Insights into the Metabolism and Evolution of the Genus <i>Acidiphilium</i> , a Typical Acidophile in Acid Mine Drainage

Abstract

Here, we report three new <i>Acidiphilium</i> genomes, reclassified existing <i>Acidiphilium</i> species, and performed the first comparative genomic analysis on <i>Acidiphilium</i> in an attempt to address the metabolic potential, ecological functions, and evolutionary history of the genus <i>Acidiphilium</i> In the genomes of <i>Acidiphilium</i>, we found an abundant repertoire of horizontally transferred genes (HTGs) contributing to environmental adaption and metabolic expansion, including genes conferring photosynthesis (<i>puf, puh</i>), CO₂ assimilation (<i>rbc</i>), capacity for methane metabolism (<i>mmo, mdh</i>, <i>frm</i>), nitrogen source utilization (<i>nar, cyn, hmp</i>), sulfur compound utilization (<i>sox, psr, sqr</i>), and multiple metal and osmotic stress resistance capacities (<i>czc, cop, ect</i>). Additionally, the predicted donors of horizontal gene transfer were present in a cooccurrence network of <i>Acidiphilium</i> Genome-scale positive selection analysis revealed that 15 genes contained adaptive mutations, most of which were multifunctional and played critical roles in the survival of extreme conditions. We proposed that <i>Acidiphilium</i> originated in mild conditions and adapted to extreme environments such as acidic mineral sites after the acquisition of many essential functions.<b>IMPORTANCE</b> Extremophiles, organisms that thrive in extreme environments, are key models for research on biological adaption. They can provide hints for the origin and evolution of life, as well as improve the understanding of biogeochemical cycling of elements. Extremely acidophilic bacteria such as <i>Acidiphilium</i> are widespread in acid mine drainage (AMD) systems, but the metabolic potential, ecological functions, and evolutionary history of this genus are still ambiguous. Here, we sequenced the genomes of three new <i>Acidiphilium</i> strains and performed comparative genomic analysis on this extremely acidophilic bacterial genus. We found in the genomes of <i>Acidiphilium</i> an abundant repertoire of horizontally transferred genes (HTGs) contributing to environmental adaption and metabolic ability expansion, as indicated by phylogenetic reconstruction and gene context comparison. This study has advanced our understanding of microbial evolution and biogeochemical cycling in extreme niches.