UPLC-MS metabolomics provides insights into the differences between black- and white-shelled Pacific oysters <i>Crassostrea gigas</i> -- Journal of Oceanology and Limnology,2021,39(1):340-349

	Cite this paper:
	Xi CHEN, Qiuyun JIANG, Hongce SONG, Lingling LI, Chaoyi XIE, Baoyu HUANG, Yaqiong LIU, Meiwei ZHANG, Lei WEI, Xiaotong WANG. UPLC-MS metabolomics provides insights into the differences between black- and white-shelled Pacific oysters Crassostrea gigas[J]. Journal of Oceanology and Limnology, 2021, 39(1): 340-349

UPLC-MS metabolomics provides insights into the differences between black- and white-shelled Pacific oysters Crassostrea gigas

Xi CHEN, Qiuyun JIANG, Hongce SONG, Lingling LI, Chaoyi XIE, Baoyu HUANG, Yaqiong LIU, Meiwei ZHANG, Lei WEI, Xiaotong WANG

School of Agriculture, Ludong University, Yantai 264025, China

Abstract:

A variety of shell colors are one of the most fundamental characteristics of molluscs, which have importantly ecological and economic significance. The Pacific oyster Crassostrea gigas is distributed in many sea areas around the world and also an aquacultured mollusc with high nutritional value. In this study, the whole soft body and the mantle tissue of black-shelled Pacific oyster (BSO) and white-shelled Pacific oyster (WSO) with starkly different melanin contents were compared, and the differences in physiology and metabolism between BSO and WSO were analyzed. The results of physiological indicators suggested BSO show more melanin, more dry matter, more crude lipid content, and stronger ability to scavenge free radicals than WSO. The altered metabolites of glycerophospholipids, fatty acyls, and steroids revealed different regulatory mechanisms of lipids. The correlation analysis of metabolomics and previously published RNAseq data suggested that BSO and WSO mainly differed in the basal metabolic processes, such as lipid, amino acid and purine metabolisms. This study provides insights into the changes in the physiological indictors and the metabolites of oysters with varying melanin content.

Key words: Crassostrea gigas|UPLC-MS metabolomics|physiological indicators|melanin|shell color

