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A free-living protist that lacks canonical eukaryotic DNA replication and segregation systems

View ORCID ProfileDayana E. Salas-Leiva, View ORCID ProfileEelco C. Tromer, View ORCID ProfileBruce A. Curtis, View ORCID ProfileJon Jerlström-Hultqvist, View ORCID ProfileMartin Kolisko, View ORCID ProfileZhenzhen Yi, View ORCID ProfileJoan S. Salas-Leiva, Lucie Gallot-Lavallée, View ORCID ProfileGeert J. P. L. Kops, View ORCID ProfileJohn M. Archibald, View ORCID ProfileAlastair G. B. Simpson, View ORCID ProfileAndrew J. Roger
doi: https://doi.org/10.1101/2021.03.14.435266
Dayana E. Salas-Leiva
1Centre for Comparative Genomics and Evolutionary Bioinformatics (CGEB), Department of Biochemistry and Molecular Biology, Dalhousie University, Halifax, NS, Canada, B3H 4R2
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Eelco C. Tromer
2Department of Biochemistry, University of Cambridge, Cambridge, United Kingdom
3Oncode Institute, Hubrecht Institute – KNAW (Royal Netherlands Academy of Arts and Sciences) and University Medical Centre Utrecht, Utrecht, The Netherlands
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Bruce A. Curtis
1Centre for Comparative Genomics and Evolutionary Bioinformatics (CGEB), