Neglected role of iron redox cycle in direct interspecies electron transfer in anaerobic methanogenesis: Inspired from biogeochemical processes

• Published in: Water research (Oxford) Vol. 262; p. 122125
• Main Authors: Xu, Hui, Wang, Mingwei, Hei, Shengqiang, Qi, Xiang, Zhang, Xiaoyuan, Liang, Peng, Fu, Wanyi, Pan, Bingcai, Huang, Xia
• Format: Journal Article
• Language: English
• Published: England Elsevier Ltd 15.09.2024
• Subjects: Aminobacterium; Anaerobic digestion; butyrates; carbon dioxide; cognition; cytochromes; Direct interspecies electron transfer; electron transfer; energy; Fe(III/II) redox cycles; fimbriae; genes; Geobacteraceae; hydrogen; methane production; microorganisms; mineralization; propionic acid; RNA; Semiconductive iron oxides; Syntrophic methanogenesis; wastewater treatment; water; Syntrophic methanogenesis; Fe(III/II) redox cycles; Semiconductive iron oxides; Anaerobic digestion; Direct interspecies electron transfer
• ISSN: 0043-1354; 1879-2448; 1879-2448
• DOI: 10.1016/j.watres.2024.122125

•SM from VFAs was significantly enhanced by semiconductive iron oxides.•The predominant IET pathway was redirected from classical IHT to robust DIET.•An electrical transport matrix was conjectured consisting of iron oxides and pili.•The crucial role of capacitive iron redox cycles was verified to mediate DIET.•DIET-active microorganisms and metabolic pathways were regulated and promoted. Anaerobic digestion is an indispensable technical option towards green and low-carbon wastewater treatment, with interspecies electron transfer (IET) playing a key role in its efficiency and operational stability. The exogenous semiconductive iron oxides have been proven to effectively enhance IET, while the cognition of the physicochemical-biochemical coupling stimulatory mechanism was circumscribed and remains to be elucidated. In this study, semiconductive iron oxides, α-Fe2O3, γ-Fe2O3, α-FeOOH, and γ-FeOOH were found to significantly enhance syntrophic methanogenesis by 76.39, 72.40, 37.33, and 32.64% through redirecting the dominant IET pathway from classical interspecies hydrogen transfer to robust direct interspecies electron transfer (DIET). Their alternative roles as electron shuttles potentially substituting for c-type cytochromes were conjectured to establish an electron transport matrix associated with conductive pili. Distinguished from the conventional electron conductor mechanism of conductive Fe3O4, semiconductive iron oxides facilitated DIET intrinsically through the capacitive Fe(III/II) redox cycles coupled with secondary mineralization. The growth of Aminobacterium, Sedimentibacter, and Methanothrix was enriched and the gene copy numbers of Geobacteraceae 16S ribosomal ribonucleic acid were selectively flourished by 2.0-∼4.5- fold to establish a favorable microflora for DIET pathway. Metabolic pathways of syntrophic acetogenesis from propionate/butyrate and CO2 reduction methanogenesis were correspondingly promoted. The above findings provide new insights into the underlying mechanism of iron minerals enhancing the DIET-oriented pathway and offer paradigms for redox-mediated energy harvesting biological wastewater treatment. [Display omitted]