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

Microbially mediated Mn(Ⅱ) oxidation plays a critical role in regulating the global Mn(Ⅱ) cycle and represents an environmentally friendly strategy for remediation Mn(Ⅱ) 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(Ⅱ). The Mn(Ⅱ) oxidation efficiency of strain ss21 reached 98.82% and 97.05% for 200 and 400 mg/L Mn(Ⅱ), respectively. Transcriptome analysis suggested that direct Mn(II) oxidation was associated with the genes encoding copper resistance system multicopper oxidase (HV701_RS04390), LLM-type flavin oxidoreductase (HV701_RS19365) and quinone oxidoreductase (HV701_RS24690), indicating their potential roles in regulating extracellular electron transfer for continuous Mn(II) oxidation. In addition, thioredoxin (HV701_RS19360) and glutathione peroxidase (HV701_RS19445) genes maintained intracellular redox homeostasis, ensuring stable and efficient Mn(Ⅱ) oxidation under high Mn(Ⅱ) stress. Moreover, genes (iscU, hscA, fliS, HV701_RS03300, and HV701_RS06395) associated with metabolic support, motility, and transcriptional regulation supported indirect Mn(Ⅱ) oxidation. Metabolomics analysis revealed the upregulation of L-Tyrosine, L-Isoleucine, Glutamic acid, Gln-His-His, Flavin Adenine Dinucleotide (FAD), Xanthine contributed to alleviating oxidative stress and producing reactive oxygen species (ROS) during Mn(Ⅱ) oxidation, which corresponded to the Mn(Ⅱ) oxidation genes. This study provides a comprehensive understanding of the molecular mechanisms of biological Mn(Ⅱ) oxidation by Achromobacter sp. and highlights its potential application in the bioremediation of Mn contaminated aquatic environments.