Analysis of differentially expressed genes in the sea cucumber <i>Apostichopus japonicus</i> under heat stress

Dongxue Xu; Jingjing Zhang; Wenqi Song; Lina Sun; Ji Liu; Yuanxue Gu; Yanru Chen; Bin Xia

doi:10.1007/s13131-023-2196-4

Volume 42 Issue 11

Nov. 2023

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Article Navigation > Acta Oceanologica Sinica > 2023 > 42(11): 117-126

Dongxue Xu, Jingjing Zhang, Wenqi Song, Lina Sun, Ji Liu, Yuanxue Gu, Yanru Chen, Bin Xia. Analysis of differentially expressed genes in the sea cucumber Apostichopus japonicus under heat stress[J]. Acta Oceanologica Sinica, 2023, 42(11): 117-126. doi: 10.1007/s13131-023-2196-4

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Dongxue Xu, Jingjing Zhang, Wenqi Song, Lina Sun, Ji Liu, Yuanxue Gu, Yanru Chen, Bin Xia. Analysis of differentially expressed genes in the sea cucumber Apostichopus japonicus under heat stress[J]. Acta Oceanologica Sinica, 2023, 42(11): 117-126. doi: 10.1007/s13131-023-2196-4

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Analysis of differentially expressed genes in the sea cucumber Apostichopus japonicus under heat stress

doi: 10.1007/s13131-023-2196-4

1.
School of Marine Science and Engineering, Qingdao Agricultural University, Qingdao 266109, China
2.
Key Laboratory of Mariculture of Ministry of Education, Ocean University of China, Qingdao 266003, China
3.
CAS Key Laboratory of Marine Ecology and Environmental Sciences, Institute of Oceanology, Chinese Academy of Sciences, Qingdao 266071, China

Funds: The National Natural Science Foundation of China under contract Nos 42276143 and 31902360; the Shandong Provincial Natural Science Foundation under contract Nos ZR2022MC050 and ZR2022QD003; the “First Class Fishery Discipline” Programme [(2020)3] in Shandong Province.

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Corresponding author: E-mail: ac_xbin@126.com
Received Date: 2022-11-02
Accepted Date: 2023-05-27

Available Online: 2024-01-13

Publish Date: 2023-11-01

Abstract

Abstract

The sea cucumber Apostichopus japonicus plays important roles in marine benthic ecosystem as environmental cleaners, and it is the important aquaculture species in China. High water temperature poses critical threat for the survival of A. japonicus, which has resulted in extensive death in summer. To explore the genes expression profiles under different levels of heat stress, the high-throughput RNA-seq was applied in this study. Our results revealed a total of 1371, 1225 and 1408 differentially expressed genes (DEGs) in 26℃ for 6 h, 26℃ for 48 h and 30℃ for 6 h respectively in comparison with Control group. The pathway analysis suggested “Protein processing in endoplasmic reticulum (ER)” was significantly enriched in all these heat stress (HS) treatment groups. The expression results of key DEGs in this pathway (Hsp70, Derlin, NEF, PDI, GPR94 and ERP57) by qRT-PCR was in accordance with the RNA-seq data. The subcluster analysis of DEGs revealed that a variety of heat shock proteins (HSPs) and calcium ion binding proteins had an obvious up-regulated expression in 26℃ for 6 h, comparatively low expression in 26℃ for 48 h, and the highest expression in 30℃ for 6 h. The other DEGs subcluster, consisting of critical components of extracellular matrix (ECM) and a subset of peptidases and proteases, showed significantly rising tendency in 30℃ for 6 h. Additionally, the expression of matrix metalloproteases (MMP1, MMP16 and MMP19) was prominently affected by HS, and peaked in 30℃ for 6 h. This study provides a series of candidate genes for further study about heat shock response in A. japonicus, especially genes associated with protein processing in ER and regulation of ECM, which also offers new insights into cellular homeostasis under stressful conditions in marine invertebrates.
- Apostichopus japonicus,
- heat stress,
- RNA-seq,
- protein processing,
- extracellular matrix

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References(58)

References

Ackerman P A, Forsyth R B, Mazur C F, et al. 2000. Stress hormones and the cellular stress response in salmonids. Fish Physiology and Biochemistry, 23(4): 327–336. doi: 10.1023/A:1011107610971

An Zhenhua, Dong Yunwei, Dong Shuanglin. 2007. Temperature effects on growth-ration relationships of juvenile sea cucumber Apostichopus japonicus (Selenka). Aquaculture, 272(1–4): 644–648. doi: 10.1016/j.aquaculture.2007.08.038

