Actinobacteria have frequently been reported in the Andean Puna, including strains of the genus Micrococcus. These strains demonstrate resistance to high levels of UV radiation, arsenic, and multiple antibiotics, and possess large linear plasmids. A comparative analysis of the sequences and putative functions of these plasmids was conducted. The presence of large regions with high sequence identity (exceeding 30 kb in total) in all three studied Micrococcus megaplasmids indicates a clear evolutionary link among these elements. Genes related to essential plasmid functions were primarily found within these conserved regions, while genes associated with resistance to metals and antibiotics resided in accessory regions. Moreover, the abundance of open reading frames related to transposition and recombination, along with local deviations from the average GC content, provides evidence for the mosaic nature and considerable genetic plasticity of these plasmids. This study presents evidence of a common ancestor for linear plasmids in Micrococcus and suggests that horizontal gene transfer likely occurs frequently within Andean lakes, providing the native microbial community with a beneficial gene pool to withstand extreme conditions. Additionally, the successful transfer of the linear plasmid pLMA1 by a DNase-insensitive, conjugation-type mechanism and its potential use as a genetic vector is demonstrated.