Cite this paper:
Yang ZHANG, Youquan WANG, Xiaoyu LIU, Beichen DING, Yi SUN, Yaqing CHANG, Jun DING. Metabolomics analysis for skin ulceration syndrome of Apostichopus japonicus based on UPLC/Q-TOF MS[J]. Journal of Oceanology and Limnology, 2021, 39(4): 1559-1569

Metabolomics analysis for skin ulceration syndrome of Apostichopus japonicus based on UPLC/Q-TOF MS

Yang ZHANG, Youquan WANG, Xiaoyu LIU, Beichen DING, Yi SUN, Yaqing CHANG, Jun DING
Key Laboratory of Mariculture & Stock Enhancement in North China's Sea, Ministry of Agriculture and Rural Affairs, Dalian Ocean University, Dalian 116023, China
Abstract:
Skin ulceration syndrome (SUS) is the main diseases affected the development of sea cucumber (Apostichopus japonicus) culture industries. To better observe the changes in the sea cucumber A. japonicus with SUS and understand the pathogenesis of the disease, activities of superoxide dismutase (SOD), catalase (CAT), and level of malondialdehyde (MDA) in coelomic fluid were detected using the Assay Kit and metabolites in the body wall were assessed using ultra-performance liquid chromatography and quadrupole-time of flight mass spectrometry. The results indicated that level of MDA was increased during SUS compared with healthy individuals (P<0.01), but activities of SOD and CAT were reduced (P<0.05). In metabolomics analysis, metabolites, such as adenosine, choline, betaine aldehyde, palmitic acid, and taurine, were found to be upregulated and 2-oxoadipic acid, anthranilic acid (vitamin L1), thioetheramide-PC, cholesterol-3-sulfate, and pentadecanoic acid were downregulated (VIP>1 and P<0.1). Pathway enrichment analysis indicated most enrichment of KEGG pathways were mainly related to energy metabolism, immunity, and osmoregulation such as ABC transporters, glycine, serine and threonine metabolism, tryptophan metabolism and neuroactive ligand-receptor interaction. Our study reflected the difference in enzyme activity and metabolites between A. japonicus with SUS and those without, which will provide reference data for investigating SUS.
Key words:    Apostichopus japonicus|skin ulceration syndrome (SUS)|metabolome|differential metabolites   
Received: 2020-05-25   Revised: 2020-07-22
Tools
PDF (1512 KB) Free
Print this page
Add to favorites
Email this article to others
Authors
Articles by Yang ZHANG
Articles by Youquan WANG
Articles by Xiaoyu LIU
Articles by Beichen DING
Articles by Yi SUN
Articles by Yaqing CHANG
Articles by Jun DING
References:
Baldissera M D, Souza C F, Doleski P H, Monteiro S G, da Silva A S, Baldisserotto B. 2018. Serum adenosine deaminase and xanthine oxidase activities in silver catfish naturally infected with Ichthyophthirius multifiliis:the influence of these enzymes on inflammatory and oxidative status. Journal of Fish Diseases, 41(2):263-268, https://doi.org/10.1111/jfd.12709.
Borths E L, Locher K P, Lee A T, Rees D C. 2002. The structure of Escherichia coli BtuF and binding to its cognate ATP binding cassette transporter. Proceedings of the National Academy of Sciences of the United States of America, 99(26):16 642-16 647, https://doi.org/10.1073/pnas. 262659699.
Chang Z Q, Li J, Liu P, Kuo M M C, He Y Y, Chen P, Li J T. 2012. cDNA cloning and expression profile analysis of an ATP-binding cassette transporter in the hepatopancreas and intestine of shrimp Fenneropenaeus chinensis.Aquaculture, 356-357:250-255, https://doi.org/10.1016/j.aquaculture.2012.05.009.
Cossu C, Doyotte A, Babut M, Exinger A, Vasseur P. 2000.Antioxidant biomarkers in freshwater bivalves, Unio tumidus, in response to different contamination profiles of aquatic sediments. Ecotoxicology and Environmental Safety, 45(2):106-121, https://doi.org/10.1006/eesa.1999.1842.
