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The Transcriptome of Paraphelidium Tribonemae Illuminates the Ancestry of Fungi and Opisthosporidia

59 Pages Posted: 10 Apr 2018 Sneak Peek Status: Under Review

See all articles by Guifré Torruella

Guifré Torruella

University of Paris-Saclay - Unité  d’Ecologie, Systématique  et  Evolution

Xavier Grau‐Bové

Universitat Pompeu Fabra - Institut de Biologia Evolutiva

David Moreira

University of Paris-Saclay - Unité  d’Ecologie, Systématique  et  Evolution

Sergey A. Karpov

University of Paris-Saclay - Unité  d’Ecologie, Systématique  et  Evolution

John A. Burns

American Museum of Natural History - Sackler Institute for Comparative Genomics

Arnau Sebé-Pedrós

Weizmann Institute of Science

Eckhard Völcker

Penard Laboratory

Purificación López‐García

University of Paris-Saclay - Unité  d’Ecologie, Systématique  et  Evolution

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Abstract

Aphelids constitute a group of diverse, yet poorly known, parasites of algae. Their life cycle and morphology resemble those of zoosporic fungi (chytrids) and rozellids (Cryptomycota/Rozellosporidia), another specious group of parasites of fungi and oomycetes. Unlike fungi, which are osmotrophs, aphelids and rozellids are phagotrophs, feeding on the host’s cytoplasm. Combined RNA polymerase and rRNA gene trees suggested that aphelids and rozellids relate to Microsporidia, extremely reduced parasites with remnant mitochondria. Accordingly, aphelids, rozellids and Microsporidia were proposed to form a monophyletic clade sister to Fungi, called Opisthosporidia. Microsporidia would have subsequently lost the ancestral opisthosporidian phagotrophy. However, the limited phylogenetic signal of those genes combined with microsporidian fast-evolving sequences have resulted in incongruent tree topologies, showing either rozellids or aphelids as the earliestbranching lineages of Opisthosporidia, and challenging their monophyly. We have generated the first transcriptome data for one aphelid species, Paraphelidium tribonemae. Multi-gene phylogenomic analyses clearly confirm the monophyly of Opisthosporidia, placing aphelids as the earliest branching opisthosporidian lineage. This is consistent with the rich proteome inferred for P. tribonemae, which includes cellulases likely involved in algal cell-wall penetration, enzymes involved in chitin biosynthesis and several metabolic pathways that were lost in the comparatively reduced Rozella allomycis genome. Contrary to recent claims suggesting a parasitic root for Fungi, our results suggest that Fungi and Opisthosporidia evolved from a free-living phagotrophic ancestor that became osmotrophic at the fungal root and evolved towards phagotrophic parasitism in the opisthosporidian line.

Suggested Citation

Torruella, Guifré and Grau‐Bové, Xavier and Moreira, David and Karpov, Sergey A. and Burns, John A. and Sebé-Pedrós, Arnau and Völcker, Eckhard and López‐García, Purificación, The Transcriptome of Paraphelidium Tribonemae Illuminates the Ancestry of Fungi and Opisthosporidia (2018). Available at SSRN: https://ssrn.com/abstract=3155652 or http://dx.doi.org/10.2139/ssrn.3155652
This is a paper under consideration at Cell Press and has not been peer-reviewed.

Guifré Torruella

University of Paris-Saclay - Unité  d’Ecologie, Systématique  et  Evolution

Orsay
France

Xavier Grau‐Bové

Universitat Pompeu Fabra - Institut de Biologia Evolutiva

Barcelona, Catalonia
Spain

David Moreira

University of Paris-Saclay - Unité  d’Ecologie, Systématique  et  Evolution

Orsay
France

Sergey A. Karpov

University of Paris-Saclay - Unité  d’Ecologie, Systématique  et  Evolution

Orsay
France

John A. Burns

American Museum of Natural History - Sackler Institute for Comparative Genomics

New York, NY
United States

Arnau Sebé-Pedrós

Weizmann Institute of Science

Rehovot, 76100
Israel

Eckhard Völcker

Penard Laboratory

Cape Town, 7708
South Africa

Purificación López‐García (Contact Author)

University of Paris-Saclay - Unité  d’Ecologie, Systématique  et  Evolution ( email )

Orsay
France

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