Abstract
The mechanism of bacterial adaption to manganese-polluted environments was explored using 50 manganese-tolerant strains of bacteria isolated from soil of the largest manganese mine in China. Efficiency of manganese removal by the isolated strains was investigated using atomic absorption spectrophotometry. Bacillus safensis strain ST7 was the most effective manganese-oxidizing bacteria among the tested isolates, achieving up to 82% removal at a Mn(II) concentration of 2,200 mg/L. Bacteria-mediated manganese oxide precipitates and high motility were observed, and the growth of strain ST7 was inhibited while its biofilm formation was promoted by the presence of Mn(II). In addition, strain ST7 could grow in the presence of high concentrations of Al(III), Cr(VI), and Fe(III). Genome-wide analysis of the gene expression profile of strain ST7 using the RNA-seq method revealed that 2,580 genes were differently expressed under Mn(II) exposure, and there were more downregulated genes (n = 2,021) than upregulated genes (n = 559) induced by Mn stress. KAAS analysis indicated that these differently expressed genes were mainly enriched in material metabolisms, cellular processes, organism systems, and genetic and environmental information processing pathways. A total of twenty-six genes from the transcriptome of strain ST7 were involved in lignocellulosic degradation. Furthermore, after 15 genes were knocked out by homologous recombination technology, it was observed that the transporters, multicopper oxidase, and proteins involved in sporulation and flagellogenesis contributed to the removal of Mn(II) in strain ST7. In summary, B. safensis ST7 adapted to Mn exposure by changing its metabolism, upregulating cation transporters, inhibiting sporulation and flagellogenesis, and activating an alternative stress-related sigB pathway. This bacterial strain could potentially be used to restore soil polluted by multiple heavy metals and is a candidate to support the consolidated bioprocessing community.
Highlights
Manganese (Mn), one of the most abundant metals in the Earth’s crust, exerts a significant impact on the biogeochemical cycles of other metals, sulfur, and carbon and is considered the strongest naturally occurring oxidizing agent in the environment (Tebo et al, 2005)
Soil was sampled from an abandoned manganese mine located in Songtao county, Guizhou, China, that had not performed smelting for 7 years, and 50 bacterial strains were isolated on media supplemented with 200 mg/L Mn(II) (Supplementary Table S2)
These seven strains were characterized as Rhizobium sp., Arthrobacter oxydans, and B. safensis based on nucleotide sequence similarities of the 16S rRNA gene and gyrase subunit A gene (Supplementary Figures S2, S3)
Summary
Manganese (Mn), one of the most abundant metals in the Earth’s crust, exerts a significant impact on the biogeochemical cycles of other metals, sulfur, and carbon and is considered the strongest naturally occurring oxidizing agent in the environment (Tebo et al, 2005). Mn participates in oxidative stress resistance, metabolism and decomposition of reactive oxygen species (ROS) (Bosma et al, 2021), and is required for the development and function of nerve and immune cells, control of blood sugar and vitamin levels in animals, and photosynthesis and respiration processes in plants (Gao et al, 2014). Consumption of food or drinking water containing a high level of Mn has undesirable effects on human health (O’Neal and Zheng, 2015). Excessive Mn can accumulate in the human pancreas, bone, kidney, liver, adrenal, and pituitary glands, with toxic effects and a half-life of nine years in bones (O’Neal and Zheng, 2015). Mn toxicity is associated with dopaminergic dysfunction, and Parkinson’s and Alzheimer’s diseases (Bjørklund et al, 2019)
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