Cr(VI) bioreduction enhanced by the electron transfer between flavin reductase and persistent free radicals

Cheng Yu; Yassine Riahi; Qian Wang; Mengyang Feng; Abdelkader Mohamed; Ke Dai; Peng Cai; Qiaoyun Huang

doi:10.1016/j.chemosphere.2024.143746

Cr(VI) bioreduction enhanced by the electron transfer between flavin reductase and persistent free radicals

Chemosphere. 2024 Nov 12:143746. doi: 10.1016/j.chemosphere.2024.143746. Online ahead of print.

Authors

Cheng Yu¹, Yassine Riahi¹, Qian Wang¹, Mengyang Feng¹, Abdelkader Mohamed², Ke Dai³, Peng Cai⁴, Qiaoyun Huang⁴

Affiliations

¹ College of Resources and Environment, Huazhong Agricultural University, Wuhan 430070, P.R.China.
² College of Resources and Environment, Huazhong Agricultural University, Wuhan 430070, P.R.China; Soil and Water Res. Department, Nuclear Research Center, Egyptian Atomic Energy Authority, 13759, Egypt.
³ College of Resources and Environment, Huazhong Agricultural University, Wuhan 430070, P.R.China; Key Laboratory of Arable Soil Remediation Technology (Central China), Ministry of Agriculture and Rural Affairs, Wuhan 430070, P.R.China. Electronic address: dk@mail.hzau.edu.cn.
⁴ College of Resources and Environment, Huazhong Agricultural University, Wuhan 430070, P.R.China; Key Laboratory of Arable Soil Remediation Technology (Central China), Ministry of Agriculture and Rural Affairs, Wuhan 430070, P.R.China; National Key Laboratory of Agricultural Microbiology, Wuhan 430070, P.R.China.

PMID: 39542366
DOI: 10.1016/j.chemosphere.2024.143746

Abstract

Persistent free radicals (PFRs) in biochar are an important electron shuttle for mediating electron transfer, which has significant impact on the biogeochemical redox reactions. Although the influence of biochar on the extracellular electron transfer (EET) for redox cycle has been extensively studied, the molecular mechanism for promoting the EET with PFRs remains poorly understood. This study investigated the oxygen-centered PFRs-mediated Cr(VI) reduction by Shewanella oneidensis MR-1 (MR-1) and exhibited the molecular mechanism of electron transfer between flavin substances and PFRs. Results showed that the Cr(VI) bioreduction rate by MR-1 increased from 31% to 70% with the addition of biochar. Electrochemical results illustrated that biochar increased biocurrent generation in the Cr(VI) bioreduction process. 3D-EEM and LC/MS spectra indicated that MR-1 secreted the flavin mononucleotide (FMN) reductase that relied on the [H] to provide the electrons. Electron paramagnetic resonance spectra illustrated that PFRs in biochar accepted the electrons from FMN reductase and stored those bioelectrons. Because of the oxidation of FMN, the electron transfer from FMN reductase to PFRs would increase the intracellular reactive oxygen species, which further produced the extracellular ·O₂^-. The reduced PFRs released the bioelectrons, accelerating the Cr(VI) reduction by ·O₂^-. Together with the results of the mutant strains experiment, it was found that the EET by c-cytochrome and free radicals contributed to the Cr(VI) bioreduction by 7.1% and 92.9%, respectively. These findings revealed that the PFRs could participate in the EET process and promote the redox reactions, providing a new approach for enhancing the remediation of heavy metal pollution by microorganisms and suggesting the important role of PFRs in the electron transfer process.

Keywords: extracellular electron transfer; flavin; microbial redox; persistent free radicals; reactive oxygen species.