Atiakshin D, Kostin A, Trotsenko I, et al. 2022. Carboxypeptidase A3—a key component of the protease phenotype of mast cells. Cells, 11(3): 570. doi: 10.3390/cells11030570

Benjamini Y, Hochberg Y. 1995. Controlling the false discovery rate: a practical and powerful approach to multiple testing. Journal of the Royal Statistical Society: Series B (Methodological), 57(1): 289–300. doi: 10.1111/j.2517-6161.1995.tb02031.x

Bertolotti A, Zhang Yuhong, Hendershot L M, et al. 2000. Dynamic interaction of BiP and ER stress transducers in the unfolded-protein response. Nature Cell Biology, 2(6): 326–332. doi: 10.1038/35014014

Byrne M. 2010. Impact of climate change stressors on marine invertebrate life histories with a focus on the Mollusca and Echinodermata. In: Yu Juzhu, Henderson-Sellers A, eds. Climate Alert: Climate Change Monitoring and Strategy. Sydney: Sydney University Press, 169–212

Callwood J, Melmaiee K, Kulkarni K P, et al. 2021. Differential morpho-physiological and transcriptomic responses to heat stress in two blueberry species. International Journal of Molecular Sciences, 22(5): 2481. doi: 10.3390/ijms22052481

Das S, Mandal M, Chakraborti T, et al. 2003. Structure and evolutionary aspects of matrix metalloproteinases: a brief overview. Molecular and Cellular Biochemistry, 253(1–2): 31–40

Ding Haidong, Mo Shuangrong, Qian Ying, et al. 2020. Integrated proteome and transcriptome analyses revealed key factors involved in tomato ( Solanum lycopersicum) under high temperature stress. Food and Energy Security, 9(4): e239. doi: 10.1002/fes3.239

Dong Yunwei, Dong Shuanglin. 2008. Induced thermotolerance and expression of heat shock protein 70 in sea cucumber Apostichopus japonicus. Fisheries Science, 74(3): 573–578. doi: 10.1111/j.1444-2906.2008.01560.x

El Golli-Bennour E, Bacha H. 2011. Hsp70 expression as biomarkers of oxidative stress: mycotoxins’ exploration. Toxicology, 287(1–3): 1–7. doi: 10.1016/j.tox.2011.06.002

Feige M J, Hendershot L M. 2011. Disulfide bonds in ER protein folding and homeostasis. Current Opinion in Cell Biology, 23(2): 167–175. doi: 10.1016/j.ceb.2010.10.012

Han Qingxi, Keesing J K, Liu Dongyan. 2016. A review of sea cucumber aquaculture, ranching, and stock enhancement in China. Reviews in Fisheries Science & Aquaculture, 24(4): 326–341

Han Lingshu, Sun Yi, Cao Yue, et al. 2021. Analysis of the gene transcription patterns and DNA methylation characteristics of triploid sea cucumbers ( Apostichopus japonicus). Scientific Reports, 11(1): 7564. doi: 10.1038/s41598-021-87278-9

Hendershot L M. 2004. The ER function BiP is a master regulator of ER function. Mount Sinai Journal of Medicine, 71(5): 289–297

Huang Jinqiang, Li Yongjuan, Liu Zhe, et al. 2018. Transcriptomic responses to heat stress in rainbow trout Oncorhynchus mykiss head kidney. Fish & Shellfish Immunology, 82: 32–40

Huo Da, Liu Shilin, Yang Hongsheng. 2017. Analysis of causes and corresponding strategies for summer massive mortalities of sea cucumber. Studia Marina Sinica (in Chinese), (52): 47–58

Karouna-Renier N K, Zehr J P. 1999. Ecological implications of molecular biomarkers: assaying sub-lethal stress in the midge Chironomus tentans using heat shock protein 70 (HSP-70) expression. Hydrobiologia, 401: 255–264. doi: 10.1023/A:1003730225536

Lamare M, Burritt D, Lister K. 2011. Ultraviolet radiation and echinoderms: past, present and future perspectives. Advances in Marine Biology, 59: 145–187

Lewis S, Handy R D, Cordi B, et al. 1999. Stress proteins (HSP’s): methods of detection and their use as an environmental biomarker. Ecotoxicology, 8(5): 351–368. doi: 10.1023/A:1008982421299

Li Chao, Fang Huahua, Xu Dongxue. 2019. Effect of seasonal high temperature on the immune response in Apostichopus japonicus by transcriptome analysis. Fish & Shellfish Immunology, 92: 765–771

Li J, Ni Min, Lee B, et al. 2008. The unfolded protein response regulator GRP78/BiP is required for endoplasmic reticulum integrity and stress-induced autophagy in mammalian cells. Cell Death & Differentiation, 15(9): 1460–1471

