硝酸盐氨化 Geobacteraceae 产生的前所未有的 N2O 具有独特的 N2O 同位素特征。

IF 5.1 1区 生物学 Q1 MICROBIOLOGY
mBio Pub Date : 2024-10-30 DOI:10.1128/mbio.02540-24
Zhenxing Xu, Shohei Hattori, Yoko Masuda, Sakae Toyoda, Keisuke Koba, Pei Yu, Naohiro Yoshida, Zong-Jun Du, Keishi Senoo
{"title":"硝酸盐氨化 Geobacteraceae 产生的前所未有的 N2O 具有独特的 N2O 同位素特征。","authors":"Zhenxing Xu, Shohei Hattori, Yoko Masuda, Sakae Toyoda, Keisuke Koba, Pei Yu, Naohiro Yoshida, Zong-Jun Du, Keishi Senoo","doi":"10.1128/mbio.02540-24","DOIUrl":null,"url":null,"abstract":"<p><p>Dissimilatory nitrate reduction to ammonium (DNRA), driven by nitrate-ammonifying bacteria, is an increasingly appreciated nitrogen-cycling pathway in terrestrial ecosystems. This process reportedly generates nitrous oxide (N<sub>2</sub>O), a strong greenhouse gas with ozone-depleting effects. However, it remains poorly understood how N<sub>2</sub>O is produced by environmental nitrate-ammonifiers and how to identify DNRA-derived N<sub>2</sub>O. In this study, we characterize two novel enzymatic pathways responsible for N<sub>2</sub>O production in <i>Geobacteraceae</i> strains, which are predominant nitrate-ammonifying bacteria in paddy soils. The first pathway involves a membrane-bound nitrate reductase (Nar) and a hybrid cluster protein complex (Hcp-Hcr) that catalyzes the conversion of NO<sub>2</sub><sup>-</sup> to NO and subsequently to N<sub>2</sub>O. The second pathway is observed in Nar-deficient bacteria, where the nitrite reductase (NrfA) generates NO, which is then reduced to N<sub>2</sub>O by Hcp-Hcr. These enzyme combinations are prevalent across the domain Bacteria. Moreover, we observe distinctive isotopocule signatures of DNRA-derived N<sub>2</sub>O from other established N<sub>2</sub>O production pathways, especially through the highest <sup>15</sup>N-site preference (SP) values (43.0‰-49.9‰) reported so far, indicating a robust means for N<sub>2</sub>O source partitioning. Our findings demonstrate two novel N<sub>2</sub>O production pathways in DNRA that can be isotopically distinguished from other pathways.IMPORTANCEStimulation of DNRA is a promising strategy to improve fertilizer efficiency and reduce N<sub>2</sub>O emission in agriculture soils. This process converts water-leachable NO<sub>3</sub><sup>-</sup> and NO<sub>2</sub><sup>-</sup> into soil-adsorbable NH<sub>4</sub><sup>+</sup>, thereby alleviating nitrogen loss and N<sub>2</sub>O emission resulting from denitrification. However, several studies have noted that DNRA can also be a source of N<sub>2</sub>O, contributing to global warming. This contribution is often masked by other N<sub>2</sub>O generation processes, leading to a limited understanding of DNRA as an N<sub>2</sub>O source. Our study reveals two widespread yet overlooked N<sub>2</sub>O production pathways in <i>Geobacteraceae</i>, the predominant DNRA bacteria in paddy soils, along with their distinctive isotopocule signatures. These findings offer novel insights into the role of the DNRA bacteria in N<sub>2</sub>O production and underscore the significance of N<sub>2</sub>O isotopocule signatures in microbial N<sub>2</sub>O source tracking.</p>","PeriodicalId":18315,"journal":{"name":"mBio","volume":null,"pages":null},"PeriodicalIF":5.1000,"publicationDate":"2024-10-30","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":"{\"title\":\"Unprecedented N<sub>2</sub>O production by nitrate-ammonifying <i>Geobacteraceae</i> with distinctive N<sub>2</sub>O isotopocule signatures.