Here,　we　report　three　new　Acidiphilium　genomes,　reclassified　existing　Acidiphilium　species,　and　performed　the　first　comparative　genomic　analysis　on　Acidiphilium　in　an　attempt　to　address　the　metabolic　potential,　ecological　functions,　and　evolutionary　history　of　the　genus　Acidiphilium.　In　the　genomes　of　Acidiphilium,　we　found　an　abundant　repertoire　of　horizontally　transferred　genes　(HTGs)　contributing　to　environmental　adaption　and　metabolic　expansion,　including　genes　conferring　photosynthesis　(puf,　puh),　CO2　assimilation　(rbc),　capacity　for　methane　metabolism　(rnmo,　mdh,　frm),　nitrogen　source　utilization　(nor,　cyn,　limp),　sulfur　compound　utilization　(sox,　psr,　sqr),　and　multiple　metal　and　osmotic　stress　resistance　capacities　(czc,　cop,　ect).　Additionally,　the　predicted　donors　of　horizontal　gene　transfer　were　present　in　a　cooccurrence　network　of　Acidiphilium.　Genome-scale　positive　selection　analysis　revealed　that　15　genes　contained　adaptive　mutations,　most　of　which　were　multi-functional　and　played　critical　roles　in　the　survival　of　extreme　conditions.　We　proposed　that　Acidiphilium　originated　in　mild　conditions　and　adapted　to　extreme　environments　such　as　acidic　mineral　sites　after　the　acquisition　of　many　essential　functions.　IMPORTANCE　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　Acidiphilium　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　Acidiphilium　strains　and　performed　comparative　genomic　analysis　on　this　extremely　acidophilic　bacterial　genus.　We　found　in　the　genomes　of　Acidiphilium　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.