Received: 2020-03-12 Revised: 2020-05-03

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Articles by Xi CHEN

Articles by Qiuyun JIANG

Articles by Hongce SONG

Articles by Lingling LI

Articles by Chaoyi XIE

Articles by Baoyu HUANG

Articles by Yaqiong LIU

Articles by Meiwei ZHANG

Articles by Lei WEI

Articles by Xiaotong WANG

References:
Asha K K, Anandan R, Mathew S, Lakshmanan P T. 2014.Biochemical profile of oyster Crassostrea madrasensis and its nutritional attributes. The Egyptian Journal of Aquatic Research, 40(1):35-41.
Berik N, Çankırılıgil E C, Gül G. 2017. Mineral content of smooth scallop (Flexopecten glaber) caught Canakkale, Turkey and evaluation in terms of food safety. Journal of Trace Elements in Medicine and Biology, 42:97-102.
Chan C F, Huang C C, Lee M Y, Lin Y S. 2014. Fermented broth in tyrosinase- and melanogenesis inhibition.Molecules, 19(9):13 122-13 135.
Chen Q S, Wang X C, Cong P X, Liu Y J, Wang Y M, Xu J, Xue C H. 2017. Mechanism of phospholipid hydrolysis for oyster Crassostrea plicatula phospholipids during storage using shotgun lipidomics. Lipids, 52(12):1 045-1 058.
Cullis P T, De Kruijff B. 1979. Lipid polymorphism and the functional roles of lipids in biological membranes.Biochimica et Biophysica Acta (BBA)-Reviews on Biomembranes, 559(4):399-420.
Debecker S, Sommaruga R, Maes T, Stoks R. 2015. Larval UV exposure impairs adult immune function through a trade-off with larval investment in cuticular melanin. Functional Ecology, 29(10):1 292-1 299.
Dietvorst J, Londesborough J, Steensma H Y. 2005. Maltotriose utilization in lager yeast strains:MTT1 encodes a maltotriose transporter. Yeast, 22(10):775-788.
Ding J, Zhao L, Chang Y Q, Zhao W M, Du Z L, Hao Z L. 2015. Transcriptome sequencing and characterization of japanese scallop Patinopecten yessoensis from different shell color lines. PLoS One, 10(2):e0116406.
Dong X P, Zhu B W, Zhao H X, Zhou D Y, Wu H T, Yang J F, Li D M, Murata Y. 2010. Preparation and in vitro antioxidant activity of enzymatic hydrolysates from oyster (Crassostrea talienwhannensis) meat. International Journal of Food Science & Technology, 45(5):978-984.
ElObeid A S, Kamal-Eldin A, Abdelhalim M A K, Haseeb A M. 2017. Pharmacological properties of melanin and its function in health. Basic & Clinical Pharmacology & Toxicology, 120(6):515-522.
Eom D S, Inoue S, Patterson L B, Gordon T N, Slingwine R, Kondo S, Watanabe M, Parichy D M. 2012. Melanophore migration and survival during zebrafish adult pigment stripe development require the immunoglobulin superfamily adhesion molecule Igsf11. PLoS Genetics, 8(8):e1002899.
Feng D D, Li Q, Yu H, Zhao X L, Kong L F. 2015. Comparative transcriptome analysis of the Pacific Oyster Crassostrea gigas characterized by shell colors:identification of genetic bases potentially involved in pigmentation. PLoS One, 10(12):e0145257.
Gebhardt S E, Thomas R G. 2002. Nutritive Value of Foods.United States Department of Agriculture. Agricultural Research Service, Home and Garden Bulletin, Beltsville, Maryland.
Green T J, Dixon T J, Devic E, Adlard R D, Barnes A C. 2009.Differential expression of genes encoding anti-oxidant enzymes in Sydney rock oysters, Saccostrea glomerata(Gould) selected for disease resistance. Fish & Shellfish Immunology, 26(5):799-810.
Hansson L A. 2004. Plasticity in pigmentation induced by conflicting threats from predation and UV radiation.Ecology, 85(4):1 005-1 016.
Hao R J, Du X D, Yang C Y, Deng Y W, Zheng Z, Wang Q H. 2019. Integrated application of transcriptomics and metabolomics provides insights into unsynchronized growth in pearl oyster Pinctada fucata martensii. Science of the Total Environment, 666:46-56.
