Collaborative Research: Does ocean acidification induce a methylation response that affects the fitness of the next generation in oysters?

合作研究：海洋酸化是否会引起影响牡蛎下一代健康的甲基化反应？

• 批准号: 1634167
• 负责人: Steven Roberts
• 金额: $ 38.88万
• 依托单位: University of Washington
• 依托单位国家: 美国
• 项目类别: Standard Grant
• 财政年份: 2017
• 资助国家: 美国
• 起止时间: 2017-01-01 至 2021-06-30
• 项目状态: 已结题
• 来源: https://www.nsf.gov/awardsearch/showAward?AWD_ID=1634167&HistoricalAwards=false
• 关键词: Collaborative; Research; Does; ocean; acidification

Marine ecosystems worldwide are threatened by ocean acidification, a process caused by the unprecedented rate at which carbon dioxide is increasing in the atmosphere. Since ocean change is predicted to be rapid, extreme, and widespread, marine species may face an "adapt-or-die" scenario. However, modifications to the DNA sequence may be induced in response to a stress like ocean acidification and then inherited. Such "epigenetic" modifications may hold the key to population viability under global climate change, but they have been understudied. The aim of this research is to characterize the role of DNA methylation, a heritable epigenetic system, in the response of Eastern oysters (Crassostrea virginica) to ocean acidification. The intellectual merit lies in the integrative approach, which will characterize the role of DNA methylation in the intergenerational response of oysters to ocean acidification. These interdisciplinary data, spanning from molecular to organismal levels, will provide insight into mechanisms that underlie the capacity of marine invertebrates to respond to ocean acidification and lay the foundation for future transgenerational studies. Ocean acidification currently threatens marine species worldwide and has already caused significant losses in aquaculture, especially in Crassostrea species. This research has broader impacts for breeding, aquaculture, and the economy. Under the investigators' "Epigenetics to Ocean" (E2O) training program, the investigators will build STEM talent in bioinformatics and biogeochemistry, expose girls in low-income school districts to careers in genomics, and advance the field through open science and reproducibility. This research will specifically test if intermittent exposure to low pH induces a methylation response with downstream beneficial effects for biomineralization. These methylation states could be inherited and confer a fitness advantage to larvae that possess them. Phase 1 of the project will use an exposure experiment to determine the degree to which DNA methylation is altered and regulates the response to OA. Data from this experiment will be used to test the hypotheses that (i) DNA methylation, induced in the tissue of shell formation (i.e., mantle tissue), is correlated with changes in transcription and regulation of pallial fluid pH (calcifying fluid pH, measured by microelectrode), and (ii) that methylation changes induced in the mantle tissue are also induced in the germline --indicating that such changes are potentially heritable. Phase 2 of the project will use a pair-mated cross experiment to test the hypothesis that parental exposure to OA alters larval traits (calcification rate, shell structure, and polymorph mineralogy). Larvae will be generated from parents exposed to OA or control seawater, and then raised under control or OA conditions. Results will be used to (i) characterize inheritance of induced methylation states, (ii) estimate the variance in larval traits explained by genotype, non-genetic maternal/paternal effects, adult OA exposure, larval OA exposure, and parental methylome, and (iii) test the hypothesis that adult exposure alters the heritability (a quantity that predicts evolutionary response) of larval traits. Since the effects of epigenetic phenomena on estimates of heritability are highly debated, the results would advance understanding of this important issue. Because the investigators could discover that DNA methylation is a mechanism for heritable plastic responses to OA, knowledge of this mechanism would significantly improve and potentially transform predictive models for how organisms respond to global change.

