eLife (Jul 2015)
Chromerid genomes reveal the evolutionary path from photosynthetic algae to obligate intracellular parasites
- Yong H Woo,
- Hifzur Ansari,
- Thomas D Otto,
- Christen M Klinger,
- Martin Kolisko,
- Jan Michálek,
- Alka Saxena,
- Dhanasekaran Shanmugam,
- Annageldi Tayyrov,
- Alaguraj Veluchamy,
- Shahjahan Ali,
- Axel Bernal,
- Javier del Campo,
- Jaromír Cihlář,
- Pavel Flegontov,
- Sebastian G Gornik,
- Eva Hajdušková,
- Aleš Horák,
- Jan Janouškovec,
- Nicholas J Katris,
- Fred D Mast,
- Diego Miranda-Saavedra,
- Tobias Mourier,
- Raeece Naeem,
- Mridul Nair,
- Aswini K Panigrahi,
- Neil D Rawlings,
- Eriko Padron-Regalado,
- Abhinay Ramaprasad,
- Nadira Samad,
- Aleš Tomčala,
- Jon Wilkes,
- Daniel E Neafsey,
- Christian Doerig,
- Chris Bowler,
- Patrick J Keeling,
- David S Roos,
- Joel B Dacks,
- Thomas J Templeton,
- Ross F Waller,
- Julius Lukeš,
- Miroslav Oborník,
- Arnab Pain
Affiliations
- Yong H Woo
- ORCiD
- Pathogen Genomics Laboratory, Biological and Environmental Sciences and Engineering Division, King Abdullah University of Science and Technology, Thuwal, Saudi Arabia
- Hifzur Ansari
- Pathogen Genomics Laboratory, Biological and Environmental Sciences and Engineering Division, King Abdullah University of Science and Technology, Thuwal, Saudi Arabia
- Thomas D Otto
- Parasite Genomics, Wellcome Trust Sanger Institute, Wellcome Trust Genome Campus, Cambridge, United Kingdom
- Christen M Klinger
- Department of Cell Biology, University of Alberta, Edmonton, Canada
- Martin Kolisko
- Canadian Institute for Advanced Research, Department of Botany, University of British Columbia, Vancouver, Canada
- Jan Michálek
- Institute of Parasitology, Biology Centre, Czech Academy of Sciences, České Budějovice, Czech Republic; Faculty of Sciences, University of South Bohemia, České Budějovice, Czech Republic
- Alka Saxena
- Pathogen Genomics Laboratory, Biological and Environmental Sciences and Engineering Division, King Abdullah University of Science and Technology, Thuwal, Saudi Arabia
- Dhanasekaran Shanmugam
- Biochemical Sciences Division, CSIR National Chemical Laboratory, Pune, India
- Annageldi Tayyrov
- Pathogen Genomics Laboratory, Biological and Environmental Sciences and Engineering Division, King Abdullah University of Science and Technology, Thuwal, Saudi Arabia
- Alaguraj Veluchamy
- Ecology and Evolutionary Biology Section, Institut de Biologie de l'Ecole Normale Supérieure, CNRS UMR8197 INSERM U1024, Paris, France
- Shahjahan Ali
- Bioscience Core Laboratory, King Abdullah University of Science and Technology, Thuwal, Saudi Arabia
- Axel Bernal
- Department of Biology, University of Pennsylvania, Philadelphia, United States
- Javier del Campo
- ORCiD
- Canadian Institute for Advanced Research, Department of Botany, University of British Columbia, Vancouver, Canada
- Jaromír Cihlář
- Institute of Parasitology, Biology Centre, Czech Academy of Sciences, České Budějovice, Czech Republic; Faculty of Sciences, University of South Bohemia, České Budějovice, Czech Republic
- Pavel Flegontov
- Institute of Parasitology, Biology Centre, Czech Academy of Sciences, České Budějovice, Czech Republic; Life Science Research Centre, Faculty of Science, University of Ostrava, Ostrava, Czech Republic
- Sebastian G Gornik
- School of Botany, University of Melbourne, Parkville, Australia
- Eva Hajdušková
- Institute of Parasitology, Biology Centre, Czech Academy of Sciences, České Budějovice, Czech Republic
- Aleš Horák
- Institute of Parasitology, Biology Centre, Czech Academy of Sciences, České Budějovice, Czech Republic; Faculty of Sciences, University of South Bohemia, České Budějovice, Czech Republic
- Jan Janouškovec
- Canadian Institute for Advanced Research, Department of Botany, University of British Columbia, Vancouver, Canada