\",\"authors\":\"Zhenxing Xu, Shohei Hattori, Yoko Masuda, Sakae Toyoda, Keisuke Koba, Pei Yu, Naohiro Yoshida, Zong-Jun Du, Keishi Senoo\",\"doi\":\"10.1128/mbio.02540-24\",\"DOIUrl\":null,\"url\":null,\"abstract\":\"<p><p>Dissimilatory nitrate reduction to ammonium (DNRA), driven by nitrate-ammonifying bacteria, is an increasingly appreciated nitrogen-cycling pathway in terrestrial ecosystems. This process reportedly generates nitrous oxide (N<sub>2</sub>O), a strong greenhouse gas with ozone-depleting effects. However, it remains poorly understood how N<sub>2</sub>O is produced by environmental nitrate-ammonifiers and how to identify DNRA-derived N<sub>2</sub>O. In this study, we characterize two novel enzymatic pathways responsible for N<sub>2</sub>O production in <i>Geobacteraceae</i> strains, which are predominant nitrate-ammonifying bacteria in paddy soils. The first pathway involves a membrane-bound nitrate reductase (Nar) and a hybrid cluster protein complex (Hcp-Hcr) that catalyzes the conversion of NO<sub>2</sub><sup>-</sup> to NO and subsequently to N<sub>2</sub>O. The second pathway is observed in Nar-deficient bacteria, where the nitrite reductase (NrfA) generates NO, which is then reduced to N<sub>2</sub>O by Hcp-Hcr. These enzyme combinations are prevalent across the domain Bacteria. Moreover, we observe distinctive isotopocule signatures of DNRA-derived N<sub>2</sub>O from other established N<sub>2</sub>O production pathways, especially through the highest <sup>15</sup>N-site preference (SP) values (43.0‰-49.9‰) reported so far, indicating a robust means for N<sub>2</sub>O source partitioning. Our findings demonstrate two novel N<sub>2</sub>O production pathways in DNRA that can be isotopically distinguished from other pathways.IMPORTANCEStimulation of DNRA is a promising strategy to improve fertilizer efficiency and reduce N<sub>2</sub>O emission in agriculture soils. This process converts water-leachable NO<sub>3</sub><sup>-</sup> and NO<sub>2</sub><sup>-</sup> into soil-adsorbable NH<sub>4</sub><sup>+</sup>, thereby alleviating nitrogen loss and N<sub>2</sub>O emission resulting from denitrification. However, several studies have noted that DNRA can also be a source of N<sub>2</sub>O, contributing to global warming. This contribution is often masked by other N<sub>2</sub>O generation processes, leading to a limited understanding of DNRA as an N<sub>2</sub>O source. Our study reveals two widespread yet overlooked N<sub>2</sub>O production pathways in <i>Geobacteraceae</i>, the predominant DNRA bacteria in paddy soils, along with their distinctive isotopocule signatures. These findings offer novel insights into the role of the DNRA bacteria in N<sub>2</sub>O production and underscore the significance of N<sub>2</sub>O isotopocule signatures in microbial N<sub>2</sub>O source tracking.</p>\",\"PeriodicalId\":18315,\"journal\":{\"name\":\"mBio\",\"volume\":null,\"pages\":null},\"PeriodicalIF\":5.1000,\"publicationDate\":\"2024-10-30\",\"publicationTypes\":\"Journal Article\",\"fieldsOfStudy\":null,\"isOpenAccess\":false,\"openAccessPdf\":\"\",\"citationCount\":\"0\",\"resultStr\":null,\"platform\":\"Semanticscholar\",\"paperid\":null,\"PeriodicalName\":\"mBio\",\"FirstCategoryId\":\"99\",\"ListUrlMain\":\"https://doi.org/10.1128/mbio.02540-24\",\"RegionNum\":1,\"RegionCategory\":\"生物学\",\"ArticlePicture\":[],\"TitleCN\":null,\"AbstractTextCN\":null,\"PMCID\":null,\"EPubDate\":\"\",\"PubModel\":\"\",\"JCR\":\"Q1\",\"JCRName\":\"MICROBIOLOGY\",\"Score\":null,\"Total\":0}","platform":"Semanticscholar","paperid":null,"PeriodicalName":"mBio","FirstCategoryId":"99","ListUrlMain":"https://doi.org/10.1128/mbio.02540-24","RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q1","JCRName":"MICROBIOLOGY","Score":null,"Total":0}
引用次数: 0

