DPANN　is　known　as　highly　diverse,　globally　widespread,　and　mostly　ectosymbiotic　archaeal　superphylum.　However,　this　group　of　archaea　was　overlooked　for　a　long　time,　and　there　were　limited　in-depth　studies　reported.　In　this　investigation,　41　metagenome-assembled　genomes　(MAGs)　belonging　to　the　DPANN　superphylum　were　recovered　(18　MAGs　had　average　nucleotide　identity　[ANI]　values　of,95%　and　a　percentage　of　conserved　proteins　[POCP]　of　＞50%,　while　14　MAGs　showed　a　POCP　of　＜50%),　which　were　analyzed　comparatively　with　515　other　published　DPANN　genomes.　Mismatches　to　known　16S　rRNA　gene　primers　were　identified　among　16S　rRNA　genes　of　DPANN　archaea.　Numbers　of　gene　families　lost　(mostly　related　to　energy　and　amino　acid　metabolism)　were　over　three　times　greater　than　those　gained　in　the　evolution　of　DPANN　archaea.　Lateral　gene　transfer　(LGT;　similar　to　45.5%　was　cross-domain)　had　facilitated　niche　adaption　of　the　DPANN　archaea,　ensuring　a　delicate　equilibrium　of　streamlined　genomes　with　efficient　niche-adaptive　strategies.　For　instance,　LGT-derived　cytochrome　bd　ubiquinol　oxidase　and　arginine　deiminase　in　the　genomes　of　＂Candidatus　Micrarchaeota＂　could　help　them　better　adapt　to　aerobic　acidic　mine　drainage　habitats.　In　addition,　most　DPANN　archaea　acquired　enzymes　for　biosynthesis　of　extracellular　polymeric　substances　(EPS)　and　transketolase/transaldolase　for　the　pentose　phosphate　pathway　from　Bacteria.　IMPORTANCE　The　domain　Archaea　is　a　key　research　model　for　gaining　insights　into　the　origin　and　evolution　of　life,　as　well　as　the　relevant　biogeochemical　processes.　The　discovery　of　nanosized　DPANN　archaea　has　overthrown　many　aspects　of　microbiology.　However,　the　DPANN　superphylum　still　contains　a　vast　genetic　novelty　and　diversity　that　need　to　be　explored.　Comprehensively　comparative　genomic　analysis　on　the　DPANN　superphylum　was　performed　in　this　study,　with　an　attempt　to　illuminate　its　metabolic　potential,　ecological　distribution　and　evolutionary　history.　Many　interphylum　differences　within　the　DPANN　superphylum　were　found.　For　example,　Altiarchaeota　had　the　biggest　genome　among　DPANN　phyla,　possessing　many　pathways　missing　in　other　phyla,　such　as　formaldehyde　assimilation　and　the　Wood-Ljungdahl　pathway.　In　addition,　LGT　acted　as　an　important　force　to　provide　DPANN　archaeal　genetic　flexibility　that　permitted　the　occupation　of　diverse　niches.　This　study　has　advanced　our　understanding　of　the　diversity　and　genome　evolution　of　archaea.