Chimeric origins of ochrophytes and haptophytes revealed through an ancient plastid proteome

Author:

Dorrell Richard G1ORCID,Gile Gillian2,McCallum Giselle1,Méheust Raphaël3ORCID,Bapteste Eric P3,Klinger Christen M4,Brillet-Guéguen Loraine5,Freeman Katalina D2,Richter Daniel J67ORCID,Bowler Chris1ORCID

Affiliation:

1. IBENS, Département de Biologie, École Normale Supérieure, CNRS, Inserm, PSL Research University, Paris, France

2. School of Life Sciences, Arizona State University, Tempe, United States

3. Institut de Biologie Paris-Seine, Université Pierre et Marie Curie, Paris, France

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

5. CNRS, UPMC, FR2424, ABiMS, Station Biologique, Roscoff, France

6. Sorbonne Universités, Université Pierre et Marie Curie, CNRS UMR 7144

7. Adaptation et Diversité en Milieu Marin, Équipe EPEP, Station Biologique de Roscoff, Roscoff, France

Abstract

Plastids are supported by a wide range of proteins encoded within the nucleus and imported from the cytoplasm. These plastid-targeted proteins may originate from the endosymbiont, the host, or other sources entirely. Here, we identify and characterise 770 plastid-targeted proteins that are conserved across the ochrophytes, a major group of algae including diatoms, pelagophytes and kelps, that possess plastids derived from red algae. We show that the ancestral ochrophyte plastid proteome was an evolutionary chimera, with 25% of its phylogenetically tractable nucleus-encoded proteins deriving from green algae. We additionally show that functional mixing of host and plastid proteomes, such as through dual-targeting, is an ancestral feature of plastid evolution. Finally, we detect a clear phylogenetic signal from one ochrophyte subgroup, the lineage containing pelagophytes and dictyochophytes, in plastid-targeted proteins from another major algal lineage, the haptophytes. This may represent a possible serial endosymbiosis event deep in eukaryotic evolutionary history.

Funder

EMBO

European Research Council

Institut de France

Seventh Framework Programme

Gordon and Betty Moore Foundation

Paris Sciences et Lettres, Labex-MemoLife

Agence Nationale de la Recherche

Publisher

eLife Sciences Publications, Ltd

Subject

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

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