Linxweiler M, Schick B, Zimmermann R. 2017. Let’s talk about Secs: Sec61, Sec62 and Sec63 in signal transduction, oncology and personalized medicine. Signal Transduction and Targeted Therapy, 2: 17002. doi: 10.1038/sigtrans.2017.2

Liu Ziqiang, Liu Yuxin, Zhou Dayong, et al. 2019. The role of matrix metalloprotease (MMP) to the autolysis of sea cucumber ( Stichopus japonicus). Journal of the Science of Food and Agriculture, 99(13): 5752–5759. doi: 10.1002/jsfa.9843

Liu Ji, Xu Dongxue, Chen Yanru, et al. 2022. Adverse effects of dietary virgin (nano) microplastics on growth performance, immune response, and resistance to ammonia stress and pathogen challenge in juvenile sea cucumber Apostichopus japonicus (Selenka). Journal of Hazardous Materials, 423: 127038. doi: 10.1016/j.jhazmat.2021.127038

Liu Yixin, Zhou Dayong, Liu Ziqiang, et al. 2018. Structural and biochemical changes in dermis of sea cucumber ( Stichopus japonicus) during autolysis in response to cutting the body wall. Food Chemistry, 240: 1254–1261. doi: 10.1016/j.foodchem.2017.08.071

Liu Yuxin, Zhou Dayong, Ma Dongdong, et al. 2016. Changes in collagenous tissue microstructures and distributions of cathepsin L in body wall of autolytic sea cucumber ( Stichopus japonicus). Food Chemistry, 212: 341–348. doi: 10.1016/j.foodchem.2016.05.173

Lv Zhimeng, Han Guanghui, Li Chenghua. 2022. Tissue inhibitor of metalloproteinases 1 is involved in ROS-mediated inflammation via regulating matrix metalloproteinase 1 expression in the sea cucumber Apostichopus japonicus. Developmental & Comparative Immunology, 127: 104298

Lyons P J, Callaway M B, Fricker L D. 2008. Characterization of carboxypeptidase A6, an extracellular matrix peptidase. Journal of Biological Chemistry, 283(11): 7054–7063. doi: 10.1074/jbc.M707680200

Miao Ting, Wan Zixuan, Sun Lina, et al. 2017. Extracellular matrix remodeling and matrix metalloproteinases (ajMMP-2 like and ajMMP-16 like) characterization during intestine regeneration of sea cucumber Apostichopus japonicus. Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology, 212: 12–23. doi: 10.1016/j.cbpb.2017.06.011

Mohanty B P, Mahanty A, Mitra T, et al. 2018. Heat shock proteins in stress in teleosts. In: Asea A A A, Kaur P, eds. Regulation of Heat Shock Protein Responses. Chambndge: Springer, 71–94

Moreira-de-Sousa C, de Souza R B, Fontanetti C S. 2018. HSP70 as a biomarker: an excellent tool in environmental contamination analysis—a review. Water, Air, & Soil Pollution, 229(8): 264

Mouw J K, Ou Guanqing, Weaver V M. 2014. Extracellular matrix assembly: a multiscale deconstruction. Nature Reviews Molecular Cell Biology, 15(12): 771–785

Mukundan M K, Antony P D, Nair M R. 1986. A review on autolysis in fish. Fisheries Research, 4(3–4): 259–269. doi: 10.1016/0165-7836(86)90007-X

Nguyen K D T, Morley S A, Lai C H, et al. 2011. Upper temperature limits of tropical marine ectotherms: global warming implications. PLoS One, 6(12): e29340. doi: 10.1371/journal.pone.0029340

Novikova E G, Reznik S E, Varlamov O, et al. 2000. Carboxypeptidase Z is present in the regulated secretory pathway and extracellular matrix in cultured cells and in human tissues. Journal of Biological Chemistry, 275(7): 4865–4870. doi: 10.1074/jbc.275.7.4865

Oh G W, Ko S C, Lee D H, et al. 2017. Biological activities and biomedical potential of sea cucumber ( Stichopus japonicus): a review. Fisheries and Aquatic Sciences, 20(1): 28. doi: 10.1186/s41240-017-0071-y

Pinsino A, Matranga V. 2015. Sea urchin immune cells as sentinels of environmental stress. Developmental & Comparative Immunology, 49(1): 198–205

Randall D J, Tsui T K N. 2002. Ammonia toxicity in fish. Marine Pollution Bulletin, 45(1–12): 17–23. doi: 10.1016/S0025-326X(02)00227-8

Ru Xiaoshang, Zhang Libin, Li Xiaoni, et al. 2019. Development strategies for the sea cucumber industry in China. Journal of Oceanology and Limnology, 37(1): 300–312. doi: 10.1007/s00343-019-7344-5

