转录组和代谢组学联合分析小管福寿螺温度胁迫响应机制
作者:
作者单位:

1.南京师范大学生命科学学院 南京 210023;2.南京林业大学生命科学学院 南京 210037

作者简介:

储海燕,女,硕士研究生;研究方向:分子生态学;E-mail:chuhaiyan0222@163.com。

基金项目:

国家自然科学基金项目(No. 32170434),2024年江苏省研究生科研与实践创新计划项目(No. SJCX24_0633);


Integrated Transcriptomic and Metabolomic Responses in the Hepatopancreas of an Invasive Apple Snail Under Temperature Stress
Author:
Affiliation:

1.College of Life Sciences, Nanjing Normal University, Nanjing 210023; 2.College of Life Sciences, Nanjing Forestry University, Nanjing 210037, China

  • 摘要
  • | |
  • 访问统计
  • |
  • 参考文献 [45]
  • |
  • 相似文献 [20]
  • | | |
  • 文章评论
    摘要:

    温度是影响水生生物生长、发育和新陈代谢的重要因素。对环境温度的耐受性是影响小管福寿螺(Pomacea canaliculata)分布和扩散的重要因子。为探究温度胁迫下小管福寿螺的响应调控机制,本研究采用转录组学和代谢组学联合分析小管福寿螺肝胰腺组织在高温(36 ℃)和低温(10 ℃)胁迫48 h后,基因表达情况以及代谢产物的变化。与对照组(25 ℃)相比,高温胁迫下共获得446个差异表达基因和233种差异代谢物;低温胁迫下筛选出288个差异表达基因和119种差异代谢物。高温组差异表达基因和代谢物在氨基酸、脂质运输和免疫系统通路中上调,在脂肪酸代谢和细胞色素P450通路中下调。在低温胁迫下,丙氨酸、天冬氨酸、谷氨酸、富马酸和α-酮戊二酸发生显著变化,可能影响三羧酸循环的能量产生。此外,还有一些基因显著富集在药物代谢和热休克蛋白等相关通路中,以减轻温度胁迫对小管福寿螺生理过程的影响。随机选取6个基因进行荧光定量PCR验证,基因表达趋势与转录组结果一致。综上所述,急性温度胁迫会引起小管福寿螺肝胰腺的免疫应激和能量代谢等过程,小管福寿螺通过调控氨基酸代谢及增加不饱和脂肪酸的含量等使自身快速适应环境温度变化。

    Abstract:

    [Objectives] Temperature is an important factor that affects the growth, development, and metabolism of aquatic organisms. Temperature tolerance significantly affects the survival and expansion of the invasive Apple Snail Pomacea canaliculata. [Methods] Transcriptome sequencing and metabolomic analysis were used to examine the alterations in the hepatopancreas of P. canaliculata exposed to high (36 ℃) and low (10 ℃) temperature stress for 48 h. After cleaning the raw sequencing data, we identified differentially expressed genes by |log2FoldChange| > 1 and P < 0.05. Gene ontology (GO) annotation and pathway enrichment analysis were then performed on the differentially expressed genes. Significantly changed metabolites were identified by variable important in projection > 1, P < 0.05, and |log2FoldChange| > 1.5. Kyoto encyclopedia of genes and genomes (KEGG) was used to search for the metabolic pathways of significantly changed metabolites. The Pearson correlation coefficient was used to analyze the correlation between differentially expressed genes and significantly changed metabolites. [Results] Compared to the control group, the high-temperature group had 446 genes and 233 metabolites with differential expression, while the low-temperature group had 288 genes and 119 metabolites exhibiting differential expression. The majority of genes and metabolites were upregulated in pathways related to amino acids, lipid transport, and immune system processes (Fig. 1), while they were downregulated in lipid acid and cytochrome P450 pathways during high-temperature stress (Fig. 2). Under low-temperature stress, significant changes were observed in alanine, aspartate, glutamate, fumaric acid, and alpha-ketoglutaric acid (Figs. 3, 4), which are involved in the energy production of the TCA cycle. Furthermore, several genes enriched in the drug metabolism pathway and heat shock proteins were found to mitigate the effects on their physiological processes. Finally, the expression patterns of these differentially expressed genes in the quantitative real-time PCR analyses were similar to those obtained by RNA-seq, indicating the accuracy and reliability of the RNA-Seq results (Fig. 6). [Conclusion] Acute temperature stress can induce immune stress and energy metabolism processes in the hepatopancreas of P. canaliculata. P. canaliculata rapidly adapts to environmental temperature changes by regulating amino acid metabolism and increasing the content of unsaturated fatty acids.

