Endosymbiotic relationships between eukaryotic and prokaryotic cells are common in nature. Endosymbioses between two eukaryotes are also known; cyanobacterium-derived plastids have spread horizontally when one eukaryote assimilated another. A unique instance of a non-photosynthetic, eukaryotic endosymbiont involves members of the genus Paramoeba, amoebozoans that infect marine animals such as farmed fish and sea urchins. Paramoeba species harbor endosymbionts belonging to the Kinetoplastea, a diverse group of flagellate protists including some that cause devastating diseases. To elucidate the nature of this eukaryote-eukaryote association, we sequenced the genomes and transcriptomes of Paramoeba pemaquidensis and its endosymbiont Perkinsela sp. The endosymbiont nuclear genome is ~9.5 Mbp in size, the smallest of a kinetoplastid thus far discovered. Genomic analyses show that Perkinsela sp. has lost the ability to make a flagellum but retains hallmark features of kinetoplastid biology, including polycistronic transcription, trans-splicing, and a glycosome-like organelle. Mosaic biochemical pathways suggest extensive 'cross-talk' between the two organisms, and electron microscopy shows that the endosymbiont ingests amoeba cytoplasm, a novel form of endosymbiont-host communication. Our data reveal the cell biological and biochemical basis of the obligate relationship between Perkinsela sp. and its amoeba host, and provide a foundation for understanding pathogenicity determinants in economically important Paramoeba.

Canadian Institute for Advanced Research Program in Integrated Microbial Biodiversity Toronto Canada

Center for Computational Sciences University of Tsukuba Tsukuba Japan

Centre for Comparative Genomics and Evolutionary Bioinformatics Dalhousie University Halifax Nova Scotia Canada

Department of Biochemistry and Molecular Biology Dalhousie University Halifax Nova Scotia Canada

Department of Plant Sciences University of Oxford Oxford United Kingdom

Department of Zoology National Museum of Nature and Science Tsukuba Japan

Faculty of Sciences University of South Bohemia České Budějovice Czech Republic

Graduate School of Life and Environmental Sciences University of Tsukuba Tsukuba Japan

Graduate School of Life Sciences Tohoku University Tohoku Japan

Institute for Marine and Antarctic Sciences University of Tasmania Launceston Australia

Institute of Parasitology Biology Centre Czech Academy of Sciences České Budějovice Czech Republic

Laboratory for Cell Biology Philipps University Marburg Germany

Life Science Research Centre Faculty of Science University of Ostrava Ostrava Czech Republic

National Institute of Advanced Industrial Science and Technology Tsukuba Japan

Sir William Dunn School of Pathology University of Oxford Oxford United Kingdom

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Comprehensive analysis of the Kinetoplastea intron landscape reveals a novel intron-containing gene and the first exclusively trans-splicing eukaryote

A lineage-specific protein network at the trypanosome nuclear envelope

Distribution of Merlin in eukaryotes and first report of DNA transposons in kinetoplastid protists

Euglenozoa: taxonomy, diversity and ecology, symbioses and viruses

Inventory and Evolution of Mitochondrion-localized Family A DNA Polymerases in Euglenozoa

Evolution of metabolic capabilities and molecular features of diplonemids, kinetoplastids, and euglenids

Massive mitochondrial DNA content in diplonemid and kinetoplastid protists