Hu S J, Zhao G H, Zheng Y X, Qu M, Jin Q, Tong C Q, Li W. 2017. Effect of drying procedures on the physicochemical properties and antioxidant activities of polysaccharides from Crassostrea gigas. PLoS One, 12(11):e0188536.
Jongejan A, Leurs R. 2005. Delineation of receptor-ligand interactions at the human histamine H₁ receptor by a combined approach of site-directed mutagenesis and computational techniques-or-how to bind the H₁ receptor. Archiv Der Pharmazie, 338(5-6):248-259.
Kanehisa M, Araki M, Goto S, Hattori M, Hirakawa M, Itoh M, Katayama T, Kawashima S, Okuda S, Tokimatsu T, Yamanishi Y. 2008. KEGG for linking genomes to life and the environment. Nucleic Acids Research, 36(S1):D480-D484.
Koizumi S, Yamamoto S, Hayasaka T, Konishi Y, YamaguchiOkada M, Goto-Inoue N, Sugiura Y, Setou M, Namba H. 2010. Imaging mass spectrometry revealed the production of lyso-phosphatidylcholine in the injured ischemic Rat Brain. Neuroscience, 168(1):219-225.
Lin J Y, Fisher D E. 2007. Melanocyte biology and skin pigmentation. Nature, 445(7130):843-850.
Liu X, Wu F C, Zhao H E, Zhang G F, Guo X M. 2009. A novel shell color variant of the pacific abalone Haliotis discus hannai Ino subject to genetic control and dietary influence.Journal of Shellfish Research, 28(2):419-424.
McCord J. 1985. Oxygen-derived free radicals in postischemic tissue injury. New England Journal of Medicine, 312(3):159-163.
Mitton J B. 1977. Shell color and pattern variation in Mytilus edulis and its adaptive significance. Chesapeake Science, 18:387-390.
Mochel F. 2018. Lipids and synaptic functions. Journal of Inherited Metabolic Disease, 41(6):1 117-1 122.
Moment G B. 1962. Reflexive selection:a possible answer to an old puzzle. Science, 136(3512):262-263.
Moret Y, Moreau J. 2012. The immune role of the arthropod exoskeleton. Invertebrate Survival Journal, 9:200-206.
Morris P. 2012. Animal eyes (Oxford Animal Biology Series)by Michael F. Land & Dan-Eric Nilsson. Zoological Journal of the Linnean Society, 166(4):912.
Newkirk G F. 1980. Genetics of shell color in Mytilus edulis L.and the association of growth rate with shell color. Journal of Experimental Marine Biology and Ecology, 47(1):89-94.
Pierce S K, Rowland-Faux L M, Crombie B N. 1995. The mechanism of glycine betaine regulation in response to hyperosmotic stress in oyster mitochondria:a comparative study of Atlantic and Chesapeake Bay oysters. Journal of Experimental Zoology, 271(3):161-170.
Sedej M, Platzer W, Vukoja A, Schuligoi R, Peskar B A, Heinemann Á, Waldhoer M. 2008. Effects of PGH₂ and PGD₂ on CRTH2 and DP receptors in primary cells and co-expressed in HEK293 cells. BMC Pharmacology, 8(S1):A10.
Sharma S, Wagh S, Govindarajan R. 2002. Melanosomal proteins-role in melanin polymerization. Pigment Cell Research, 15(2):127-133.
Shen Q, Wang Y Y, Gong L K, Guo R, Dong W, Cheung H Y. 2012. Shotgun lipidomics strategy for fast analysis of phospholipids in fisheries waste and its potential in species differentiation. Journal of Agricultural and Food Chemistry, 60(37):9 384-9 393.
Smith D A S. 1975. Polymorphism and selective predation in Donax faba Gmelin (Bivalvia:Tellinacea). Journal of Experimental Marine Biology and Ecology, 17(2):205-219.
Song J L, Li Q, Yu Y, Wan S, Han L C, Du S J. 2018. Mapping genetic loci for quantitative traits of golden shell color, mineral element contents, and growth-related traits in Pacific Oyster (Crassostrea gigas). Marine Biotechnology, 20(5):666-675.
Speiser D I, Johnsen S. 2008. Comparative morphology of the concave mirror eyes of scallops (Pectinoidea). American Malacological Bulletin, 26(1-2):27-33.
Thayer C W. 1971. Fish-like crypsis in swimming monomyaria.Journal of Molluscan Studies, 39(5):371-376.
