Multi-tissue metabolomic profiling reveals the crucial metabolites and pathways associated with scallop growth

Abstract Background Bivalves represent a vital economic resource in aquaculture for their high productivity and extensive market demand. Growth is one of the most important and desired aquaculture traits for bivalves, regulated by multiple levels, notably intricate metabolic processes. However, the...

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Main Authors: Yihan Zhang, Huizhen Wang, Shiqi Liu, Xiangfu Kong, Lirong Chang, Liang Zhao, Zhenmin Bao, Xiaoli Hu
Format: Article
Language:English
Published: BMC 2024-11-01
Series:BMC Genomics
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Online Access:https://doi.org/10.1186/s12864-024-11016-4
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author Yihan Zhang
Huizhen Wang
Shiqi Liu
Xiangfu Kong
Lirong Chang
Liang Zhao
Zhenmin Bao
Xiaoli Hu
author_facet Yihan Zhang
Huizhen Wang
Shiqi Liu
Xiangfu Kong
Lirong Chang
Liang Zhao
Zhenmin Bao
Xiaoli Hu
author_sort Yihan Zhang
collection DOAJ
description Abstract Background Bivalves represent a vital economic resource in aquaculture for their high productivity and extensive market demand. Growth is one of the most important and desired aquaculture traits for bivalves, regulated by multiple levels, notably intricate metabolic processes. However, the understanding of the metabolic profiles that influence bivalve growth is limited, particularly from a multi-tissue perspective. Results In this study, metabolic profiles of multiple tissues of Chlamys farreri with different growth performance were systematically investigated by ultraperformance liquid chromatography quadrupole time-of-flight mass spectrometry (UPLC-Q-TOF-MS). Through comparing the metabolic variation between fast-growing (FG) scallops and slow-growing (SG) scallops, 613, 509, 105, and 192 significantly different metabolites (SDMs) were identified in the mantle, gill, adductor muscle, and digestive gland, respectively. Growth-related metabolic pathways including sphingolipid metabolism, fatty acid biosynthesis, and ABC transporter pathway, along with 11 SDMs associated with growth traits were identified in all four tissues, implying they were involved in the growth of multiple tissues in scallops. Tissue-specific metabolic profiling indicated that sulfur-containing amino acid metabolism in the mantle potentially contributed to shell growth, while the gill synergistically participated with the mantle through various metabolic processes, such as tyrosine metabolism, glycine, serine, and threonine metabolism and melanogenesis; energy metabolism was crucial for adductor muscle growth; and nutrients digestion and absorption in the digestive gland were linked to scallop growth. Conclusions Our results represent the first comprehensive analysis of the crucial pathways and metabolites associated with the growth of C. farreri, offering valuable insights for future bivalve aquaculture production.
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spelling doaj-art-f2c1c602cd7d421a85df02b8dc05abbd2024-11-17T12:11:41ZengBMCBMC Genomics1471-21642024-11-0125111610.1186/s12864-024-11016-4Multi-tissue metabolomic profiling reveals the crucial metabolites and pathways associated with scallop growthYihan Zhang0Huizhen Wang1Shiqi Liu2Xiangfu Kong3Lirong Chang4Liang Zhao5Zhenmin Bao6Xiaoli Hu7MOE Key Laboratory of Marine Genetics and Breeding, College of Marine Life Sciences, Ocean University of ChinaMOE Key Laboratory of Marine Genetics and Breeding, College of Marine Life Sciences, Ocean University of ChinaMOE Key Laboratory of Marine Genetics and Breeding, College of Marine Life Sciences, Ocean University of ChinaMOE Key Laboratory of Marine Genetics and Breeding, College of Marine Life Sciences, Ocean University of ChinaMOE Key Laboratory of Marine Genetics and Breeding, College of Marine Life Sciences, Ocean University of ChinaLiaoning Ocean and Fisheries Science Research InstituteMOE Key Laboratory of Marine Genetics and Breeding, College of Marine Life Sciences, Ocean University of ChinaMOE Key Laboratory of Marine Genetics and Breeding, College of Marine Life Sciences, Ocean University of ChinaAbstract Background Bivalves represent a vital economic resource in aquaculture for their high productivity and extensive market demand. Growth is one of the most important and desired aquaculture traits for bivalves, regulated by multiple levels, notably intricate metabolic processes. However, the understanding of the metabolic profiles that influence bivalve growth is limited, particularly from a multi-tissue perspective. Results In this study, metabolic profiles of multiple tissues of Chlamys farreri with different growth performance were systematically investigated by ultraperformance liquid chromatography quadrupole time-of-flight mass spectrometry (UPLC-Q-TOF-MS). Through comparing the metabolic variation between fast-growing (FG) scallops and slow-growing (SG) scallops, 613, 509, 105, and 192 significantly different metabolites (SDMs) were identified in the mantle, gill, adductor muscle, and digestive gland, respectively. Growth-related metabolic pathways including sphingolipid metabolism, fatty acid biosynthesis, and ABC transporter pathway, along with 11 SDMs associated with growth traits were identified in all four tissues, implying they were involved in the growth of multiple tissues in scallops. Tissue-specific metabolic profiling indicated that sulfur-containing amino acid metabolism in the mantle potentially contributed to shell growth, while the gill synergistically participated with the mantle through various metabolic processes, such as tyrosine metabolism, glycine, serine, and threonine metabolism and melanogenesis; energy metabolism was crucial for adductor muscle growth; and nutrients digestion and absorption in the digestive gland were linked to scallop growth. Conclusions Our results represent the first comprehensive analysis of the crucial pathways and metabolites associated with the growth of C. farreri, offering valuable insights for future bivalve aquaculture production.https://doi.org/10.1186/s12864-024-11016-4MetabolomicsBivalveMulti-tissueGrowthChlamys farreri
spellingShingle Yihan Zhang
Huizhen Wang
Shiqi Liu
Xiangfu Kong
Lirong Chang
Liang Zhao
Zhenmin Bao
Xiaoli Hu
Multi-tissue metabolomic profiling reveals the crucial metabolites and pathways associated with scallop growth
BMC Genomics
Metabolomics
Bivalve
Multi-tissue
Growth
Chlamys farreri
title Multi-tissue metabolomic profiling reveals the crucial metabolites and pathways associated with scallop growth
title_full Multi-tissue metabolomic profiling reveals the crucial metabolites and pathways associated with scallop growth
title_fullStr Multi-tissue metabolomic profiling reveals the crucial metabolites and pathways associated with scallop growth
title_full_unstemmed Multi-tissue metabolomic profiling reveals the crucial metabolites and pathways associated with scallop growth
title_short Multi-tissue metabolomic profiling reveals the crucial metabolites and pathways associated with scallop growth
title_sort multi tissue metabolomic profiling reveals the crucial metabolites and pathways associated with scallop growth
topic Metabolomics
Bivalve
Multi-tissue
Growth
Chlamys farreri
url https://doi.org/10.1186/s12864-024-11016-4
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