摘要

由硝酸盐氨化细菌驱动的硝酸盐还原成氨(DNRA)是陆地生态系统中一个日益受到重视的氮循环途径。据报道,这一过程会产生一氧化二氮(N2O),这是一种具有臭氧消耗效应的强温室气体。然而,人们对环境硝酸盐氨化剂如何产生一氧化二氮以及如何识别 DNRA 衍生的一氧化二氮仍然知之甚少。在本研究中,我们描述了水稻田土壤中主要硝酸盐氨化细菌革兰氏菌株产生 N2O 的两种新型酶途径。第一种途径涉及膜结合硝酸还原酶(Nar)和杂交簇蛋白复合物(Hcp-Hcr),它们催化 NO2- 转化为 NO,然后再转化为 N2O。在缺乏 Nar 的细菌中观察到第二种途径,即亚硝酸盐还原酶(NrfA)生成 NO,然后由 Hcp-Hcr 还原成 N2O。这些酶组合在整个细菌领域都很普遍。此外,我们还观察到 DNRA 衍生的 N2O 与其他已建立的 N2O 生产途径具有不同的同位素特征,特别是通过迄今为止报道的最高 15N 位点偏好(SP)值(43.0‰-49.9‰),这表明 N2O 来源分区具有强大的手段。我们的研究结果表明,DNRA 中有两种新的 N2O 生成途径,可以从同位素角度将它们与其他途径区分开来。重要意义对 DNRA 进行优化是提高肥料效率和减少农业土壤中 N2O 排放的一种有前途的策略。这一过程将可渗出水的 NO3- 和 NO2- 转化为可被土壤吸收的 NH4+,从而减少了反硝化作用造成的氮素损失和 N2O 排放。然而,一些研究指出,DNRA 也可能成为一氧化二氮的来源,导致全球变暖。这种贡献往往被其他氧化亚氮生成过程所掩盖,导致人们对 DNRA 作为氧化亚氮来源的认识有限。我们的研究揭示了水稻田土壤中最主要的二硝基氧化还原菌(Geobacteraceae)中两种广泛存在但被忽视的一氧化二氮产生途径,以及它们独特的同位素标记。这些发现为了解 DNRA 细菌在 N2O 生产中的作用提供了新的视角,并强调了 N2O 同位素特征在微生物 N2O 源追踪中的重要性。
本文章由计算机程序翻译,如有差异,请以英文原文为准。
Unprecedented N2O production by nitrate-ammonifying Geobacteraceae with distinctive N2O isotopocule signatures.

Dissimilatory nitrate reduction to ammonium (DNRA), driven by nitrate-ammonifying bacteria, is an increasingly appreciated nitrogen-cycling pathway in terrestrial ecosystems. This process reportedly generates nitrous oxide (N2O), a strong greenhouse gas with ozone-depleting effects. However, it remains poorly understood how N2O is produced by environmental nitrate-ammonifiers and how to identify DNRA-derived N2O. In this study, we characterize two novel enzymatic pathways responsible for N2O production in Geobacteraceae strains, which are predominant nitrate-ammonifying bacteria in paddy soils. The first pathway involves a membrane-bound nitrate reductase (Nar) and a hybrid cluster protein complex (Hcp-Hcr) that catalyzes the conversion of NO2- to NO and subsequently to N2O. The second pathway is observed in Nar-deficient bacteria, where the nitrite reductase (NrfA) generates NO, which is then reduced to N2O by Hcp-Hcr. These enzyme combinations are prevalent across the domain Bacteria. Moreover, we observe distinctive isotopocule signatures of DNRA-derived N2O from other established N2O production pathways, especially through the highest 15N-site preference (SP) values (43.0‰-49.9‰) reported so far, indicating a robust means for N2O source partitioning. Our findings demonstrate two novel N2O production pathways in DNRA that can be isotopically distinguished from other pathways.IMPORTANCEStimulation of DNRA is a promising strategy to improve fertilizer efficiency and reduce N2O emission in agriculture soils. This process converts water-leachable NO3- and NO2- into soil-adsorbable NH4+, thereby alleviating nitrogen loss and N2O emission resulting from denitrification. However, several studies have noted that DNRA can also be a source of N2O, contributing to global warming. This contribution is often masked by other N2O generation processes, leading to a limited understanding of DNRA as an N2O source. Our study reveals two widespread yet overlooked N2O production pathways in Geobacteraceae, the predominant DNRA bacteria in paddy soils, along with their distinctive isotopocule signatures. These findings offer novel insights into the role of the DNRA bacteria in N2O production and underscore the significance of N2O isotopocule signatures in microbial N2O source tracking.

求助全文
通过发布文献求助,成功后即可免费获取论文全文。 去求助
来源期刊
mBio
mBio MICROBIOLOGY-
CiteScore
10.50
自引率
3.10%
发文量
762
审稿时长
1 months
期刊介绍: mBio® is ASM''s first broad-scope, online-only, open access journal. mBio offers streamlined review and publication of the best research in microbiology and allied fields.
×
引用
GB/T 7714-2015
复制
MLA
复制
APA
复制
导出至
BibTeX EndNote RefMan NoteFirst NoteExpress
×
提示
您的信息不完整,为了账户安全,请先补充。
现在去补充
×
提示
您因"违规操作"
具体请查看互助需知
我知道了
×
提示
确定
请完成安全验证×
copy
已复制链接
快去分享给好友吧!
我知道了
右上角分享
点击右上角分享
0
联系我们:info@booksci.cn Book学术提供免费学术资源搜索服务,方便国内外学者检索中英文文献。致力于提供最便捷和优质的服务体验。 Copyright © 2023 布克学术 All rights reserved.
京ICP备2023020795号-1
ghs 京公网安备 11010802042870号
Book学术文献互助
Book学术文献互助群
群 号:481959085
Book学术官方微信