Van Den Bossche K, Naeyaert J M, Lambert J. 2006. The quest for the mechanism of melanin transfer. Traffic, 7(7):769-778.
Videira I F D S, Moura D F L, Magina S. 2013. Mechanisms regulating melanogenesis. Anais Brasileiros de Dermatologia, 88(1):76-83.
Wang X T, Xu W J, Wei L, Zhu C L, He C, Song H C, Cai Z Q, Yu W C, Jiang Q Y, Li L L, Wang K, Feng C G. 2019.Nanopore sequencing and de novo assembly of a blackshelled Pacific oyster (Crassostrea gigas) genome.Frontiers in Genetics, 10:1 211.
Wei L, Jiang Q Y, Cai Z Q, Yu W C, He C, Guo W, Wang X T.2019. Immune-related molecular and physiological differences between black-shelled and white-shelled Pacific oysters Crassostrea gigas. Fish & Shellfish Immunology, 92:64-71.
Williams S T. 2017. Molluscan shell colour. Biological Reviews, 92(2):1 039-1 058.
Wolken J J. 1988. Photobehavior of marine invertebrates:extraocular photoreception. Comparative Biochemistry and Physiology Part C:Comparative Pharmacology, 91(1):145-149.
Wu C L, Jiang Q Y, Wei L, Cai Z Q, Chen J, Yu W C, He C, Wang J, Guo W, Wang X T. 2018. A rhodopsin-like gene may be associated with the light-sensitivity of adult pacific oyster Crassostrea gigas. Frontiers in physiology, 9:221.
Wu C L, Wang J, Yang Y J, Li Z, Guo T, Li Y C, Wang X T. 2015. Adult pacific oyster (Crassostrea gigas) may have light sensitivity. PLoS One, 10(10):e0140149.
Xing D, Li Q, Kong L F, Yu H. 2018. Heritability estimate for mantle edge pigmentation and correlation with shell pigmentation in the white-shell strain of Pacific oyster, Crassostrea gigas. Aquaculture, 482:73-77.
Xu L, Li Q, Yu H, Kong L F. 2017. Estimates of heritability for growth and shell color traits and their genetic correlations in the black shell strain of Pacific Oyster Crassostrea gigas. Marine Biotechnology, 19(5):421-429.
Xu M, Huang J, Shi Y, Zhang H, He M X. 2019. Comparative transcriptomic and proteomic analysis of yellow shell and black shell pearl oysters, Pinctada fucata martensii. BMC Genomics, 20(1):469.
Yin P P, Jia A R, Heimann K, Zhang M S, Liu X, Zhang W, Liu C H. 2020. Hot water pretreatment-induced significant metabolite changes in the sea cucumber Apostichopus japonicus. Food Chemistry, 314:126211.
Yu W C, He C, Cai Z Q, Xu F, Wei L, Chen J, Jiang Q Y, Wei N, Li Z, Guo W, Wang X T. 2017. A preliminary study on the pattern, the physiological bases and the molecular mechanism of the adductor muscle scar pigmentation in Pacific oyster Crassostrea gigas. Frontiers in Physiology, 8:699.
Zhang G F, Fang X D, Guo X M, Li L, Luo R B, Xu F, Yang P C, Zhang L L, Wang X T, Qi H G, Xiong Z Q, Que H Y, Xie Y L, Holland P W H, Paps J, Zhu Y B, Wu F C, Chen Y X, Wang J F, Peng C F, Meng J, Yang L, Liu J, Wen B, Zhang N, Huang Z Y, Zhu Q H, Feng Y, Mount A, Hedgecock D, Xu Z, Liu Y J, Domazet-Lošo T, Du Y S, Sun X Q, Zhang S D, Liu B H, Cheng P Z, Jiang X T, Li J, Fan D D, Wang W, Fu W J, Wang T, Wang B, Zhang J B, Peng Z Y, Li Y X, Li N, Wang J P, Chen M S, He Y, Tan F J, Song X R, Zheng Q M, Huang R L, Yang H L, Du X D, Chen L, Yang M, Gaffney P M, Wang S, Luo L H, She Z C, Ming Y, Huang W, Zhang S, Huang B Y, Zhang Y, Qu T, Ni P X, Miao G Y, Wang J Y, Wang Q, Steinberg C E W, Wang H Y, Li N, Qian L M, Zhang G J, Li Y R, Yang H M, Liu X, Wang J, Yin Y, Wang J. 2012. The oyster genome reveals stress adaptation and complexity of shell formation. Nature, 490(7418):49-54.
Zhu W H, Yu H T, Wang Y, Chang Y, Wan J Y, Xu N, Wang J L, Liu W S. 2019. Integration of transcriptomics, proteomics and metabolomics data to reveal the biological mechanisms of abrin injury in human lung epithelial cells.Toxicology Letters, 312:1-10.