Chromerid genomes reveal the evolutionary path from photosynthetic algae to obligate intracellular parasites

Yong Woo(King Abdullah University of Science and Technology), Hifzur Rahman Ansari(King Abdullah University of Science and Technology), Thomas D. Otto(Wellcome Sanger Institute), Christen M. Klinger(University of Alberta), Martin Kolísko(Canadian Institute for Advanced Research), Jan Michálek(University of South Bohemia in České Budějovice), Alka Saxena(King Abdullah University of Science and Technology), Dhanasekaran Shanmugam(National Chemical Laboratory), Annageldi Tayyrov(King Abdullah University of Science and Technology), Alaguraj Veluchamy(Centre National de la Recherche Scientifique), Shahjahan Ali(King Abdullah University of Science and Technology), Axel Bernal(University of Pennsylvania), Javier del Campo(Canadian Institute for Advanced Research), Jaromír Cihlář(University of South Bohemia in České Budějovice), Pavel Flegontov(University of Ostrava), Sebastian G. Gornik(The University of Melbourne), Eva Hajdušková(Institute of Parasitology), Aleš Horák(University of South Bohemia in České Budějovice), Jan Janouškovec(Canadian Institute for Advanced Research), Nicholas J Katris(The University of Melbourne), Fred D. Mast(Center for Infectious Disease Research), Diego Miranda‐Saavedra(IE University), Tobias Mourier(University of Copenhagen), Raeece Naeem(King Abdullah University of Science and Technology), Mridul Nair(King Abdullah University of Science and Technology), Aswini K. Panigrahi(King Abdullah University of Science and Technology), Neil D. Rawlings(European Bioinformatics Institute), Eriko Padron-Regalado(King Abdullah University of Science and Technology), Abhinay Ramaprasad(King Abdullah University of Science and Technology), Nadira Samad(The University of Melbourne), Aleš Tomčala(University of South Bohemia in České Budějovice), Jonathan Wilkes(Wellcome Centre for Molecular Parasitology), Daniel E. Neafsey(Broad Institute), Christian Doerig(Monash University), Chris Bowler(Centre National de la Recherche Scientifique), Patrick J. Keeling(Canadian Institute for Advanced Research), David S. Roos(University of Pennsylvania), Joel B. Dacks(University of Alberta), Thomas J. Templeton(Cornell University), Ross F. Waller(The University of Melbourne), Julius Lukeš(Canadian Institute for Advanced Research), Miroslav Obornı́k(Czech Academy of Sciences), Arnab Pain(King Abdullah University of Science and Technology)
eLife
July 14, 2015
10.7554/elife.06974
Cited by 327Open Access
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Abstract

The eukaryotic phylum Apicomplexa encompasses thousands of obligate intracellular parasites of humans and animals with immense socio-economic and health impacts. We sequenced nuclear genomes of Chromera velia and Vitrella brassicaformis, free-living non-parasitic photosynthetic algae closely related to apicomplexans. Proteins from key metabolic pathways and from the endomembrane trafficking systems associated with a free-living lifestyle have been progressively and non-randomly lost during adaptation to parasitism. The free-living ancestor contained a broad repertoire of genes many of which were repurposed for parasitic processes, such as extracellular proteins, components of a motility apparatus, and DNA- and RNA-binding protein families. Based on transcriptome analyses across 36 environmental conditions, Chromera orthologs of apicomplexan invasion-related motility genes were co-regulated with genes encoding the flagellar apparatus, supporting the functional contribution of flagella to the evolution of invasion machinery. This study provides insights into how obligate parasites with diverse life strategies arose from a once free-living phototrophic marine alga.

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