Deng H, He C B, Zhou Z C, Liu C, Tan K F, Wang N B, Jiang B, Gao X G, Liu W D. 2008. Isolation and pathogenicity of pathogens from skin ulceration disease and viscera ejection syndrome of the sea cucumber Apostichopus japonicus. Aquaculture, 287(1-2):18-27, https://doi.org/10.1016/j.aquaculture.2008.10.015.
Ejendal K F, Hrycyna C A. 2002. Multidrug resistance and cancer:the role of the human ABC transporter ABCG2.Current Protein and Peptide Science, 3(5):503-511, https://doi.org/10.2174/1389203023380521.
Gu C X, Cheng Y L, Zhen X, Chen X X, Zhou K W. 2019.Determination of progestin residues in fish by UPLC-QTOF/MS coupled with QuEChERS. Journal of Analytical Methods in Chemistry, 2019:6426958, https://doi.org/10.1155/2019/6426958.
Hao R J, Wang Z M, Yang C Y, Deng Y W, Zheng Z, Wang Q H, Du X D. 2018. Metabolomic responses of juvenile pearl oyster Pinctada maxima to different growth performances. Aquaculture, 491:258-265, https://doi.org/10.1016/j.aquaculture.2018.03.050.
Hu C H, Xia M S, Xiong L, Xu X R. 2005. Effects of Cu bearing montmorillonite on Aeromonas hydrophila adhesion to epithelial cells of Nile tilapia. Journal of Fisheries of China, 29(5):619-623, https://doi.org/10.3321/j.issn:1000-0615.2005.05.006. (in Chinese with English abstract)
Huo D, Sun L, Ru X S, Zhang L B, Lin C G, Liu S L, Xin X K, Yang H S. 2018. Impact of hypoxia stress on the physiological responses of sea cucumber Apostichopus japonicus:respiration, digestion, immunity and oxidative damage. PeerJ, 6:e4651, https://doi.org/10.7717/peerj.4651.
Huo D, Sun L, Zhang L B, Ru X S, Liu S L, Yang H S. 2019.Metabolome responses of the sea cucumber Apostichopus japonicus to multiple environmental stresses:heat and hypoxia. Marine Pollution Bulletin, 138:407-420, https://doi.org/10.1016/j.marpolbul.2018.11.063.
Jiang J W, Zhou Z C, Dong Y, Jiang B, Chen Z, Gao S, Guan X Y, Han L. 2017. Seasonal variations of immune parameters in the coelomic fluid of sea cucumber Apostichopus japonicus cultured in pond. Aquaculture Research, 48(4):1 677-1 687, https://doi.org/10.1111/are.13005.
Jiang X L, Du Y S, Wang P, Liu R Z, Yang X S, Lv Q. 2009.Effects of alginate-derived oligosaccharide on the activities of immunoenzymes in the coelomic fluid and body wall of sea cucumber (Apostichopus japonicus).Periodical of Ocean University of China, 39(6):1 188-1 192, https://doi.org/10.3969/j.issn.1672-5174.2009.06.006. (in Chinese with English abstract)
Kanehisa M, Sato Y, Kawashima M, Furumichi M, Tanabe M. 2015. KEGG as a reference resource for gene and protein annotation. Nucleic Acids Research, 44(D1):D457-D462, https://doi.org/10.1093/nar/gkv1070.
Kathawala R J, Gupta P, Ashby C R Jr, Chen Z S. 2015. The modulation of ABC transporter-mediated multidrug resistance in cancer:a review of the past decade. Drug Resistance Updates, 18:1-17, https://doi.org/10.1016/j.drup.2014.11.002.
Lasley R D, Rhee J W, Van Wylen D G L, Mentzer R M Jr. 1990. Adenosine A1 receptor mediated protection of the globally ischemic isolated rat heart. Journal of Molecular and Cellular Cardiology, 22(1):39-47, https://doi.org/10.1016/0022-2828(90)90970-D.
Lauss M, Kriegner A, Vierlinger K, Noehammer C. 2007.Characterization of the drugged human genome.Pharmacogenomics, 8:1 063-1 073, https://doi.org/10.2217/14622416.8.8.1063.
