Silicate minerals enhance the expression of genes related to mineral dissolution by <i>Priestia aryabhattai</i> strain C4-10

Silicate mineral-microbe interactions are essential for soil formation, element biogeochemical cycles, and carbon sequestration. However, the molecular mechanisms by which gram-positive bacteria mediate mineral dissolution remain largely unexplored. Here, we characterized a highly effective mineral-dissolving <i>Priestia aryabhattai</i> strain, C4-10, for its biotite and lizardite dissolution activity, alongside the underlying molecular mechanisms. In the medium supplemented with biotite or lizardite, C4-10 significantly increased the Fe, Mg, and Si concentrations between 4 and 48 h of incubation compared to the controls. Notably, in the C4-10-inoculated medium supplemented with biotite or lizardite, significantly decreased pH values in the medium and increased cell counts and biofilm formation on the mineral surfaces were observed over 24 h of incubation. A comparative transcriptomic analysis indicated that significantly upregulated differentially expressed genes were enriched in pathways related to glyoxylate and dicarboxylate metabolism, amino acid biosynthesis, the tricarboxylic acid cycle, and ABC transporters in the presence of biotite. Additionally, the gene expression of <i>lutA_2</i> and <i>actP</i> associated with acid metabolism, <i>glgC</i> linked to biofilm formation, <i>gtaB_3</i> related to cell wall components, and <i>02676</i>, <i>levE</i>, and <i>glnQ</i> associated with transporters, was significantly upregulated in C4-10 in the presence of biotite or lizardite. Importantly, strong positive correlations were observed between the Fe or Mg concentrations and the relative expression levels of these genes during the biotite or lizardite dissolution process by C4-10. Our findings illustrate the involvement of multiple genes and metabolic pathways related to mineral dissolution, highlighting similar molecular mechanisms associated with both biotite and lizardite dissolution by C4-10.IMPORTANCETo date, the molecular mechanisms underlying the dissolution of silicate minerals by gram-positive bacteria remain poorly understood. This study characterizes the mechanisms involved in biotite and lizardite dissolution by C4-10. C4-10 enhanced mineral dissolution through the production of organic acids, cell adsorption, and biofilm formation on mineral surfaces. The presence of biotite upregulated the expression of genes related to mineral dissolution and enriched metabolic pathways, including glyoxylate and dicarboxylate metabolism, amino acid biosynthesis, butanoate metabolism, the tricarboxylic acid cycle, and ABC transporters. Furthermore, significant correlations were observed between Fe or Mg concentrations in the medium and the expression levels of genes associated with acid metabolism, biofilm formation, cell wall metabolism, and transporters during the dissolution of biotite or lizardite by C4-10. Our results provide new insights into the interactions between silicate minerals and mineral-dissolving gram-positive bacteria, as well as the molecular mechanisms that facilitate in these processes.