    参考文献
    Akram M. 2014. Citric acid cycle and role of its intermediates in metabolism. Cell Biochemistry and Biophysics, 68(3):475–478.
    Ansart A, Vernon P. 2003. Cold hardiness in molluscs. Acta Oecologica, 24(2):95–102.
    Cadierno M P, Dreon M S, Heras H. 2018. Validation by qPCR of reference genes for reproductive studies in the invasive apple Snail Pomacea canaliculata. Malacologia, 62(1):163–170.
    Casares D, Escribá P V, Rosselló C A. 2019. Membrane lipid composition:effect on membrane and organelle structure, function and compartmentalization and therapeutic avenues. International Journal of Molecular Sciences, 20(9):2167.
    Chen Y, Wu X, Lai J, et al. 2023. Integrated biochemical, transcriptomic and metabolomic analyses provide insight into heat stress response in Yangtze Sturgeon (Acipenser dabryanus). Ecotoxicology and Environmental Safety, 249:114366.
    Chin R M, Fu X, Pai M Y, et al. 2014. The metabolite α-ketoglutarate extends lifespan by inhibiting ATP synthase and TOR. Nature, 510(7505):397–401.
    Cowie R H, Hayes K A, Thiengo S C. 2006. What are apple snails confused taxonomy and some preliminary resolution // Joshi R C, Sebastian L S. Global Advances in Ecology and Management of Golden Apple Snails. Nueva Ecija:Philippine Rice Research Institute, 3–23.
    Harayama T, Riezman H. 2018. Understanding the diversity of membrane lipid composition. Nature Reviews Molecular Cell Biology, 19(5):281–296.
    Hayes K A, Burks R L, Castro-Vazquez A, et al. 2015. Insights from an integrated view of the biology of apple snails (Caenogastropoda:Ampullariidae). Malacologia, 58(1/2):245–302.
    Hayward S A L, Manso B, Cossins A R. 2014. Molecular basis of chill resistance adaptations in poikilothermic animals. Journal of Experimental Biology, 217(1):6–15.
    Ito K. 2002. Environmental factors influencing overwintering success of the golden apple snail, Pomacea canaliculata (Gastropoda:Ampullariidae), in the northernmost population of Japan. Applied Entomology and Zoology, 37(4):655–661.
    Jacob P, Hirt H, Bendahmane A. 2017. The heat-shock protein/chaperone network and multiple stress resistance. Plant Biotechnology Journal, 15(4):405–414.
    Jahan K, Nie H, Yin Z, et al. 2022. Comparative transcriptome analysis to reveal the genes and pathways associated with adaptation strategies in two different populations of Manila clam (Ruditapes philippinarum) under acute temperature challenge. Aquaculture, 552:737999.
    Kwong K L, Dudgeon D, Wong P K, et al. 2010. Secondary production and diet of an invasive snail in freshwater wetlands:implications for resource utilization and competition. Biological Invasions, 12(5):1153–1164.
    Lei J, Chen L, Li H. 2017. Using ensemble forecasting to examine how climate change promotes worldwide invasion of the golden apple snail (Pomacea canaliculata). Environmental Monitoring and Assessment, 189(8):404.
    Leiva F P, Calosi P, Verberk W C E P. 2019. Scaling of thermal tolerance with body mass and genome size in ectotherms:a comparison between water- and air-breathers. Philosophical Transactions of the Royal Society B, Biological Sciences, 374(1778):20190035.
    Liu G F, Yang Q Q, Lin H F, et al. 2018. Differential gene expression in Pomacea canaliculata (Mollusca:Gastropoda) under low temperature condition. Journal of Molluscan Studies, 84(4):397–403.
    Liu J, Sun Z, Wang Z, et al. 2020. A comparative transcriptomics approach to analyzing the differences in cold resistance in Pomacea canaliculata between Guangdong and Hunan. Journal of Immunology Research, 2020:8025140.
    Lowe S, Browne M, Boudjelas S, et al. 2000. 100 of the world’s worst invasive alien species:A selection from the global invasive species database. The Invasive Species Specialist Group (ISSG) a specialist group of the Species Survival Commission (SSC) of the World Conservation Union (IUCN), 12.
    Lulijwa R, Alfaro A C, Young T. 2022. Metabolomics in salmonid aquaculture research:applications and future perspectives. Reviews in Aquaculture, 14(2):547–577.
    Matsukura K, Izumi Y, Yoshida K, et al. 2016. Cold tolerance of invasive freshwater snails, Pomacea canaliculata, P. maculata, and their hybrids helps explain their different distributions. Freshwater Biology, 61(1):80–87.
    Matsukura K, Tsumuki H, Izumi Y, et al. 2009. Temperature and water availability affect decrease of cold hardiness in the apple snail, Pomacea canaliculata. Malacologia, 51(2):263–269.
