title: Chromerid genomes reveal the evolutionary path from photosynthetic algae to obligate intracellular parasites.
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.
authors.affiliation: Pathogen Genomics Laboratory, Biological and Environmental Sciences and Engineering Division, King Abdullah University of Science and Technology, Thuwal, Saudi Arabia.
authors.forename: Yong H
authors.identifier: http://orcid.org/0000-0002-0338-6493
authors.initials: YH
authors.lastname: Woo
authors.affiliation: Pathogen Genomics Laboratory, Biological and Environmental Sciences and Engineering Division, King Abdullah University of Science and Technology, Thuwal, Saudi Arabia.
authors.forename: Hifzur
authors.initials: H
authors.lastname: Ansari
authors.affiliation: Parasite Genomics, Wellcome Trust Sanger Institute, Wellcome Trust Genome Campus, Cambridge, United Kingdom.
authors.forename: Thomas D
authors.initials: TD
authors.lastname: Otto
authors.affiliation: Department of Cell Biology, University of Alberta, Edmonton, Canada.
authors.forename: Christen M
authors.initials: CM
authors.lastname: Klinger
authors.affiliation: Canadian Institute for Advanced Research, Department of Botany, University of British Columbia, Vancouver, Canada.
authors.forename: Martin
authors.initials: M
authors.lastname: Kolisko
authors.affiliation: Institute of Parasitology, Biology Centre, Czech Academy of Sciences, České Budějovice, Czech Republic.
authors.forename: Jan
authors.initials: J
authors.lastname: Michálek
authors.affiliation: Pathogen Genomics Laboratory, Biological and Environmental Sciences and Engineering Division, King Abdullah University of Science and Technology, Thuwal, Saudi Arabia.
authors.forename: Alka
authors.initials: A
authors.lastname: Saxena
authors.affiliation: Biochemical Sciences Division, CSIR National Chemical Laboratory, Pune, India.
authors.forename: Dhanasekaran
authors.initials: D
authors.lastname: Shanmugam
authors.affiliation: Pathogen Genomics Laboratory, Biological and Environmental Sciences and Engineering Division, King Abdullah University of Science and Technology, Thuwal, Saudi Arabia.
authors.forename: Annageldi
authors.initials: A
authors.lastname: Tayyrov
authors.affiliation: Ecology and Evolutionary Biology Section, Institut de Biologie de l'Ecole Normale Supérieure, CNRS UMR8197 INSERM U1024, Paris, France.
authors.forename: Alaguraj
authors.initials: A
authors.lastname: Veluchamy
authors.affiliation: Bioscience Core Laboratory, King Abdullah University of Science and Technology, Thuwal, Saudi Arabia.
authors.forename: Shahjahan
authors.initials: S
authors.lastname: Ali
authors.affiliation: Department of Biology, University of Pennsylvania, Philadelphia, United States.
authors.forename: Axel
authors.initials: A
authors.lastname: Bernal
authors.affiliation: Canadian Institute for Advanced Research, Department of Botany, University of British Columbia, Vancouver, Canada.
authors.forename: Javier
authors.identifier: http://orcid.org/0000-0002-5292-1421
authors.initials: J
authors.lastname: del Campo
authors.affiliation: Institute of Parasitology, Biology Centre, Czech Academy of Sciences, České Budějovice, Czech Republic.
authors.forename: Jaromír
authors.initials: J
authors.lastname: Cihlář
authors.affiliation: Institute of Parasitology, Biology Centre, Czech Academy of Sciences, České Budějovice, Czech Republic.
authors.forename: Pavel
authors.initials: P
authors.lastname: Flegontov
authors.affiliation: School of Botany, University of Melbourne, Parkville, Australia.
authors.forename: Sebastian G
authors.initials: SG
authors.lastname: Gornik
authors.affiliation: Institute of Parasitology, Biology Centre, Czech Academy of Sciences, České Budějovice, Czech Republic.
authors.forename: Eva
authors.initials: E
authors.lastname: Hajdušková
authors.affiliation: Institute of Parasitology, Biology Centre, Czech Academy of Sciences, České Budějovice, Czech Republic.
authors.forename: Aleš
authors.initials: A
authors.lastname: Horák
authors.affiliation: Canadian Institute for Advanced Research, Department of Botany, University of British Columbia, Vancouver, Canada.
authors.forename: Jan
authors.initials: J
authors.lastname: Janouškovec
authors.affiliation: School of Botany, University of Melbourne, Parkville, Australia.
authors.forename: Nicholas J
authors.initials: NJ
authors.lastname: Katris
authors.affiliation: Seattle Biomedical Research Institute, Seattle, United States.
authors.forename: Fred D
authors.initials: FD
authors.lastname: Mast
authors.affiliation: Centro de Biología Molecular Severo Ochoa, CSIC/Universidad Autónoma de Madrid, Madrid, Spain.
authors.forename: Diego
authors.initials: D
authors.lastname: Miranda-Saavedra
authors.affiliation: Centre for GeoGenetics, Natural History Museum of Denmark, University of Copenhagen, Copenhagen, Denmark.
