Acid mine drainage (AMD) is characterized by an acid and metal-rich run-off thatoriginates from mining systems. Despite having been studied for many decades,much remains unknown about the microbial community dynamics in AMD sites,especially during their early development, when the acidity is moderate. Here, wedescribe draft genome assemblies from single cells retrieved from an early-stageAMD sample. These cells belong to the genus Hydrotalea and are closely related toHydrotalea flava. The phylogeny and average nucleotide identity analysis suggestthat all single amplified genomes (SAGs) form two clades that may represent differ-ent strains. These cells have the genomic potential for denitrification, copper andother metal resistance. Two coexisting CRISPR-Cas loci were recovered acrossSAGs, and we observed heterogeneity in the population with regard to the spacersequences, together with the loss of trailer-end spacers. Our results suggest thatthe genomes of Hydrotalea sp. strains studied here are adjusting to a quickly chang-ing selective pressure at the microhabitat scale, and an important form of this selec-tive pressure is infection by foreign DNA.