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

YH. Woo, H. Ansari, TD. Otto, CM. Klinger, M. Kolisko, J. Michálek, A. Saxena, D. Shanmugam, A. Tayyrov, A. Veluchamy, S. Ali, A. Bernal, J. del Campo, J. Cihlář, P. Flegontov, SG. Gornik, E. Hajdušková, A. Horák, J. Janouškovec, NJ. Katris, FD....

. 2015 ; 4 (-) : e06974. [pub] 20150715

Language English Country England, Great Britain

Document type Journal Article, Research Support, N.I.H., Extramural, Research Support, Non-U.S. Gov't

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.

Biochemical Sciences Division CSIR National Chemical Laboratory Pune India

Bioscience Core Laboratory King Abdullah University of Science and Technology Thuwal Saudi Arabia

Broad Genome Sequencing and Analysis Program Broad Institute of MIT and Harvard Cambridge United States

Canadian Institute for Advanced Research Department of Botany University of British Columbia Vancouver Canada

Centre for GeoGenetics Natural History Museum of Denmark University of Copenhagen Copenhagen Denmark

Centro de Biología Molecular Severo Ochoa CSIC Universidad Autónoma de Madrid Madrid Spain

Department of Biology University of Pennsylvania Philadelphia United States

Department of Cell Biology University of Alberta Edmonton Canada

Department of Microbiology and Immunology Weill Cornell Medical College New York United States

Department of Microbiology Monash University Clayton Australia

Ecology and Evolutionary Biology Section Institut de Biologie de l'Ecole Normale Supérieure CNRS UMR8197 INSERM U1024 Paris France

European Bioinformatics Institute Wellcome Genome Campus Hinxton Cambridge United Kingdom

Institute of Parasitology Biology Centre Czech Academy of Sciences České Budějovice Czech Republic

Parasite Genomics Wellcome Trust Sanger Institute Wellcome Trust Genome Campus Cambridge United Kingdom

Pathogen Genomics Laboratory Biological and Environmental Sciences and Engineering Division King Abdullah University of Science and Technology Thuwal Saudi Arabia

School of Botany University of Melbourne Parkville Australia

Seattle Biomedical Research Institute Seattle United States

Wellcome Trust Centre For Molecular Parasitology Institute of Infection Immunity and Inflammation College of Medical Veterinary and Life Sciences University of Glasgow Glasgow United Kingdom

References provided by Crossref.org

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$a 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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