全球海洋生态系统受到海洋酸化的威胁，这是大气中二氧化碳以前所未有的速度增加造成的。由于海洋变化被预测为快速、极端和广泛，海洋物种可能面临“适应或死亡”的情景。然而，对DNA序列的修改可能会被诱导以应对海洋酸化等压力，然后遗传。这种“表观遗传”的改变可能是全球气候变化下种群生存的关键，但它们一直没有得到充分的研究。本研究的目的是描述DNA甲基化的作用，一个可遗传的表观遗传系统，在东部牡蛎（Crassostrea virginica）对海洋酸化的反应。知识价值在于综合方法，它将描述DNA甲基化在牡蛎对海洋酸化的代际反应中的作用。这些跨学科的数据，从分子到生物体水平，将提供深入了解海洋无脊椎动物应对海洋酸化能力的机制，并为未来的跨代研究奠定基础。海洋酸化目前威胁着全世界的海洋物种，并已对水产养殖造成重大损失，特别是对牡蛎物种。这项研究对育种，水产养殖和经济产生了更广泛的影响。根据研究人员的“表观遗传学到海洋”（E2 O）培训计划，研究人员将培养生物信息学和生物化学方面的STEM人才，使低收入学区的女孩接触基因组学职业，并通过开放科学和可重复性推进该领域。这项研究将专门测试间歇性暴露于低pH值是否会诱导甲基化反应，并对生物矿化产生下游有益影响。这些甲基化状态可以遗传，并赋予拥有它们的幼虫适应性优势。该项目的第一阶段将使用暴露实验来确定DNA甲基化改变的程度，并调节对OA的反应。来自该实验的数据将用于检验以下假设：（i）在壳形成的组织中诱导的DNA甲基化（即，外套膜组织），与转录和调节的变化相关的苍白球液pH值（钙化液pH值，通过微电极测量），和（ii）甲基化变化诱导的外套膜组织中也诱导生殖系-表明这种变化是潜在的遗传。该项目的第2阶段将使用配对交叉实验来检验亲本暴露于OA会改变幼虫性状（钙化率、壳结构和多晶型矿物学）的假设。幼虫将从暴露于OA或对照海水的亲本产生，然后在对照或OA条件下饲养。结果将用于（i）表征诱导甲基化状态的遗传，（ii）估计由基因型、非遗传母体/父亲效应、成虫OA暴露、幼虫OA暴露和亲本甲基化组解释的幼虫性状的方差，以及（iii）检验成虫暴露改变幼虫性状遗传力（预测进化反应的量）的假设。由于表观遗传现象对遗传力估计的影响存在很大争议，因此这些结果将促进对这一重要问题的理解。由于研究人员可以发现DNA甲基化是对OA的遗传性可塑性反应的一种机制，因此对这种机制的了解将显着改善并可能改变生物体如何应对全球变化的预测模型。

项目成果

General DNA methylation patterns and environmentally-induced differential methylation in the eastern oyster (Crassostrea virginica)

• DOI: 10.3389/fmars.2020.00225
• 发表时间: 2020-01
• 期刊: bioRxiv
• 作者: Yaamini R. Venkataraman;Alan M. Downey‐Wall;J. Ries;I. Westfield;S. White;S. Roberts;K. Lotterhos

Invertebrate methylomes provide insight into mechanisms of environmental tolerance and reveal methodological biases

无脊椎动物甲基化组提供了对环境耐受机制的深入了解并揭示了方法学偏差

• DOI: 10.1111/1755-0998.13542
• 发表时间: 2021
• 期刊: Molecular Ecology Resources
• 影响因子: 7.7
• 作者: Trigg, Shelly A.;Venkataraman, Yaamini R.;Gavery, Mackenzie R.;Roberts, Steven B.;Bhattacharya, Debashish;Downey‐Wall, Alan;Eirin‐Lopez, Jose M.;Johnson, Kevin M.;Lotterhos, Katie E.;Puritz, Jonathan B.
• 通讯作者: Puritz, Jonathan B.

Larval Response to Parental Low pH Exposure in the Pacific Oyster Crassostrea gigas

• DOI: 10.2983/035.038.0325
• 发表时间: 2019-12
• 期刊: Journal of Shellfish Research
• 影响因子: 1.3
• 作者: Yaamini R. Venkataraman;L. Spencer;S. Roberts