Ruggiano A, Foresti O, Carvalho P. 2014. ER-associated degradation: protein quality control and beyond. Journal of Cell Biology, 204(6): 869–879. doi: 10.1083/jcb.201312042

Slater M, Chen Jiaxin. 2015. Sea cucumber biology and ecology. In: Brown N P, Eddy S D, eds. Echinoderm Aquaculture. New Jersey: Wiley-Blackwell, 47–55

Song Shuang, Wu Sufeng, Ai Chunqing, et al. 2018. Compositional analysis of sulfated polysaccharides from sea cucumber ( Stichopus japonicus) released by autolysis reaction. International Journal of Biological Macromolecules, 114: 420–425. doi: 10.1016/j.ijbiomac.2018.03.137

Sowmya R, Rathinaraj K, Sachindra N M. 2011. An autolytic process for recovery of antioxidant activity rich carotenoprotein from shrimp heads. Marine Biotechnology, 13(5): 918–927. doi: 10.1007/s10126-010-9353-4

Wang Yunfeng, Li Caijuan, Pan Chenglong, et al. 2019. Alterations to transcriptomic profile, histopathology, and oxidative stress in liver of pikeperch ( Sander lucioperca) under heat stress. Fish & Shellfish Immunology, 95: 659–669

Wang Wenlei, Lin Yinghui, Teng Fei, et al. 2018a. Comparative transcriptome analysis between heat-tolerant and sensitive Pyropia haitanensis strains in response to high temperature stress. Algal Research, 29: 104–112. doi: 10.1016/j.algal.2017.11.026

Wang Lingling, Song Xiaorui, Song Linsheng. 2018b. The oyster immunity. Developmental & Comparative Immunology, 80: 99–118

Wang Fangyu, Yang Hongsheng, Gao Fei, et al. 2008. 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

Wilkinson D J, Desilets A, Lin Hua, et al. 2017. The serine proteinase hepsin is an activator of pro-matrix metalloproteinases: molecular mechanisms and implications for extracellular matrix turnover. Scientific Reports, 7(1): 16693. doi: 10.1038/s41598-017-17028-3

Xia Sudong, Zhao Peng, Chen Kang, et al. 2012. Feeding preferences of the sea cucumber Apostichopus japonicus (Selenka) on various seaweed diets. Aquaculture, 344–349: 205–209

Xu Dongxue, Su Lin, Zhao Peng. 2015. Apostichopus japonicus in the worldwide production and trade of sea cucumbers. Developments in Aquaculture and Fisheries Science, 39: 383–398

Xu Dongxue, Sun Lina, Liu Shilin, et al. 2014. Molecular cloning of heat shock protein 10 (Hsp10) and 60 (Hsp60) cDNAs and their expression analysis under thermal stress in the sea cucumber Apostichopus japonicus. Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology, 171: 49–57. doi: 10.1016/j.cbpb.2014.03.009

Xu Dongxue, Sun Lina, Liu Shilin, et al. 2016. Understanding the heat shock response in the sea cucumber Apostichopus japonicus, using iTRAQ-based proteomics. International Journal of Molecular Sciences, 17(2): 150. doi: 10.3390/ijms17020150

Xu Dongxue, Zhou Shun, Sun Lina. 2018. RNA-seq based transcriptional analysis reveals dynamic genes expression profiles and immune-associated regulation under heat stress in Apostichopus japonicus. Fish & Shellfish Immunology, 78: 169–176

Yan Longjie, Sun Lechang, Cao Kaiyuan, et al. 2021. Type I collagen from sea cucumber ( Stichopus japonicus) and the role of matrix metalloproteinase-2 in autolysis. Food Bioscience, 41: 100959. doi: 10.1016/j.fbio.2021.100959

Zattas D, Adle D J, Rubenstein E M, et al. 2013. N-terminal acetylation of the yeast Derlin Der1 is essential for Hrd1 ubiquitin-ligase activity toward luminal ER substrates. Molecular Biology of the Cell, 24(7): 890–900. doi: 10.1091/mbc.e12-11-0838

Zhang Chi, Liang Weikang, Zhang Weiwei, et al. 2016. Characterization of a metalloprotease involved in Vibrio splendidus infection in the sea cucumber, Apostichopus japonicus. Microbial Pathogenesis, 101: 96–103. doi: 10.1016/j.micpath.2016.11.005

Zhu Xinghai, Ni Ping, Sturrock M, et al. 2022. Fine-mapping and association analysis of candidate genes for papilla number in sea cucumber, Apostichopus japonicus. Marine Life Science & Technology, 4(3): 343–355

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