Genomic traits, transcriptional responses, and metabolic activities determine functional divergence in mineral dissolution between Priestia megaterium PMA2-2 and Priestia flexa PMD1-1.

Abstract

Priestia strains are gram-positive bacteria and globally distributed in mineral-rich environments. However, the functional divergence in mineral dissolution and its molecular drivers among Priestia strains remains poorly understood. Here, we employ comparative phenotypic and multi-omics analyses to decipher the molecular mechanisms for divergent mineral dissolution phenotypes between the efficient mineral-dissolving Priestia megaterium PMA2-2 and the inefficient mineral-dissolving Priestia flexa PMD1-1. Compared to PMD1-1, PMA2-2 exhibited significantly enhanced biotite dissolution, medium acidification, polysaccharide production, and biofilm formation on the biotite surface. Genomic analysis revealed that PMA2-2 harbored more genes associated with organic acid metabolism, biofilm formation, and EPS biosynthesis than PMD1-1. Transcriptomic and metabolomic analyses linked PMA2-2's enhanced biotite-dissolution phenotype to the coordinated upregulation of genes located on both its chromosome and plasmids, and enhanced production of exometabolites involved in organic acids, proton efflux, biofilm formation, polysaccharide production, amino acid metabolism, cell wall components, and flagellar assembly. Furthermore, genes involved in environmental sensing (including two-component systems and quorum sensing) and nutrient transport systems (ABC transporters) were also upregulated in PMA2-2. Genomic conservation analysis of PMA2-2 revealed that the genes responsible for efficient mineral dissolution are widespread and phylogenetically conserved across the Priestia genus. These core mineral dissolution-related genes were responsive to a range of silicate and oxide minerals (biotite, potassium-feldspar, olivine, and hematite). Our findings establish a genotype-to-phenotype map for mineral dissolution, providing new insights into the functional divergence in mineral dissolution between Priestia strains PMA2-2 and PMD1-1, as well as the molecular mechanisms that facilitate these processes.IMPORTANCETo date, the molecular mechanisms underlying the functional divergence in mineral dissolution in gram-positive Priestia strains are largely unexplored. This study characterizes the mechanisms involved in functional divergence in biotite dissolution between two closely related strains of Priestia, one an efficient mineral-dissolving strain (PMA2-2) and the other an inefficient mineral-dissolving strain (PMD1-1). The coordinated upregulation of genes and exometabolites associated with organic acid and polysaccharide production, proton efflux, biofilm formation, cell wall components, as well as environmental sensing and nutrient transport systems may be responsible for PMA2-2's enhanced biotite dissolution phenotype. The multiple genes associated with efficient mineral dissolution by PMA2-2 are widespread and conserved among Priestia strains. Furthermore, a range of silicate and oxide minerals induced the expression of these core genes related to mineral dissolution by PMA2-2. Our results provide new understandings concerning the molecular mechanisms responsible for driving functional divergence in mineral dissolution between these Priestia strains.