Euglenozoan kleptoplasty illuminates the early evolution of photoendosymbiosis

Proceedings of the National Academy of Sciences of the United States of America · 9 authors, 8 centres

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This laboratory study investigates the mixotrophic euglenozoan Rapaza viridis and its algal prey to model early plastid integration. The central result is that R. viridis lacks permanent plastids, instead using transient kleptoplasts while expressing nucleus-encoded proteins with targeting signals to the kleptoplasts.

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The study examines Rapaza viridis, a mixotrophic euglenozoan sister to photoautotrophic Euglenophyceae, as a model for the early evolution of plastid acquisition. Using time-course transmission electron microscopy, plastid genomics, and transcriptomics of R. viridis and its prey Tetraselmis sp., researchers found that R. viridis does not have canonical plastids. Instead, it acquires and maintains functional kleptoplasts transiently from ingested prey. The organism expresses a series of nucleus-encoded proteins with targeting signals homologous to those in Euglenophyceae, which are likely transported into the kleptoplasts.

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biomedical research

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ORIGINAL PAPER

PMC10041101

Euglenozoan kleptoplasty illuminates the early evolution of photoendosymbiosis

Proceedings of the National Academy of Sciences of the United States of America

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ABSTRACT

Significance The integration of fully established plastids involved horizontal transfer of chloroplast-associated genes to the host genome. Analyses of the euglenozoan Rapaza viridis , however, demonstrated that the proteins associated with its kleptoplasts (kP) are derived from diverse algae other than its kleptoplast donor. Some of them are shared with the plastid-targeted proteins of its sister lineage, Euglenophyceae, whose canonical plastid originated from a distinct green alga. The gradual accumulation of repeated horizontal gene transfer events constructed a genome in R. viridis that facilitates transient photosynthesis in the kleptoplasts. The mechanism for maintaining functionally active kleptoplasts in R. viridis provides context for understanding the early stages in the secondary endosymbiotic origin of plastids in euglenophytes and beyond. Keywords: endosymbiosis, horizontal gene transfer, kleptoplasty, plastid evolution, euglenozoa

CITATION EXPORT

Anna Karnkowska, Naoji Yubuki, Moe Maruyama et al.. Euglenozoan kleptoplasty illuminates the early evolution of photoendosymbiosis. Proceedings of the National Academy of Sciences of the United States of America. (2023). https://doi.org/10.1073/pnas.2220100120

AUTHORS

9 · 8 CENTRES

Anna Karnkowska, Naoji Yubuki, Moe Maruyama, Aika Yamaguchi, Yuichiro Kashiyama, Toshinobu Suzaki, Patrick J Keeling, Vladimír Hampl, Brian S Leander

aDepartment of Botany, Beaty Biodiversity Research Centre and Museum, University of British Columbia, Vancouver, BC V6T 1Z4, Canada
bDepartment of Parasitology, Faculty of Science, Charles University, BIOCEV, Prague 25250, Czech Republic
cInstitute of Evolutionary Biology, Biological and Chemical Research Centre, Faculty of Biology, University of Warsaw, 02-096, Warsaw, Poland
dDepartment of Applied Chemistry and Food Science, Faculty of Environmental and Information Sciences, Fukui University of Technology, Fukui 910-8505, Japan
eDepartment of Applied Science and Engineering, Graduate School of Engineering, Fukui University of Technology, Fukui 910-8505, Japan
fDepartment of Biological Sciences, Faculty of Science, Hokkaido University, Sapporo 060-0808, Japan
gDepartment of Biology, Graduate School of Science, Kobe University, Kobe 657-8501, Japan
hDepartment of Zoology, Beaty Biodiversity Research Centre and Museum, University of British Columbia, Vancouver, BC V6T 1Z4, Canada