Li C H, Feng W D, Qiu L H, Xia C G, Su X R, Jin C H, Zhou T T, Zeng Y, Li T W. 2012. Characterization of skin ulceration syndrome associated microRNAs in sea cucumber Apostichopus japonicus by deep sequencing.Fish and Shellfish Immunology, 33(2):436-441, https://doi.org/10.1016/j.fsi.2012.04.013.
Li H W, Zhu Q, Wu L Y, Yin Y L, Kong X F. 2016. Physiological function and dietary application of tryptophan in livestock and poultry. Chinese Journal of Animal Nutrition, 28(3):659-664 https://doi.org/10.3969/j.issn.1006-267x.2016.03.004. (in Chinese with English abstract)
Liu H, Zheng F, Sun X, Hong X, Dong S, Wang B, Tang X, Wang Y. 2010. Identification of the pathogens associated with skin ulceration and peristome tumescence in cultured sea cucumbers Apostichopus japonicus (Selenka). Journal of Invertebrate Pathology, 105(3):236-242, https://doi.org/10.1016/j.jip.2010.05.016.
Liu X L, Ji C L, Zhao J M, Wu H F. 2013. Differential metabolic responses of clam Ruditapes philippinarum to Vibrio anguillarum and Vibrio splendidus challenges. Fish and Shellfish Immunology, 35(6):2 001-2 007, https://doi.org/10.1016/j.fsi.2013.09.014.
Lv Z M, Guo M, Li C H, Shao Y N, Zhao X L, Zhang W W. 2019. Divergent proteomics response of Apostichopus japonicus suffering from skin ulceration syndrome and pathogen infection. Comparative Biochemistry and Physiology-Part D:Genomics and Proteomics, 30:196-205, https://doi.org/10.1016/j.cbd.2019.03.003.
Ma X Z, Pang Z D, Wang J H, Song Z, Zhao L M, Du X J, Deng X L. 2018. The role and mechanism of KCa3.1 channels in human monocyte migration induced by palmitic acid. Experimental Cell Research, 369(2):208-217, https://doi.org/10.1016/j.yexcr.2018.05.020.
Mallat Z, Lambeau G, Tedgui A. 2010. Lipoprotein-associated and secreted phospholipases A2 in cardiovascular disease.Circulation, 122(21):2 183-2 200, https://doi.org/10.1161/CIRCULATIONAHA.110.936393.
Perrino L A, Pierce S K. 2000. Betaine aldehyde dehydrogenase kinetics partially account for oyster population differences in glycine betaine synthesis. The Journal of Experimental Zoology, 286(3):238-249, https://doi.org/10.1002/(SICI) 1097-010X(20000215)286:3<238::AID-JEZ3>3.0.CO;2-E.
Pfeuffer M, Jaudszus A. 2016. Pentadecanoic and heptadecanoic acids:multifaceted odd-chain fatty acids. Advances in Nutrition, 7(4):730-734, https://doi.org/10.3945/an.115.011387.
Pillon N J, Azizi P M, Li Y E, Liu J, Wang C, Chan K L, Hopperton K E, Bazinet R P, Heit B, Bilan P J, Lee W L, Klip A. 2015. Palmitate-induced inflammatory pathways in human adipose microvascular endothelial cells promote monocyte adhesion and impair insulin transcytosis.American Journal of Physiology-Endocrinology and Metabolism, 309(1):E35-E44, https://doi.org/10.1152/ajpendo.00611.2014.
Richard L F, Dahms T E, Webster R O. 1998. Adenosine prevents permeability increase in oxidant-injured endothelial monolayers. American Journal of Physiology-Heart and Circulatory Physiology, 274(1):H35-H42, https://doi.org/10.1152/ajpheart.1998.274.1.H35.
Roccatagliata A J, Maier M S, Seldes A M, Pujol C A, Damonte E B. 1996. Antiviral sulfated steroids from the ophiuroid Ophioplocus januarii. Journal of Natural Products, 59(9):887-889, https://doi.org/10.1021/np960171a.
