Genome sequencing reveals metabolic and cellular interdependence in an amoeba-kinetoplastid symbiosis

Goro Tanifuji, Ugo Cenci, Daniel Moog, Samuel Dean, Takuro Nakayama, Vojtěch David, Ivan Fiala, Bruce A. Curtis, Shannon J. Sibbald, Naoko T. Onodera, Morgan Colp, Pavel Flegontov, Jessica Johnson-Mackinnon, Michael McPhee, Yuji Inagaki, Tetsuo Hashimoto, Steven Kelly, Keith Gull, Julius Lukeš, John M. Archibald

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    24 Citations (Scopus)

    Abstract

    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.

    Original languageEnglish
    Article number11688
    JournalScientific reports
    Volume7
    Issue number1
    DOIs
    Publication statusPublished - 2017 Dec 1

    ASJC Scopus subject areas

    • General

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  • Cite this

    Tanifuji, G., Cenci, U., Moog, D., Dean, S., Nakayama, T., David, V., Fiala, I., Curtis, B. A., Sibbald, S. J., Onodera, N. T., Colp, M., Flegontov, P., Johnson-Mackinnon, J., McPhee, M., Inagaki, Y., Hashimoto, T., Kelly, S., Gull, K., Lukeš, J., & Archibald, J. M. (2017). Genome sequencing reveals metabolic and cellular interdependence in an amoeba-kinetoplastid symbiosis. Scientific reports, 7(1), [11688]. https://doi.org/10.1038/s41598-017-11866-x