Deciphering the Cryptic Cycling of Methane in Sediments of a Coastal Wetland

本研究项目调查了南加州沿海湿地无氧区微生物在沉积物中产生甲烷和消耗甲烷之间的密切关系。这两种密切相关的微生物群之间的甲烷直接交换被称为“隐性甲烷循环”，直到最近才被发现，人们对其在减少沿海湿地甲烷排放方面的重要性知之甚少。这项研究将揭示碳是如何在两种微生物之间移动的，并将识别涉及的微生物。它还将揭示不同环境条件下甲烷产生和消耗之间的重要代谢反应和平衡。为了产生更广泛的影响，该项目将为两名本科生和一名研究生提供跨学科湿地科学和最先进实验室方法的培训。一门关于全球甲烷排放的新生课程将带领本科生进入这一领域，提供有关当地沿海湿地环境的教育。该项目的结果将分发给公众和学术团体，并将更好地了解沿海湿地的甲烷生产和消耗情况。自前工业化时代以来，大气中甲烷的浓度增加了一倍多，因此我们迫切需要了解控制这种强效温室气体排放的机制。最近的研究提供了第一个证据，证明微生物在富含有机物的沉积物的硫酸盐还原区同时产生和消耗甲烷，这一过程被称为“隐甲烷循环”。在该工艺中，建议将甲烷由甲基营养化产甲烷直接转化为甲烷厌氧氧化（AOM）。然而，对于参与其中的生物的身份，碳从一种代谢到另一种代谢的踪迹，或者这两个过程的环境净结果，人们知之甚少。没有这种代谢关系的细节，沉积物的甲烷收支仍然是不完整的。沿海湿地是研究隐性甲烷循环的重要研究对象，因为其富含有机和硫酸盐的沉积物促进了甲基化甲烷生成的甲基化底物的产生，并为AOM提供了电子受体。然而，厌氧微生物从这个生态系统中去除甲烷，特别是沿着海洋和陆地之间的硫酸盐梯度，仍然没有得到很好的理解。在智力方面，本研究阐明了在沿海湿地中参与隐蔽甲烷循环的产甲烷和养甲烷古菌的身份，以及在这种代谢关系中为甲烷去除提供燃料的电子受体的选择。这项研究提供了新的代谢线索，揭示了驱动甲烷生成和AOM的酶机制的多功能性。通过捕获控制这两个过程之间的平衡的环境因素，本工作的结果进一步增强了对沿海湿地沉积物中甲烷动力学的理解。这些信息可以应用于生物地球化学模型，以改进对该生态系统甲烷排放的预测，该生态系统在全球沿海地区都有发现。为了产生更广泛的影响，该研究为两名本科生和一名研究生提供创新分析和实验技术的培训。此外，该项目每年还会吸引20名本科生参加新成立的新生研讨班“甲烷——另一个温室问题”，研讨班还包括对当地湿地的实地考察。研讨会的目的是教育学生，包括那些没有进入STEM领域的学生，了解甲烷的全球来源和汇，以及它在现在和未来对全球变暖的影响。这项研究的结果将广泛传播到教育和公共推广平台，如高中、社区学院和环境非营利组织，以教授科学方法、生物地球化学循环的概念，并提高对这一重要沿海环境的认识。该奖项反映了美国国家科学基金会的法定使命，并通过使用基金会的知识价值和更广泛的影响审查标准进行评估，被认为值得支持。

This research project investigates the close relationship between methane production and consumption in sediments by microbes in the oxygen-free zone of a coastal wetland in Southern California. The direct exchange of methane between those two closely related microbial groups, which has been named "cryptic methane cycling", has only recently been identified and little is known about its importance in reducing methane emissions from coastal wetlands. This research will reveal how carbon moves between the two types of microbes, and will identify the microbes involved. It will also reveal the important metabolic reactions responsible and the balance between methane production and consumption under different environmental conditions. Towards broader impacts, this project will provide training for two undergraduate and one graduate student in interdisciplinary wetland science and state of the art laboratory methods. A new freshmen course on global methane emissions will bring undergraduate students into the field to provide education on local coastal wetland environments. Results of the project will be disseminated to public and academic groups and will provide a better understanding of methane production and consumption in coastal wetlands.Concentrations of atmospheric methane have more than doubled since the pre-industrial era, hence we urgently need to understand the mechanisms that control the emission of this potent greenhouse gas. Recent studies have provided the first evidence for the simultaneous microbial production and consumption of methane in the sulfate reduction zone of organic-rich sediments, a process named the "cryptic methane cycle." In this process, methane is proposed to be passed directly from methylotrophic methanogenesis to anaerobic oxidation of methane (AOM). However, little is known about the identity of the organisms involved, the trail of carbon from one metabolism to the other, or the environmental net result of the two processes. Without the details of this metabolic relationship, methane budgets of sediments remain incomplete. Coastal wetlands are of particular interest for the study of cryptic methane cycling, because their organic and sulfate rich sediments promote the production of methylated substrates for methylotrophic methanogenesis and provide electron acceptors for AOM. Yet, anaerobic microbial removal of methane from this ecosystem, particularly along the sulfate gradient between ocean and land, is still not well understood. Towards intellectual merit, this study elucidates the identity of methanogenic and methanotrophic archaea involved in cryptic methane cycling in a coastal wetland as well as the selection of electron acceptors that fuel methane removal in this metabolic relationship. The research provides new metabolic clues to unravel the versatility of the enzymatic machinery that drives methanogenesis and AOM. By capturing environmental factors that control the balance between the two processes working in close proximity, the results of this work further provide an enhanced understanding of methane dynamics in coastal wetland sediments. This information can be applied to biogeochemical models to improve the prediction of methane emissions from this ecosystem, which is found throughout the global coastal zone. Towards broader impacts, the research provides training in innovative analytical and experimental techniques to two undergraduate and one graduate student. The project further engages 20 undergraduates per year in a newly developed freshman seminar, "Methane - the Other Greenhouse Problem" including a field trip to the local wetland. The goal of the seminar will be to educate students, including those not entering STEM fields, about global sources and sinks of methane and its involvement in global warming now and in the future. Results of this study will be broadly disseminated to educational and public outreach platforms, such as high schools, community colleges, and environmental non-profits to teach scientific methodologies, concepts of biogeochemical cycling, and enhance the appreciation of this vital coastal environment.This award reflects NSF's statutory mission and has been deemed worthy of support through evaluation using the Foundation's intellectual merit and broader impacts review criteria.