Transcriptome analysis reveals manganese tolerance mechanisms in a novel native bacterium of Bacillus altitudinis strain HM-12

Abstract

Bacillus altitudinis HM-12, isolated from ferromanganese ore tailings, can resist up to 1200 mM Mn(II) when exposed to concentrations from 50 mM to 1400 mM. HM-12 exhibited high Mn(II) removal efficiency (90.6 %). We report the transcriptional profile of HM-12 using RNA-Seq and found 423 upregulated and 536 downregulated differentially expressed genes (DEGs) compared to the control. Gene Ontology analysis showed that DEGs were mainly linked with transporter activity, binding, catalytic activity in molecular function, cellular anatomical entity in cellular component, cellular process, and metabolic process. Kyoto Encyclopedia of Genes and Genomes analysis showed that DEGs were mostly mapped to membrane transport, signal transduction, carbohydrate and amino acid metabolism, energy metabolism, and cellular community pathways. Transport analysis showed that two manganese importer systems, mntH and mntABC, were significantly downregulated. The manganese efflux genes (mneS, yceF and ykoY) exhibited significant upregulation. Manganese homeostasis seems to be subtly regulated by manganese uptake and efflux genes. Moreover, it was found that copA as a Mn(II) oxidase gene and a copper chaperone gene copZ were considerably upregulated by signal transduction analysis. csoR encoding a transcriptional repressor which can regulate the copZA operon was upregulated. The strong Mn(II) oxidizing activity of HM-12 was also confirmed by physicochemical characterization. In metabolism and environmental information processing, yjqC encoding manganese catalase was significantly upregulated, while katE and katX encoding heme catalases were significantly downregulated. The antioxidant gene pcaC was significantly upregulated, but ykuU encoding alkyl hydroperoxide reductase, yojM encoding superoxide dismutase, and perR encoding redox-sensing transcriptional repressor were downregulated. These results highlight the oxidative activity of HM-12 by regulating the transcription of oxidase, catalase, peroxidase, and superoxide dismutase to sense the cellular redox status and prevent Mn(II) intoxication. This study provides relevant information on the biological tolerance and oxidation mechanisms in response to Mn(II) stress.