TY - JOUR
T1 - Genome sequencing reveals metabolic and cellular interdependence in an amoeba-kinetoplastid symbiosis
AU - Tanifuji, Goro
AU - Cenci, Ugo
AU - Moog, Daniel
AU - Dean, Samuel
AU - Nakayama, Takuro
AU - David, Vojtěch
AU - Fiala, Ivan
AU - Curtis, Bruce A.
AU - Sibbald, Shannon J.
AU - Onodera, Naoko T.
AU - Colp, Morgan
AU - Flegontov, Pavel
AU - Johnson-Mackinnon, Jessica
AU - McPhee, Michael
AU - Inagaki, Yuji
AU - Hashimoto, Tetsuo
AU - Kelly, Steven
AU - Gull, Keith
AU - Lukeš, Julius
AU - Archibald, John M.
N1 - Funding Information:
This work was supported by an operating grant awarded to J.M. Archibald from the Canadian Institutes of Health Research (MOP-115141) and the Czech Grant Agency (14-23986S) and ERC CZ (LL1601) to J. Lukeš. G. Tanifuji and B.A. Curtis were supported by the Tula Foundation (via Dalhousie’s Centre for Comparative Genomics and Evolutionary Bioinformatics). S. Dean and K. Gull were supported by the Wellcome Trust (092201/Z/10/Z, WT066839MA and 104627/Z/14/Z) and P. Flegontov was supported by the Institution Development Program of the University of Ostrava. J.M. Archibald and J. Lukeš are members of the Canadian Institute for Advanced Research, Program in Integrated Microbial Biodiversity. We are grateful to two anonymous reviewers and an Editorial Board Member for helpful comments on an earlier version of this paper. We thank Kanehisa Laboratories for permission to present KEGG metabolic pathway maps. We also thank M. Dlutek, E. Kim and J. Vaněček for technical assistance, and Andrew Jackson and Matthew Berriman for permission to analyze the Bodo saltans genome prior to publication.
Publisher Copyright:
© 2017 The Author(s).
PY - 2017/12/1
Y1 - 2017/12/1
N2 - 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.
AB - 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.
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U2 - 10.1038/s41598-017-11866-x
DO - 10.1038/s41598-017-11866-x
M3 - Article
C2 - 28916813
AN - SCOPUS:85029498112
VL - 7
JO - Scientific Reports
JF - Scientific Reports
SN - 2045-2322
IS - 1
M1 - 11688
ER -