Convergent evolution of lifestyles in close relatives of animals and fungi

genopisPublished in Current Biology

Phylogenomics Reveals Convergent Evolution of Lifestyles in Close Relatives of Animals and Fungi

Guifré Torruella, Alex de Mendoza, Xavier Grau-Bové, Meritxell Antó, Mark A. Chaplin, Javier del Campo, Laura Eme, Gregorio Pérez-Cordón, Christopher M. Whipps, Krista M. Nichols, Richard Paley, Andrew J. Roger, Ariadna Sitjà-Bobadilla, Stuart Donachie, Iñaki Ruiz-Trillo

The Opisthokonta are a eukaryotic supergroup divided in two main lineages: animals and related protistan taxa, and fungi and their allies [1 and 2]. There is a great diversity of lifestyles and morphologies among unicellular opisthokonts, from free-living phagotrophic flagellated bacterivores and filopodiated amoebas to cell-walled osmotrophic parasites and saprotrophs. However, these characteristics do not group into monophyletic assemblages, suggesting rampant convergent evolution within Opisthokonta. To test this hypothesis, we assembled a new phylogenomic dataset via sequencing 12 new strains of protists. Phylogenetic relationships among opisthokonts revealed independent origins of filopodiated amoebas in two lineages, one related to fungi and the other to animals. Moreover, we observed that specialized osmotrophic lifestyles evolved independently in fungi and protistan relatives of animals, indicating convergent evolution. We therefore analyzed the evolution of two key fungal characters in Opisthokonta, the flagellum and chitin synthases. Comparative analyses of the flagellar toolkit showed a previously unnoticed flagellar apparatus in two close relatives of animals, the filasterean Ministeria vibrans and Corallochytrium limacisporum. This implies that at least four different opisthokont lineages secondarily underwent flagellar simplification. Analysis of the evolutionary history of chitin synthases revealed significant expansions in both animals and fungi, and also in the Ichthyosporea and C. limacisporum, a group of cell-walled animal relatives. This indicates that the last opisthokont common ancestor had a complex toolkit of chitin synthases that was differentially retained in extant lineages. Thus, our data provide evidence for convergent evolution of specialized lifestyles in close relatives of animals and fungi from a generalist ancestor.

From photosynthetic algae to obligate intracellular parasites

F5.largePublished in eLife

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

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.

Diversity and distribution of marine unicellular opisthokonts


Published in Environmental Microbiology

Diversity and distribution of unicellular opisthokonts along the European coast analysed using high-throughput sequencing

Javier del Campo, Diego Mallo, Ramon Massana, Colomban de Vargas, Thomas A. Richards and Iñaki Ruiz-Trillo

The opisthokonts are one of the major super groups of eukaryotes. It comprises two major clades: (i) the Metazoa and their unicellular relatives and (ii) the Fungi and their unicellular relatives. There is, however, little knowledge of the role of opisthokont microbes in many natural environments, especially among non-metazoan and non-fungal opisthokonts. Here, we begin to address this gap by analysing high-throughput 18S rDNA and 18S rRNA sequencing data from different European coastal sites, sampled at different size fractions and depths. In particular, we analyse the diversity and abundance of choanoflagellates, filastereans, ichthyosporeans, nucleariids, corallochytreans and their related lineages. Our results show the great diversity of choanoflagellates in coastal waters as well as a relevant representation of the ichthyosporeans and the uncultured marine opisthokonts (MAOP). Furthermore, we describe a new lineage of marine fonticulids (MAFO) that appears to be abundant in sediments. Taken together, our work points to a greater potential ecological role for unicellular opisthokonts than previously appreciated in marine environments, both in water column and sediments, and also provides evidence of novel opisthokont phylogenetic lineages. This study highlights the importance of high-throughput sequencing approaches to unravel the diversity and distribution of both known and novel eukaryotic lineages.