Roch P. 1999. Defense mechanisms and disease prevention in farmed marine invertebrates. Aquaculture, 172(1-2):125-145, https://doi.org/10.1016/S0044-8486(98)00439-6.
Sabatine M S, Liu E, Morrow D A, Heller E, McCarroll R, Wiegand R, Berriz G F, Roth F P, Gerszten R E. 2005.Metabolomic identification of novel biomarkers of myocardial ischemia. Circulation, 112(25):3 868-3 875, https://doi.org/10.1161/CIRCULATIONAHA.105.569137.
Shao Y, Li C H, Ou C R, Zhang P, Lu Y L, Su X R, Li Y, Li T W. 2013. Divergent metabolic responses of Apostichopus japonicus suffered from skin ulceration syndrome and pathogen challenge. Journal of Agricultural and Food Chemistry, 61(45):10 766-10 771, https://doi.org/10.1021/jf4038776.
Shibata K, Yasui M, Sano M, Fukuwatari T. 2011. Fluorometric determination of 2-oxoadipic acid, a common metabolite of tryptophan and lysine, by high-performance liquid chromatography with pre-chemical derivatization.Bioscience, Biotechnology, and Biochemistry, 75(1):185-187, https://doi.org/10.1271/bbb.100723.
Viant M R, Rosenblum E S, Tjeerdema R S. 2003. NMR-based metabolomics:a powerful approach for characterizing the effects of environmental stressors on organism health.Environmental Science & Technology, 37(21):4 982-4 989, https://doi.org/10.1021/es034281x.
Wang F Y, Yang H S, Gao F, Liu G B. 2008a. Effects of acute temperature or salinity stress on the immune response in sea cucumber, Apostichopus japonicus. Comparative Biochemistry and Physiology Part A:Molecular & Integrative Physiology, 151(4):491-498, https://doi.org/10.1016/j.cbpa.2008.06.024.
Wang X J, Sun W J, Sun H, Lv H T, Wu Z M, Wang P, Liu L, Cao H X. 2008b. Analysis of the constituents in the rat plasma after oral administration of Yin Chen Hao Tang by UPLC/Q-TOF-MS/MS. Journal of Pharmaceutical and Biomedical Analysis, 46(3):477-490, https://doi.org/10.1016/j.jpba.2007.11.014.
Wang Y F, Yang J, Hu Y X, Zhang H B, Ding J, Wang L, Qiu X M. 2020. Effects of Salinities on Immune-related Indicators of Sea Cucumber (Apostichopus japonicus).Journal of Guangdong Ocean University, 40(3):22-29, https://doi.org/10.3969/j.issn.1673-9159.2020.03.004. (in Chinese with English abstract)
Wang Y H, Xiu Y J, Bi K R, Ou J T, Gu W, Wang W, Meng Q G. 2017. Integrated analysis of MRNA-seq in the haemocytes of Eriocheir sinensis in response to Spiroplasma eriocheiris infection. Fish & Shellfish Immunology, 68:289-298, https://doi.org/10.1016/j.fsi.2017.07.036.
Wiklund P, Bergman J. 2006. The chemistry of anthranilic acid. Current Organic Synthesis, 3(3):379-402, https://doi.org/10.2174/157017906777934926.
Wikoff W R, Anfora A T, Liu J, Schultz P G, Lesley S A, Peters E C, Siuzdak G. 2009. Metabolomics analysis reveals large effects of gut microflora on mammalian blood metabolites. Proceedings of the National Academy of Sciences of the United States of America, 106(10):3 698-3 703, https://doi.org/10.1073/pnas.0812874106.
Win S, Than T A, Le B H A, Garcia-Ruiz C, Fernandez-Checa J C, Kaplowitz N. 2015. Sab (Sh3bp5) dependence of jnk mediated inhibition of mitochondrial respiration in palmitic acid induced hepatocyte lipotoxicity. Journal of Hepatology, 62(6):1 367-1 374, https://doi.org/10.1016/j.jhep.2015.01.032.