    Meng X, Dong L, Shi X, et al. 2019. Screening of the candidate genes related to low-temperature tolerance of Fenneropenaeus chinensis based on high-throughput transcriptome sequencing. PLoS One, 14(4):e0211182.
    Mu Y N, Li W R, Wu B, et al. 2020. Transcriptome analysis reveals new insights into immune response to hypoxia challenge of large yellow croaker (Larimichthys crocea). Fish & Shellfish Immunology, 98:738–747.
    Ning M, Wei P, Shen H, et al. 2019. Proteomic and metabolomic responses in hepatopancreas of whiteleg shrimp Litopenaeus vannamei infected by microsporidian Enterocytozoon hepatopenaei. Fish & Shellfish Immunology, 87:534–545.
    Ren X, Yu Z, Xu Y, et al. 2020. Integrated transcriptomic and metabolomic responses in the hepatopancreas of kuruma shrimp (Marsupenaeus japonicus) under cold stress. Ecotoxicology and Environmental Safety, 206:111360.
    Seuffert M E, Burela S, Martín P R. 2010. Influence of water temperature on the activity of the freshwater snail Pomacea canaliculata (Caenogastropoda:Ampullariidae) at its southernmost limit (southern pampas, Argentina). Journal of Thermal Biology, 35(2):77–84.
    Seuffert M E, Martín P R. 2013. Juvenile growth and survival of the apple snail Pomacea canaliculata (Caenogastropoda:Ampullariidae) reared at different constant temperatures. SpringerPlus, 2(1):312.
    Song H M, Mu X D, Gu D G, et al. 2014. Molecular characteristics of the HSP70 gene and its differential expression in female and male golden apple snails (Pomacea canaliculata) under temperature stimulation. Cell Stress and Chaperones, 19(4):579–589.
    Song J, Liu B, Wang C. 2022. Metabolomic and transcriptomic responses of Argopecten irradians concentricus to thermal stresses. Frontiers in Marine Science, 9:818083.
    Song M, Zhao J, Wen H S, et al. 2019. The impact of acute thermal stress on the metabolome of the black rockfish (Sebastes schlegelii). PLoS One, 14(5):e0217133.
    Soyano K, Mushirobira Y. 2018. The mechanism of low-temperature tolerance in fish. Advances in Experimental Medicine and Biology, 1081:149–164.
    Wang B, Hao X, Xu J, et al. 2020. Cytochrome P450 metabolism mediates low-temperature resistance in pinewood nematode. FEBS Open Bio, 10(6):1171–1179.
    Wang L, Song X, Song L. 2018. The oyster immunity. Developmental & Comparative Immunology, 80:99–118.
    Wu Z, Jin L, Zheng W, et al. 2018. NMR-based serum metabolomics study reveals a innovative diagnostic model for missed abortion. Biochemical and Biophysical Research Communications, 496(2):679–685.
    Xiao Q, Lin Y, Li H, et al. 2022. Transcriptome sequencing reveals the differentially expressed lncRNAs and mRNAs in response to cold acclimation and cold stress in Pomacea canaliculata. BMC Genomics, 23(1):382.
    Xu C, Ma Q, Li E, et al. 2021. Response of lipid molecular structure to dietary lipid type in Chinese mitten crab Eriocheir sinensis:a deep lipidomics analysis. Aquaculture Reports, 19:100596.
    Xu H G, Meng X X, Wei Y L, et al. 2022. Arachidonic acid matters. Reviews in Aquaculture, 14(4):1912–1944.
    Yoshida K, Matsukura K, Cazzaniga N J, et al. 2014. Tolerance to low temperature and desiccation in two invasive apple snails, Pomacea canaliculata and P. maculata (Caenogastropoda:Ampullariidae), collected in their original distribution area (northern and central Argentina). Journal of Molluscan Studies, 80(1):62–66.
    Zanger U M, Schwab M. 2013. Cytochrome P450 enzymes in drug metabolism:regulation of gene expression, enzyme activities, and impact of genetic variation. Pharmacology & Therapeutics, 138(1):103–141.
    Zhao T, Ma A, Yang S, et al. 2021. Integrated metabolome and transcriptome analyses revealing the effects of thermal stress on lipid metabolism in juvenile turbot Scophthalmus maximus. Journal of Thermal Biology, 99:102937.
    Zheng G, Dong S, Hou Y, et al. 2012. Molecular characteristics of HSC70 gene and its expression in the golden apple snails, Pomacea canaliculata (Mollusca:Gastropoda). Aquaculture, 358:41–49.
    Zhu W, Zhang C, Tan K, et al. 2022. Variation of lipids and fatty acids in noble scallop Chlamys nobilis under low temperature stress. Aquaculture, 554:738121.
    董胜张, 白旭, 潘颖瑛, 等. 2010. 温度胁迫对我国不同地理种群福寿螺生长及存活的影响. 湖北农业科学, 49(11):2878–2882.
    王旋成, 朱一帆, 周海琳, 等. 2023. 血清非靶向代谢组学联合靶向胆汁酸代谢组学筛查结直肠癌的潜在生物标志物. 南方医科大学学报, 43(3):443–453.
    引证文献
    网友评论
    网友评论
    分享到微博
    发 布
引用本文

储海燕,杨海韵,常婷婷,沈雯佳,井木子,林友福,宁阔,李宏,陈炼.2025.转录组和代谢组学联合分析小管福寿螺温度胁迫响应机制.动物学杂志,60(1):45-58.

复制
文章指标
  • 点击次数:66
  • 下载次数: 78
  • HTML阅读次数: 0
  • 引用次数: 0
历史
  • 收稿日期:2024-06-03
  • 在线发布日期: 2025-03-04