TORC1 Regulates Thermotolerance Via Modulating Metabolic Rate and Antioxidant Capacity in Scallop

Overview

Journal Antioxidants (Basel)

Date 2024 Nov 27

PMID 39594501

Authors

Longfei Chu

Ancheng Liu

Jiaxi Chang

Junhao Zhang

Xiujiang Hou

Xinghai Zhu

Qiang Xing

Zhenmin Bao

Affiliations

Soon will be listed here.

Abstract

Target of rapamycin complex 1 (TORC1) is a key regulator of metabolism in eukaryotes across multiple pathways. Although TORC1 has been extensively studied in vertebrates and some invertebrates, research on this complex in scallops is limited. In this study, we identified the genes encoding TORC1 complex subunits in the scallop through genome-wide in silico scanning. Five genes, including , , , , and , that encode the subunits of TORC1 complex were identified in the bay scallop. We then conducted structural characterization and phylogenetic analysis of the TORC1 (AiTORC1) subunits to determine their structural features and evolutionary relationships. Next, we analyzed the spatiotemporal expressions of AiTORC1-coding genes during various embryo/larvae developmental stages and across different tissues in healthy adult scallops. The results revealed stage- and tissue-specific expression patterns, suggesting diverse roles in development and growth. Furthermore, the regulation of AiTORC1-coding genes was examined in temperature-sensitive tissues (the mantle, gill, hemocyte, and heart) of bay scallops exposed to high-temperature (32 °C) stress over different durations (0 h, 6 h, 12 h, 24 h, 3 d, 6 d, and 10 d). The expression of AiTORC1-coding genes was predominantly suppressed in the hemocyte but was generally activated in the mantle, gill, and heart, indicating a tissue-specific response to heat stress. Finally, functional validation was performed using the TOR inhibitor rapamycin to suppress AiTORC1, leading to an enhanced catabolism, a decreased antioxidant capacity, and a significant reduction in thermotolerance in bay scallops. Collectively, this study elucidates the presence, structural features, evolutional relationships, expression profiles, and roles in antioxidant capacity and metabolism regulation of AiTORC1 in the bay scallop, providing a preliminary understanding of its versatile functions in response to high-temperature challenges in marine mollusks.

References

Grimmelpont M, Payton L, Lefrancois C, Tran D . Molecular and behavioural responses of the mussel Mytilus edulis exposed to a marine heatwave. Mar Environ Res. 2024; 196:106418. DOI: 10.1016/j.marenvres.2024.106418. View

Powers 3rd R, Kaeberlein M, Caldwell S, Kennedy B, Fields S . Extension of chronological life span in yeast by decreased TOR pathway signaling. Genes Dev. 2006; 20(2):174-84. PMC: 1356109. DOI: 10.1101/gad.1381406. View

Dennis P, Fumagalli S, Thomas G . Target of rapamycin (TOR): balancing the opposing forces of protein synthesis and degradation. Curr Opin Genet Dev. 1999; 9(1):49-54. DOI: 10.1016/s0959-437x(99)80007-0. View

Schneider E, Zuckerman Z, Talwar B, Cooke S, Shultz A, Suski C . Aerobic response to thermal stress across ontogeny and habitats in a teleost fish. J Fish Biol. 2023; 103(2):336-346. DOI: 10.1111/jfb.15448. View

Rabanal-Ruiz Y, Otten E, Korolchuk V . mTORC1 as the main gateway to autophagy. Essays Biochem. 2017; 61(6):565-584. PMC: 5869864. DOI: 10.1042/EBC20170027. View

Kapahi P, Zid B, Harper T, Koslover D, Sapin V, Benzer S . Regulation of lifespan in Drosophila by modulation of genes in the TOR signaling pathway. Curr Biol. 2004; 14(10):885-90. PMC: 2754830. DOI: 10.1016/j.cub.2004.03.059. View

Yang H, Rudge D, Koos J, Vaidialingam B, Yang H, Pavletich N . mTOR kinase structure, mechanism and regulation. Nature. 2013; 497(7448):217-23. PMC: 4512754. DOI: 10.1038/nature12122. View

Rodriguez Camargo D, Link N, Dames S . The FKBP-rapamycin binding domain of human TOR undergoes strong conformational changes in the presence of membrane mimetics with and without the regulator phosphatidic acid. Biochemistry. 2012; 51(24):4909-21. DOI: 10.1021/bi3002133. View

Tjernberg A, Markova N, Griffiths W, Hallen D . DMSO-related effects in protein characterization. J Biomol Screen. 2006; 11(2):131-7. DOI: 10.1177/1087057105284218. View

10.

Sharma M, Banday Z, Shukla B, Laxmi A . Glucose-Regulated Acts as a Key Molecule in Governing Thermomemory. Plant Physiol. 2019; 180(2):1081-1100. PMC: 6548265. DOI: 10.1104/pp.18.01371. View

11.

Chen W, Wang X, Yang S . Response of phytoplankton community structure to environmental changes in the coastal areas of northern China. Mar Pollut Bull. 2023; 195:115300. DOI: 10.1016/j.marpolbul.2023.115300. View

12.

Frederich M, Portner H . Oxygen limitation of thermal tolerance defined by cardiac and ventilatory performance in spider crab, Maja squinado. Am J Physiol Regul Integr Comp Physiol. 2000; 279(5):R1531-8. DOI: 10.1152/ajpregu.2000.279.5.R1531. View

13.

Kamenev Y, Eliseikina M, Maslennikov S, Dolmatov I . The ultrastructural features of embryonic and early larval development in Yesso scallop, Mizuhopecten yessoensis. Tissue Cell. 2018; 53:76-86. DOI: 10.1016/j.tice.2018.06.002. View

14.

Ginalski K, Zhang H, Grishin N . Raptor protein contains a caspase-like domain. Trends Biochem Sci. 2004; 29(10):522-4. DOI: 10.1016/j.tibs.2004.08.006. View

15.

Cheng L, Abraham J, Hausfather Z, Trenberth K . How fast are the oceans warming?. Science. 2019; 363(6423):128-129. DOI: 10.1126/science.aav7619. View

16.

Viladrich N, Linares C, Padilla-Gamino J . Lethal and sublethal effects of thermal stress on octocorals early life-history stages. Glob Chang Biol. 2022; 28(23):7049-7062. PMC: 9828436. DOI: 10.1111/gcb.16433. View

17.

Schieke S, Phillips D, McCoy Jr J, Aponte A, Shen R, Balaban R . The mammalian target of rapamycin (mTOR) pathway regulates mitochondrial oxygen consumption and oxidative capacity. J Biol Chem. 2006; 281(37):27643-52. DOI: 10.1074/jbc.M603536200. View

18.

Chen X, Lu C, Ye Y . Effects of Cd and Zn on oxygen consumption and ammonia excretion in sipuncula (Phascolosoma esculenta). Ecotoxicol Environ Saf. 2008; 72(2):507-15. DOI: 10.1016/j.ecoenv.2007.11.019. View

19.

Rubiolo J, Lozano-Leon A, Rodriguez-Souto R, Fol Rodriguez N, Vieytes M, Botana L . The impact of depuration on mussel hepatopancreas bacteriome composition and predicted metagenome. Antonie Van Leeuwenhoek. 2018; 111(7):1117-1129. DOI: 10.1007/s10482-018-1015-y. View

20.

Yina S, Zhongjie C, Kaiyu C, Chenghua L, Xiaodong Z . Target of rapamycin signaling inhibits autophagy in sea cucumber Apostichopus japonicus. Fish Shellfish Immunol. 2020; 102:480-488. DOI: 10.1016/j.fsi.2020.05.013. View