authors.forename: Tobias
authors.initials: T
authors.lastname: Mourier
authors.affiliation: Pathogen Genomics Laboratory, Biological and Environmental Sciences and Engineering Division, King Abdullah University of Science and Technology, Thuwal, Saudi Arabia.
authors.forename: Raeece
authors.initials: R
authors.lastname: Naeem
authors.affiliation: Pathogen Genomics Laboratory, Biological and Environmental Sciences and Engineering Division, King Abdullah University of Science and Technology, Thuwal, Saudi Arabia.
authors.forename: Mridul
authors.initials: M
authors.lastname: Nair
authors.affiliation: Bioscience Core Laboratory, King Abdullah University of Science and Technology, Thuwal, Saudi Arabia.
authors.forename: Aswini K
authors.initials: AK
authors.lastname: Panigrahi
authors.affiliation: European Bioinformatics Institute (EMBL-EBI), Wellcome Genome Campus, Hinxton, Cambridge, United Kingdom.
authors.forename: Neil D
authors.initials: ND
authors.lastname: Rawlings
authors.affiliation: Pathogen Genomics Laboratory, Biological and Environmental Sciences and Engineering Division, King Abdullah University of Science and Technology, Thuwal, Saudi Arabia.
authors.forename: Eriko
authors.initials: E
authors.lastname: Padron-Regalado
authors.affiliation: Pathogen Genomics Laboratory, Biological and Environmental Sciences and Engineering Division, King Abdullah University of Science and Technology, Thuwal, Saudi Arabia.
authors.forename: Abhinay
authors.initials: A
authors.lastname: Ramaprasad
authors.affiliation: School of Botany, University of Melbourne, Parkville, Australia.
authors.forename: Nadira
authors.initials: N
authors.lastname: Samad
authors.affiliation: Institute of Parasitology, Biology Centre, Czech Academy of Sciences, České Budějovice, Czech Republic.
authors.forename: Aleš
authors.initials: A
authors.lastname: Tomčala
authors.affiliation: 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.
authors.forename: Jon
authors.initials: J
authors.lastname: Wilkes
authors.affiliation: Broad Genome Sequencing and Analysis Program, Broad Institute of MIT and Harvard, Cambridge, United States.
authors.forename: Daniel E
authors.initials: DE
authors.lastname: Neafsey
authors.affiliation: Department of Microbiology, Monash University, Clayton, Australia.
authors.forename: Christian
authors.initials: C
authors.lastname: Doerig
authors.affiliation: Ecology and Evolutionary Biology Section, Institut de Biologie de l'Ecole Normale Supérieure, CNRS UMR8197 INSERM U1024, Paris, France.
authors.forename: Chris
authors.initials: C
authors.lastname: Bowler
authors.affiliation: Canadian Institute for Advanced Research, Department of Botany, University of British Columbia, Vancouver, Canada.
authors.forename: Patrick J
authors.initials: PJ
authors.lastname: Keeling
authors.affiliation: Department of Biology, University of Pennsylvania, Philadelphia, United States.
authors.forename: David S
authors.initials: DS
authors.lastname: Roos
authors.affiliation: Department of Cell Biology, University of Alberta, Edmonton, Canada.
authors.forename: Joel B
authors.initials: JB
authors.lastname: Dacks
authors.affiliation: Department of Microbiology and Immunology, Weill Cornell Medical College, New York, United States.
authors.forename: Thomas J
authors.initials: TJ
authors.lastname: Templeton
authors.affiliation: School of Botany, University of Melbourne, Parkville, Australia.
authors.forename: Ross F
authors.initials: RF
authors.lastname: Waller
authors.affiliation: Institute of Parasitology, Biology Centre, Czech Academy of Sciences, České Budějovice, Czech Republic.
authors.forename: Julius
authors.initials: J
authors.lastname: Lukeš
authors.affiliation: Institute of Parasitology, Biology Centre, Czech Academy of Sciences, České Budějovice, Czech Republic.
authors.forename: Miroslav
authors.initials: M
authors.lastname: Oborník
authors.affiliation: Pathogen Genomics Laboratory, Biological and Environmental Sciences and Engineering Division, King Abdullah University of Science and Technology, Thuwal, Saudi Arabia.
authors.forename: Arnab
authors.identifier: http://orcid.org/0000-0002-1755-2819
authors.initials: A
authors.lastname: Pain
mesh_terms: D056893:Alveolata / Q000235:genetics*; D048028:DNA, Algal / Q000737:chemistry* / Q000235:genetics*; D019143:Evolution, Molecular; D020869:Gene Expression Profiling; D008969:Molecular Sequence Data; D017422:Sequence Analysis, DNA
chemical_list: D048028:DNA, Algal
keywords: Chromera velia; Vitrella brassicaformis; evolution of parasitism; evolutionary biology; genomics; infectious disease; malaria; microbiology; toxoplasmosis