Microbial electrotrophs-driven molecular transformations of dissolved organic matter in paddy soil

Rong Tang; Xiaoshan Luo; Wenjie He; Xixi Cai; Lingyan Huang; Lihua Zhou; Yong Yuan

doi:10.1016/j.jenvman.2025.126562

Microbial electrotrophs-driven molecular transformations of dissolved organic matter in paddy soil

J Environ Manage. 2025 Jul 12:391:126562. doi: 10.1016/j.jenvman.2025.126562. Online ahead of print.

Authors

Rong Tang¹, Xiaoshan Luo², Wenjie He¹, Xixi Cai¹, Lingyan Huang¹, Lihua Zhou³, Yong Yuan⁴

Affiliations

¹ Guangdong Key Laboratory of Environmental Catalysis and Health Risk Control, Guangzhou Key Laboratory Environmental Catalysis and Pollution Control, School of Environmental Science and Engineering, Institute of Environmental Health and Pollution Control, Guangdong University of Technology, Guangzhou, 510006, China.
² School of Materials and Environmental Engineering, Shenzhen Polytechnic University, Shenzhen, 518055, China.
³ School of Biomedical and Pharmaceutical Sciences, Guangdong University of Technology, Guangzhou, 510006, China.
⁴ Guangdong Key Laboratory of Environmental Catalysis and Health Risk Control, Guangzhou Key Laboratory Environmental Catalysis and Pollution Control, School of Environmental Science and Engineering, Institute of Environmental Health and Pollution Control, Guangdong University of Technology, Guangzhou, 510006, China. Electronic address: yuanyong@soil.gd.cn.

PMID: 40652718
DOI: 10.1016/j.jenvman.2025.126562

Abstract

Microbial electrotrophs are key players in biogeochemical cycles, but the impact of electrotrophic communities on the diverse chemical composition and properties of dissolved organic matter (DOM) molecules in paddy soils has not been comprehensively explored. Herein, we investigated the response of DOM molecules in paddy soil-based microcosms to electrotrophic communities using microbial electrosynthesis systems (MESs), high-resolution mass spectrometry, and genome-centric metagenomics techniques. Compared to the open-circuit control, the closed-circuit system exhibited a 2.6-fold increase in dissolved organic carbon concentration after 120 days of incubation in the MESs, with aromatic and tannin molecular abundances rising by 3.5-fold and 4.4-fold, respectively. These results indicate that electrotrophic activity enhances both the structural complexity and aromatization (humification degree) of soil DOM. Functional annotation revealed significant enrichment of the reductive tricarboxylic acid (rTCA) cycle and Calvin-Benson-Bassham (CBB) cycle, demonstrating active CO₂ assimilation by electrotrophs into complex organic compounds. Electrotrophic genera such as Pseudomonas, Hyphomicrobium, Phenylobacterium, Achromobacter, Geobacter, Anaeromyxobacter, and Magnetospirillum were substantially enriched under the closed-circuit conditions, with relative abundances increasing from 0.02-0.72 % to 1.65-13.68 %. These microbes likely facilitated DOM stabilization by coupling extracellular electron uptake with CO₂ fixation, thereby transforming labile organic carbon into more stable molecular structures. These findings elucidate the impact of electrotrophic bacteria in regulating the DOM transformation, providing a deeper understanding of the transformation mechanisms of DOM in paddy soils.

Keywords: Carbon conversion; DOM; Exoelectrogenic microorganisms; Microbial electrotrophy; functional genes.