Ferrihydrite-mediated methanotrophic nitrogen fixation in paddy soil under hypoxia.

IF 5.1 Q1 ECOLOGY ISME communications Pub Date : 2024-03-04 eCollection Date: 2024-01-01 DOI:10.1093/ismeco/ycae030
Linpeng Yu, Rong Jia, Shiqi Liu, Shuan Li, Sining Zhong, Guohong Liu, Raymond Jianxiong Zeng, Christopher Rensing, Shungui Zhou
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Abstract

Biological nitrogen fixation (BNF) by methanotrophic bacteria has been shown to play an important role in maintaining fertility. However, this process is still limited to aerobic methane oxidation with sufficient oxygen. It has remained unknown whether and how methanotrophic BNF proceeds in hypoxic environments. Herein, we incubated paddy soils with a ferrihydrite-containing mineral salt medium to enrich methanotrophic bacteria in the presence of methane (20%, v/v) under oxygen constraints (0.27%, v/v). The resulting microcosms showed that ferrihydrite-dependent aerobic methane oxidation significantly contributed (81%) to total BNF, increasing the 15N fixation rate by 13-fold from 0.02 to 0.28 μmol 15N2 (g dry weight soil) -1 d-1. BNF was reduced by 97% when ferrihydrite was omitted, demonstrating the involvement of ferrihydrite in methanotrophic BNF. DNA stable-isotope probing indicated that Methylocystis, Methylophilaceae, and Methylomicrobium were the dominant methanotrophs/methylotrophs that assimilated labeled isotopes (13C or 15N) into biomass. Metagenomic binning combined with electrochemical analysis suggested that Methylocystis and Methylophilaceae had the potential to perform methane-induced BNF and likely utilized riboflavin and c-type cytochromes as electron carriers for ferrihydrite reduction. It was concluded that ferrihydrite mediated methanotrophic BNF by methanotrophs/methylotrophs solely or in conjunction with iron-reducing bacteria. Overall, this study revealed a previously overlooked yet pronounced coupling of iron-dependent aerobic methane oxidation to BNF and improves our understanding of methanotrophic BNF in hypoxic zones.

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缺氧条件下水稻田土壤中铁酸盐介导的甲烷固氮作用
甲烷细菌的生物固氮(BNF)已被证明在保持肥力方面发挥着重要作用。然而,这一过程仍仅限于在氧气充足的情况下进行有氧甲烷氧化。在缺氧环境中,甲烷营养细菌是否以及如何进行 BNF 仍是一个未知数。在此,我们用含铁的矿物盐培养基培养水稻田土壤,以便在有甲烷(20%,v/v)和氧气限制(0.27%,v/v)的情况下富集甲烷营养细菌。由此产生的微生态系统表明,依赖于铁酸盐的有氧甲烷氧化作用对总 BNF 的贡献很大(81%),使 15N 固定率增加了 13 倍,从 0.02 μmol 15N2(克干重土壤)-1 d-1 增加到 0.28 μmol 15N2(克干重土壤)-1 d-1。如果不使用铁酸盐,BNF 会减少 97%,这表明铁酸盐参与了甲烷营养型 BNF。DNA 稳定同位素探测表明,甲烷菌、嗜甲烷菌和甲烷微生物是将标记同位素(13C 或 15N)同化到生物量中的主要甲烷营养体/甲基营养体。元基因组分选结合电化学分析表明,甲基孢囊菌和嗜甲氧微生物有可能进行甲烷诱导的 BNF,并很可能利用核黄素和 c 型细胞色素作为电子载体进行亚铁还原。研究得出的结论是,甲烷营养体/甲基营养体单独或与铁还原菌共同介导了亚铁酸盐的甲烷营养体BNF。总之,这项研究揭示了以前被忽视的铁依赖性有氧甲烷氧化与 BNF 的明显耦合,并增进了我们对缺氧区甲烷营养型 BNF 的了解。
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