Xie Y L, Liu L H, Huang X C, Guo Y W, Lou L G. 2005.Scalaradial inhibition of epidermal growth factor receptormediated Akt phosphorylation is independent of secretory phospholipase A2. The Journal of Pharmacology and Experimental Therapeutics, 314(3):1 210-1 217, https://doi.org/10.1124/jpet.105.086520.
Xu D X, Zhou S, Yang H S. 2017. Carbohydrate and amino acids metabolic response to heat stress in the intestine of the sea cucumber Apostichopus japonicus. Aquaculture Research, 48(12):5 883-5 891, https://doi.org/10.1111/are.13411.
Yan N, Du Y M, Liu X M, Chu M J, Shi J, Zhang H B, Liu Y H, Zhang Z F. 2019. A comparative UHPLC-QqQ-MSbased metabolomics approach for evaluating Chinese and North American wild rice. Food Chemistry, 275:618-627, https://doi.org/10.1016/j.foodchem.2018.09.153.
Yang A F, Zhou Z C, Pan Y J, Jiang J W, Dong Y, Guan X Y, Sun H J, Gao S, Chen Z. 2016. RNA sequencing analysis to capture the transcriptome landscape during skin ulceration syndrome progression in sea cucumber Apostichopus japonicus. BMC Genomics, 17:459, https://doi.org/10.1186/s12864-016-2810-3.
Yin P Y, Zhao X J, Li Q R, Wang J S, Li J S, Xu G W. 2006.Metabonomics study of intestinal fistulas based on ultraperformance liquid chromatography coupled with Q-TOF mass spectrometry (UPLC/Q-TOF MS). Journal of Proteome Research, 5(9):2 135-2 143, https://doi.org/10.1021/pr060256p.
Yu Z H, Zhou Y, Yang H S, Hu C Q. 2014. Bottom culture of the sea cucumber Apostichopus japonicus Selenka(Echinodermata:Holothuroidea) in a fish farm, southern China. Aquaculture Research, 45(9):1 434-1 441, https://doi.org/10.1111/are.12089.
Zhang C Y, Wang Y G, Rong X J. 2006. Isolation and identification of causative pathogen for skin ulcerative syndrome in Apostichopus japonicus. Journal of Fisheries of China, 30(1):118-123, https://doi.org/10.3321/j.issn:1000-0615.2006.01.019. (in Chinese with English abstract)
Zhang P J, Li C H, Zhu L, Su X R, Li Y, Jin C H, Li T W. 2013.De novo assembly of the sea cucumber Apostichopus japonicus hemocytes transcriptome to identify miRNA targets associated with skin ulceration syndrome. PLoS One, 8(9):e73506, https://doi.org/10.1371/journal.pone.0073506.
Zhang X L, Cui L F, Li S M. 2019. China Fishery Statistical Yearbook (2019). China Agriculture Press, Beijing, China. p.23. (in Chinese)
Zhao G H, Hou X L, Li X Y, Qu M, Tong C Q, Li W. 2017.Metabolomics analysis of alloxan-induced diabetes in mice using UPLC-Q-TOF-MS after Crassostrea gigas polysaccharide treatment. International Journal of Biological Macromolecules, 108:550-557, https://doi.org/10.1016/j.ijbiomac.2017.12.057.
Zhou J, He W Y, Wang W N, Yang C W, Wang L, Xin Y, Wu J, Cai D X, Liu Y, Wang A L. 2009. Molecular cloning and characterization of an ATP-binding cassette (ABC) transmembrane transporter from the white shrimp Litopenaeus vannamei. Comparative Biochemistry and Physiology Part C:Toxicology & Pharmacology, 150(4):450-458, https://doi.org/10.1016/j.cbpc.2009.06.012.
Zhou L, Li H F, Qin J G, Wang X D, Chen L Q, Xu C, Li E C. 2020. Dietary prebiotic inulin benefits on growth performance, antioxidant capacity, immune response and intestinal microbiota in Pacific white shrimp (Litopenaeus vannamei) at low salinity. Aquaculture, 518:734847, https://doi.org/10.1016/j.aquaculture.2019.734847.
Copyright © Haiyang Xuebao