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

Author:

Woo Yong H1ORCID,Ansari Hifzur1,Otto Thomas D2,Klinger Christen M3,Kolisko Martin4,Michálek Jan56,Saxena Alka1,Shanmugam Dhanasekaran7,Tayyrov Annageldi1,Veluchamy Alaguraj8,Ali Shahjahan9,Bernal Axel10,del Campo Javier4ORCID,Cihlář Jaromír56,Flegontov Pavel511,Gornik Sebastian G12,Hajdušková Eva5,Horák Aleš56,Janouškovec Jan4,Katris Nicholas J12,Mast Fred D13,Miranda-Saavedra Diego1415,Mourier Tobias16,Naeem Raeece1,Nair Mridul1,Panigrahi Aswini K9,Rawlings Neil D17,Padron-Regalado Eriko1,Ramaprasad Abhinay1,Samad Nadira12,Tomčala Aleš56,Wilkes Jon18,Neafsey Daniel E19,Doerig Christian20,Bowler Chris8,Keeling Patrick J4,Roos David S10,Dacks Joel B3,Templeton Thomas J2122,Waller Ross F1223,Lukeš Julius5624,Oborník Miroslav5625,Pain Arnab1ORCID

Affiliation:

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

2. Parasite Genomics, Wellcome Trust Sanger Institute, Wellcome Trust Genome Campus, Cambridge, United Kingdom

3. Department of Cell Biology, University of Alberta, Edmonton, Canada

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

5. Institute of Parasitology, Biology Centre, Czech Academy of Sciences, České Budějovice, Czech Republic

6. Faculty of Sciences, University of South Bohemia, České Budějovice, Czech Republic

7. Biochemical Sciences Division, CSIR National Chemical Laboratory, Pune, India

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

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

10. Department of Biology, University of Pennsylvania, Philadelphia, United States

11. Life Science Research Centre, Faculty of Science, University of Ostrava, Ostrava, Czech Republic

12. School of Botany, University of Melbourne, Parkville, Australia

13. Seattle Biomedical Research Institute, Seattle, United States

14. Centro de Biología Molecular Severo Ochoa, CSIC/Universidad Autónoma de Madrid, Madrid, Spain

15. IE Business School, IE University, Madrid, Spain

16. Centre for GeoGenetics, Natural History Museum of Denmark, University of Copenhagen, Copenhagen, Denmark

17. European Bioinformatics Institute (EMBL-EBI), Wellcome Genome Campus, Hinxton, Cambridge, United Kingdom

18. 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

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

20. Department of Microbiology, Monash University, Clayton, Australia

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

22. Department of Protozoology, Institute of Tropical Medicine, Nagasaki University, Nagasaki, Japan

23. Department of Biochemistry, University of Cambridge, Cambridge, United Kingdom

24. Canadian Institute for Advanced Research, Toronto, Canada

25. Institute of Microbiology, Czech Academy of Sciences, České Budějovice, Czech Republic

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.

Funder

King Abdullah University of Science and Technology (KAUST)

Council of Scientific and Industrial Research

National Institute of Allergy and Infectious Diseases (NIAID)

Australian Research Council (ARC)

Monash University

National Health and Medical Research Council (NHMRC)

Czech Science Foundation (Grantová agentura Ceské republiky)

Publisher

eLife Sciences Publications, Ltd

Subject

General Immunology and Microbiology,General Biochemistry, Genetics and Molecular Biology,General Medicine,General Neuroscience

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