Ecological dynamics explain modular denitrification in the ocean

IF 9.4 1区 综合性期刊 Q1 MULTIDISCIPLINARY SCIENCES Proceedings of the National Academy of Sciences of the United States of America Pub Date : 2024-12-18 DOI:10.1073/pnas.2417421121
Xin Sun, Pearse J. Buchanan, Irene H. Zhang, Magdalena San Roman, Andrew R. Babbin, Emily J. Zakem
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Abstract

Microorganisms in marine oxygen minimum zones (OMZs) drive globally impactful biogeochemical processes. One such process is multistep denitrification (NO 3 →NO 2 →NO→N 2 O→N 2 ), which dominates OMZ bioavailable nitrogen (N) loss and nitrous oxide (N 2 O) production. Denitrification-derived N loss is typically measured and modeled as a single step, but observations reveal that most denitrifiers in OMZs contain subsets (“modules”) of the complete pathway. Here, we identify the ecological mechanisms sustaining diverse denitrifiers, explain the prevalence of certain modules, and examine the implications for N loss. We describe microbial functional types carrying out diverse denitrification modules by their underlying redox chemistry, constraining their traits with thermodynamics and pathway length penalties, in an idealized OMZ ecosystem model. Biomass yields of single-step modules increase along the denitrification pathway when organic matter (OM) limits growth, which explains the viability of populations respiring NO 2 and N 2 O in a NO 3 -filled ocean. Results predict denitrifier community succession along environmental gradients: Pathway length increases as the limiting substrate shifts from OM to N, suggesting a niche for the short NO 3 →NO 2 module in free-living, OM-limited communities, and for the complete pathway in organic particle-associated communities, consistent with observations. The model captures and mechanistically explains the observed dominance and higher oxygen tolerance of the NO 3 →NO 2 module. Results also capture observations that NO 3 is the dominant source of N 2 O. Our framework advances the mechanistic understanding of the relationship between microbial ecology and N loss in the ocean and can be extended to other processes and environments.
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海洋最小含氧带(OMZ)中的微生物推动着具有全球影响的生物地球化学过程。其中一个过程是多步反硝化作用(NO 3 - →NO 2 - →NO→N 2 O→N 2),它主导着 OMZ 生物可用氮(N)的损失和一氧化二氮(N 2 O)的产生。源于反硝化作用的氮损失通常作为一个单一步骤进行测量和建模,但观察结果表明,OMZ 中的大多数反硝化作用都包含完整途径的子集("模块")。在此,我们确定了维持不同反硝化菌的生态机制,解释了某些模块的普遍性,并研究了其对氮损失的影响。在一个理想化的 OMZ 生态系统模型中,我们通过底层氧化还原化学来描述执行不同反硝化模块的微生物功能类型,用热力学和路径长度惩罚来限制它们的性状。当有机物(OM)限制生长时,单步模块的生物量产量会沿着反硝化途径增加,这解释了在充满 NO 3 的海洋中呼吸 NO 2 - 和 N 2 O 的种群的生存能力。研究结果预测了反硝化细菌群落沿环境梯度的演替:当限制性基质从 OM 转向 N 时,路径长度增加,这表明在自由生活的 OM 限制性群落中,NO 3 - →NO 2 - 短模块有其存在的空间,而在有机颗粒相关群落中,完整的路径则有其存在的空间,这与观测结果一致。该模型捕获并从机理上解释了观察到的 NO 3 - →NO 2 - 模块的优势和较高的耐氧性。结果还捕捉到了 NO 3 - 是 N 2 O 的主要来源的观测结果。我们的框架推进了对海洋中微生物生态学与氮损失之间关系的机理理解,并可扩展到其他过程和环境。
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来源期刊
CiteScore
19.00
自引率
0.90%
发文量
3575
审稿时长
2.5 months
期刊介绍: The Proceedings of the National Academy of Sciences (PNAS), a peer-reviewed journal of the National Academy of Sciences (NAS), serves as an authoritative source for high-impact, original research across the biological, physical, and social sciences. With a global scope, the journal welcomes submissions from researchers worldwide, making it an inclusive platform for advancing scientific knowledge.
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