Comparative Genomic Analysis Reveals Distribution, Organization and Evolution of Metal Resistance Genes in Genus Acidithiobacillus .

Members of genus Acidithiobacillus which can adapt up to extremely high concentration of heavy metals are universally found at acid mine drainage (AMD) sites. We here perform comparative genomic analysis of 37 strains within the genus Acidithiobacillus to answer the untouched questions as to the mechanisms and the evolutionary history of metal resistance genes in Acidithiobacillus spp. Results showed that the evolutionary history of metal resistance genes in Acidithiobacillus spp. involved a combination of gene gains and losses, HGT and gene duplication. Phylogenetic analyses revealed that metal resistance genes in Acidithiobacillus spp. were acquired by early horizontal gene transfer (HGT) events from species that shared habitats with Acidithiobacillus spp. such as Acidihalobacter, Thiobacillus, Acidiferrobacter and Thiomonas Multi-copper oxidase genes involved in copper detoxification were lost in iron-oxidizing A. ferridurans, A. ferrivorans and A. ferrooxidans, and were replaced by rusticyanin during evolution. In addition, widespread purifying selection and predicted high expression levels emphasized the indispensable roles of metal resistance genes for Acidithiobacillus spp. to adapt harsh environments. Taking together, the results suggested that Acidithiobacillus spp. recruited and consolidated additional novel functionalities in adaption to challenging environments via HGT, gene duplication and purifying selection. This study shed light on the distribution, organization, functionality and the complex evolutionary history of metal resistance genes in Acidithiobacillus spp. IMPORTANCE Horizontal gene transfer (HGT), together with natural selection and gene duplication, are three main engines that drive adaptive evolution of microbial genomes. Previous studies indicated that HGT was a main adaptive mechanism for acidophile to cope with heavy metal-rich environments. However, evidences of HGT in Acidithiobacillus species in response to challenging metal-rich environments and mechanisms addressing how metal resistance genes originated and evolved in Acidithiobacillus are still lacking. The findings of this study revealed fascinating phenomena of putative cross-phylum HGT, suggested that Acidithiobacillus spp. recruited and consolidated additional novel functionalities in adaption to challenging environments via HGT, gene duplication and purifying selection. Taken together, the insights gained in this study have improved our understanding on the metal resistance strategies of Acidithiobacillus spp.