Bio-driven Fe bond restructuring in bio-iron systems enhances electron transfer for chain elongation

IF 11.4 1区环境科学与生态学 Q1 ENGINEERING, ENVIRONMENTAL

Water Research Pub Date : 2025-06-26 DOI:10.1016/j.watres.2025.124114

Quan Liao , Lianpeng Sun , Huanzhong Deng , Siru Zhou , Mingxuan Li , Xinzhe Zhu , Chao Yang , Xiao-yan Li , Lin Lin , Ruo-hong Li

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Abstract

The bio-iron system effectively overcomes the bottleneck in the biosynthesis of medium-chain fatty acids (MCFAs) by enhancing extracellular electron transfer capability. However, the key structural characteristics and dynamic evolution of iron-based electron shuttles remain unclear, limiting system optimization and mechanistic understanding. Among the tested iron species in this study, Fe₃O₄ exhibited the most favorable extracellular electron transfer performance and MCFAs production, highlighting its potential as an efficient electron shuttle. In addition, this study revealed that microorganisms can induce partial transformation of iron powder and Fe₂O₃ into Fe₃O₄ through redox cycling. In contrast, FeCO₃ lacked both structural reconfiguration ability and electron transfer activity, thus limiting MCFAs biosynthesis. Partial least squares regression model, combined with characterization analysis, identified the Fe(III)-O-Fe(II) structure as the key structural characteristics of the electron shuttle. Moreover, X-ray absorption fine structure analysis, interpreted through Marcus theory, demonstrated that bio-driven FeO bond shortening reduces reorganization energy, while FeFe bond elongation expands the electron transfer network. This study elucidates, at the atomic level, the microbial mechanisms underlying the construction and regulation of iron-based electron shuttles, providing a theoretical foundation for the design of bioinspired materials and the optimization of bio-iron systems.

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生物铁系统中生物驱动的铁键重组增强了链延伸的电子转移

生物铁系统通过增强细胞外电子传递能力，有效克服了中链脂肪酸（MCFAs）生物合成的瓶颈。然而，铁基电子穿梭体的关键结构特征和动态演化尚不清楚，限制了系统优化和机理的理解。在本研究测试的铁种中，Fe3O4表现出最有利的细胞外电子转移性能和MCFAs的产生，突出了其作为高效电子穿梭体的潜力。此外，本研究还揭示了微生物可以通过氧化还原循环诱导铁粉和Fe2O3部分转化为Fe3O4。相比之下，FeCO3缺乏结构重构能力和电子转移活性，从而限制了MCFAs的生物合成。偏最小二乘回归模型结合表征分析，确定Fe(III)-O-Fe（II）结构是电子穿梭的关键结构特征。此外，通过Marcus理论解释的x射线吸收精细结构分析表明，生物驱动的Fe-O键缩短降低了重组能，而Fe-Fe键的延伸扩大了电子转移网络。本研究在原子水平上阐明了铁基电子穿梭体构建和调控的微生物机制，为仿生材料的设计和生物铁系统的优化提供了理论基础。

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来源期刊

Water Research 环境科学-工程：环境

CiteScore

20.80

自引率

9.40%

发文量

1307

审稿时长

38 days

期刊介绍： Water Research, along with its open access companion journal Water Research X, serves as a platform for publishing original research papers covering various aspects of the science and technology related to the anthropogenic water cycle, water quality, and its management worldwide. The audience targeted by the journal comprises biologists, chemical engineers, chemists, civil engineers, environmental engineers, limnologists, and microbiologists. The scope of the journal include: •Treatment processes for water and wastewaters (municipal, agricultural, industrial, and on-site treatment), including resource recovery and residuals management; •Urban hydrology including sewer systems, stormwater management, and green infrastructure; •Drinking water treatment and distribution; •Potable and non-potable water reuse; •Sanitation, public health, and risk assessment; •Anaerobic digestion, solid and hazardous waste management, including source characterization and the effects and control of leachates and gaseous emissions; •Contaminants (chemical, microbial, anthropogenic particles such as nanoparticles or microplastics) and related water quality sensing, monitoring, fate, and assessment; •Anthropogenic impacts on inland, tidal, coastal and urban waters, focusing on surface and ground waters, and point and non-point sources of pollution; •Environmental restoration, linked to surface water, groundwater and groundwater remediation; •Analysis of the interfaces between sediments and water, and between water and atmosphere, focusing specifically on anthropogenic impacts; •Mathematical modelling, systems analysis, machine learning, and beneficial use of big data related to the anthropogenic water cycle; •Socio-economic, policy, and regulations studies.