Department of Invertebrate Zoology, Faculty of Biology, Saint Petersburg State University, St. Petersburg, Russian Federation
Tatiana S Miroliubova
Department of Invertebrate Zoology, Faculty of Biology, Saint Petersburg State University, St. Petersburg, Russian Federation; Severtsov Institute of Ecology and Evolution, Russian Academy of Sciences, Moscow, Russian Federation
Kirill V Mikhailov
Belozersky Institute for Physico-Chemical Biology, Lomonosov Moscow State University, Moscow, Russian Federation; Kharkevich Institute for Information Transmission Problems, Russian Academy of Sciences, Moscow, Russian Federation
Thomas Birley
Department of Genetics, Evolution and Environment, University College London, London, United Kingdom
Belozersky Institute for Physico-Chemical Biology, Lomonosov Moscow State University, Moscow, Russian Federation; Kharkevich Institute for Information Transmission Problems, Russian Academy of Sciences, Moscow, Russian Federation
The phylum Apicomplexa comprises human pathogens such as Plasmodium but is also an under-explored hotspot of evolutionary diversity central to understanding the origins of parasitism and non-photosynthetic plastids. We generated single-cell transcriptomes for all major apicomplexan groups lacking large-scale sequence data. Phylogenetic analysis reveals that apicomplexan-like parasites are polyphyletic and their similar morphologies emerged convergently at least three times. Gregarines and eugregarines are monophyletic, against most expectations, and rhytidocystids and Eleutheroschizon are sister lineages to medically important taxa. Although previously unrecognized, plastids in deep-branching apicomplexans are common, and they contain some of the most divergent and AT-rich genomes ever found. In eugregarines, however, plastids are either abnormally reduced or absent, thus increasing known plastid losses in eukaryotes from two to four. Environmental sequences of ten novel plastid lineages and structural innovations in plastid proteins confirm that plastids in apicomplexans and their relatives are widespread and share a common, photosynthetic origin.