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

Yong Woo ,Raeece Naeem,Javier Del Campo,Christian Doerig,Miroslav Oborník,Jaromír Cihlář,Alka Saxena,Eriko Padron-Regalado,Arnab Pain,Julius Lukeš,Chris Bowler,Eva Hajdušková,Pavel Flegontov,Annageldi Tayyrov,Jan Janouškovec,Aleš Horák,Tobias Mourier,Nadira Samad,Dhanasekaran Shanmugam,Abhinay Ramaprasad,Alaguraj Veluchamy,Axel Bernal,Shahjahan Ali,Aleš Tomčala,Mridul Nair,Jan Michálek,Christen M Klinger ,Patrick J Keeling ,Sebastian G Gornik ,Ross F Waller ,Joel B Dacks ,Diego Miranda‐Saavedra ,Thomas J Templeton ,Aswini K Panigrahi ,David S Roos ,Fred D Mast ,Hifzur Rahman Ansari ,Martin Kolísko ,Daniel E Neafsey ,Jonathan M Wilkes ,Neil D Rawlings ,Thomas D Otto ,Nicholas J Katris

doi:10.7554/elife.06974

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.

Highlights

The phylum Apicomplexa is comprised of eukaryotic, unicellular, obligate intracellular parasites, infecting a diverse range of hosts from marine invertebrates, amphibians, reptiles, birds to mammals including humans
Genomics and evolutionary biology | Microbiology and infectious disease proteins with regulatory functions in parasitic processes (Campbell et al, 2010; Flueck et al, 2010; Radke et al, 2013; Kafsack et al, 2014; Sinha et al, 2014), extracellular proteins for interactions with the host (Templeton et al, 2004a; Anantharaman et al, 2007), an apical complex comprising a system of cytoskeletal elements and secretory organelles (Hu et al, 2006), an inner membrane complex (IMC) derived from the alveoli (Eisen et al, 2006; Kono et al, 2012; Shoguchi et al, 2013), and a nonphotosynthetic secondary plastid, termed the apicoplast (McFadden et al, 1996)
We explored whole nuclear genomes of Chromera and Vitrella to understand how obligate intracellular parasitism has evolved in Apicomplexa

Summary

Introduction

The phylum Apicomplexa is comprised of eukaryotic, unicellular, obligate intracellular parasites, infecting a diverse range of hosts from marine invertebrates, amphibians, reptiles, birds to mammals including humans. Genomics and evolutionary biology | Microbiology and infectious disease proteins with regulatory functions in parasitic processes (Campbell et al, 2010; Flueck et al, 2010; Radke et al, 2013; Kafsack et al, 2014; Sinha et al, 2014), extracellular proteins for interactions with the host (Templeton et al, 2004a; Anantharaman et al, 2007), an apical complex comprising a system of cytoskeletal elements and secretory organelles (Hu et al, 2006), an inner membrane complex (IMC) derived from the alveoli (Eisen et al, 2006; Kono et al, 2012; Shoguchi et al, 2013), and a nonphotosynthetic secondary plastid, termed the apicoplast (McFadden et al, 1996) How and when these features arose is unclear, owing to the lack of suitable outgroup species for comparative analyses.

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Conclusion