- Nicholas J Katris
- School of Botany, University of Melbourne, Parkville, Australia
- Fred D Mast
- Seattle Biomedical Research Institute, Seattle, United States
- Diego Miranda-Saavedra
- Centro de Biología Molecular Severo Ochoa, CSIC/Universidad Autónoma de Madrid, Madrid, Spain; IE Business School, IE University, Madrid, Spain
- Tobias Mourier
- Centre for GeoGenetics, Natural History Museum of Denmark, University of Copenhagen, Copenhagen, Denmark
- Raeece Naeem
- Pathogen Genomics Laboratory, Biological and Environmental Sciences and Engineering Division, King Abdullah University of Science and Technology, Thuwal, Saudi Arabia
- Mridul Nair
- Pathogen Genomics Laboratory, Biological and Environmental Sciences and Engineering Division, King Abdullah University of Science and Technology, Thuwal, Saudi Arabia
- Aswini K Panigrahi
- Bioscience Core Laboratory, King Abdullah University of Science and Technology, Thuwal, Saudi Arabia
- Neil D Rawlings
- European Bioinformatics Institute (EMBL-EBI), Wellcome Genome Campus, Hinxton, Cambridge, United Kingdom
- Eriko Padron-Regalado
- Pathogen Genomics Laboratory, Biological and Environmental Sciences and Engineering Division, King Abdullah University of Science and Technology, Thuwal, Saudi Arabia
- Abhinay Ramaprasad
- Pathogen Genomics Laboratory, Biological and Environmental Sciences and Engineering Division, King Abdullah University of Science and Technology, Thuwal, Saudi Arabia
- Nadira Samad
- School of Botany, University of Melbourne, Parkville, Australia
- Aleš Tomčala
- Institute of Parasitology, Biology Centre, Czech Academy of Sciences, České Budějovice, Czech Republic; Faculty of Sciences, University of South Bohemia, České Budějovice, Czech Republic
- Jon Wilkes
- 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
- Daniel E Neafsey
- Broad Genome Sequencing and Analysis Program, Broad Institute of MIT and Harvard, Cambridge, United States
- Christian Doerig
- Department of Microbiology, Monash University, Clayton, Australia
- Chris Bowler
- Ecology and Evolutionary Biology Section, Institut de Biologie de l'Ecole Normale Supérieure, CNRS UMR8197 INSERM U1024, Paris, France
- Patrick J Keeling
- Canadian Institute for Advanced Research, Department of Botany, University of British Columbia, Vancouver, Canada
- David S Roos
- Department of Biology, University of Pennsylvania, Philadelphia, United States
- Joel B Dacks
- Department of Cell Biology, University of Alberta, Edmonton, Canada
- Thomas J Templeton
- Department of Microbiology and Immunology, Weill Cornell Medical College, New York, United States; Department of Protozoology, Institute of Tropical Medicine, Nagasaki University, Nagasaki, Japan
- Ross F Waller
- School of Botany, University of Melbourne, Parkville, Australia; Department of Biochemistry, University of Cambridge, Cambridge, United Kingdom
- Julius Lukeš
- Institute of Parasitology, Biology Centre, Czech Academy of Sciences, České Budějovice, Czech Republic; Faculty of Sciences, University of South Bohemia, České Budějovice, Czech Republic; Canadian Institute for Advanced Research, Toronto, Canada
- Miroslav Oborník
- Institute of Parasitology, Biology Centre, Czech Academy of Sciences, České Budějovice, Czech Republic; Faculty of Sciences, University of South Bohemia, České Budějovice, Czech Republic; Institute of Microbiology, Czech Academy of Sciences, České Budějovice, Czech Republic
- Arnab Pain
- ORCiD
- Pathogen Genomics Laboratory, Biological and Environmental Sciences and Engineering Division, King Abdullah University of Science and Technology, Thuwal, Saudi Arabia
- DOI
- https://doi.org/10.7554/eLife.06974
- Journal volume & issue
-
Vol. 4
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.
Keywords
