg8BeAfWDqEF17NeqaBEK6_Ij0vuVPLLDFjNGNHB8WgT5BmN6FWne6kFW6T6InUlIxYIZlqg2HIynJkzbHMw_2CbM2xzgb04by5OWJq8RihnHSQHPhZw1fgc_5vxBhekkCE</recordid><startdate>20231220</startdate><enddate>20231220</enddate><creator>Zhao, Mingming</creator><creator>Zheng, Zhihong</creator><creator>Wang, Chuanqi</creator><creator>Yao, Defu</creator><creator>Lin, Zhongyang</creator><creator>Zhao, Yongzhen</creator><creator>Chen, Xiuli</creator><creator>Li, Shengkang</creator><creator>Aweya, Jude Juventus</creator><creator>Zhang, Yueling</creator><general>Elsevier B.V</general><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope></search><sort><creationdate>20231220</creationdate><title>Penaeid shrimp counteract high ammonia stress by generating and using functional peptides from hemocyanin, such as HMCs27</title><author>Zhao, Mingming ; Zheng, Zhihong ; Wang, Chuanqi ; Yao, Defu ; Lin, Zhongyang ; Zhao, Yongzhen ; Chen, Xiuli ; Li, Shengkang ; Aweya, Jude Juventus ; Zhang, Yueling</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c348t-d2f135f4ffebc032d63276cabad591bac37b052acdefe15eaabf4ec80866f6243</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2023</creationdate><topic>Ammonia toxicity</topic><topic>Antioxidant system</topic><topic>Hemocyanin peptides</topic><topic>Penaeus vannamei</topic><topic>Tissue damage</topic><topic>Transcriptome analysis</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Zhao, Mingming</creatorcontrib><creatorcontrib>Zheng, Zhihong</creatorcontrib><creatorcontrib>Wang, Chuanqi</creatorcontrib><creatorcontrib>Yao, Defu</creatorcontrib><creatorcontrib>Lin, Zhongyang</creatorcontrib><creatorcontrib>Zhao, Yongzhen</creatorcontrib><creatorcontrib>Chen, Xiuli</creatorcontrib><creatorcontrib>Li, Shengkang</creatorcontrib><creatorcontrib>Aweya, Jude Juventus</creatorcontrib><creatorcontrib>Zhang, Yueling</creatorcontrib><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><jtitle>The Science of the total environment</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Zhao, Mingming</au><au>Zheng, Zhihong</au><au>Wang, Chuanqi</au><au>Yao, Defu</au><au>Lin, Zhongyang</au><au>Zhao, Yongzhen</au><au>Chen, Xiuli</au><au>Li, Shengkang</au><au>Aweya, Jude Juventus</au><au>Zhang, Yueling</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Penaeid shrimp counteract high ammonia stress by generating and using functional peptides from hemocyanin, such as HMCs27</atitle><jtitle>The Science of the total environment</jtitle><date>2023-12-20</date><risdate>2023</risdate><volume>905</volume><spage>167073</spage><epage>167073</epage><pages>167073-167073</pages><artnum>167073</artnum><issn>0048-9697</issn><eissn>1879-1026</eissn><abstract>Agricultural and anthropogenic activities release high ammonia levels into aquatic ecosystems, severely affecting aquatic organisms. Penaeid shrimp can survive high ammonia stress conditions, but the underlying molecular mechanisms are unknown. Here, total hemocyanin and oxyhemocyanin levels decreased in Penaeus vannamei plasma under high ammonia stress. When shrimp were subjected to high ammonia stress for 12 h, 24 hemocyanin (HMC) derived peptides were identified in shrimp plasma, among which one peptide, designated as HMCs27, was chosen for further analysis. Shrimp survival was significantly enhanced after treatment with the recombinant protein of HMCs27 (rHMCs27), followed by high ammonia stress. Transcriptome analysis of shrimp hepatopancreas after treatment with or without rHMCs27 followed by high ammonia stress revealed 973 significantly dysregulated genes, notable among which were genes involved in oxidation and metabolism, such as cytochrome C, catalase (CAT), isocitrate dehydrogenase, superoxide dismutase (SOD), trypsin, chymotrypsin, glutathione peroxidase, glutathione s-transferase (GST), and alanine aminotransferase (ALT). In addition, levels of key biochemical indicators, such as SOD, CAT, and total antioxidant capacity (T-AOC), were significantly enhanced, whereas hepatopancreas malondialdehyde levels and plasma pH, NH3, GST, and ALT levels were significantly decreased after rHMCs27 treatment followed by high ammonia stress. Moreover, high ammonia stress induced hepatopancreas tissue injury and apoptosis, but rHMCs27 treatment ameliorated these effects. Collectively, the current study revealed that in response to high ammonia stress, shrimp generate functional peptides, such as peptide HMCs27 from hemocyanin, which helps to attenuate the ammonia toxicity by enhancing the antioxidant system and the tricarboxylic acid cycle to decrease plasma NH3 levels and pH.
[Display omitted]
•High ammonia stress decreases plasma hemocyanin and oxygenated hemocyanin levels.•Shrimp hemocyanin degrades into functional peptides during ammonia stress.•Hemocyanin-derived peptide HMCs27 helps shrimp counteract ammonia toxicity.•HMCs27 affects the antioxidant system to reduce plasma pH and NH3 levels.•Shrimp survival under ammonia stress is significantly improved by HMCs27.</abstract><pub>Elsevier B.V</pub><doi>10.1016/j.scitotenv.2023.167073</doi><tpages>1</tpages></addata></record> |
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subjects | Ammonia toxicity Antioxidant system Hemocyanin peptides Penaeus vannamei Tissue damage Transcriptome analysis |
title | Penaeid shrimp counteract high ammonia stress by generating and using functional peptides from hemocyanin, such as HMCs27 |
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