Multi-omic landscape of Mn(II) oxidation in Achromobacter pulmonis ss21: From multicopper oxidase to metabolic support electron transfer

Abstract

Microbially mediated Mn() oxidation plays a critical role in regulating the global Mn() cycle and represents an environmentally friendly strategy for remediation Mn() contaminated waters. This study presents the first demonstration that Achromobacter pulmonis ss21, a bacterium isolated from Baiyangdian Lake, exhibits the excellent capacity to oxidze Mn(). The Mn() oxidation efficiency of ss21 reached 98.82% and 97.05% for 200 and 400 mg/L Mn(), respectively. Transcriptome analysis revealed that direct Mn() oxidation was catalyzed by genes encoding copper resistance system multicopper oxidase (HV701_RS04390), LLM-type flavin oxidoreductase (HV701_RS19365) and quinone oxidoreductase (HV701_RS24690), which regulate extracellular electron transfer for continuous Mn() oxidation. In addition, thioredoxin (HV701_RS19360) and glutathione peroxidase (HV701_RS19445) genes maintained intracellular redox homeostasis, ensuring stable and efficient direct Mn() oxidation under high Mn() stress. Moreover, genes (iscU, hscA, fliS, HV701_RS03300, and HV701_RS06395) associated with metabolic support, motility, and transcriptional regulation supported indirect Mn() oxidation. Metabolomics analysis revealed the upregulation of L-Tyrosine, L-Isoleucine, glutamic acid, Gln-His-His, Flavin Adenine Dinucleotide (FAD), xanthine related to ss21 Mn() oxidation, which corresponded to the direct Mn() oxidation genes. This study provides a comprehensive understanding of the molecular mechanisms of biological Mn() oxidation by Achromobacter sp. and highlights its potential application in the bioremediation of Mn contaminated aquatic environments under high metal stress conditions. IMPORTANCEMicrobially mediated Mn() oxidation is a fundamental process in global biogeochemical cycles and offers a sustainable pathway for remediating heavy metal-polluted waters. Achromobacter pulmonis ss21 showed excellent performance in Mn() oxidation. The highly efficient removal of Mn() was achieved through oxidoreductase catalysis, regulation of extracellular electron transfer, maintenance of redox homeostasis, and ensurance of stable and efficient Mn() oxidation under high Mn() stress. Moreover, the Mn() oxidation was supported by metabolites, which prevented irreversible protein damage from oxidative stress induced by high Mn() concentration, alleviating oxidative stress, and stimulating the production of ROS. These findings expand the known diversity of Mn() oxidizing bacteria and offer valuable information for the molecular mechanisms of biological Mn() oxidation.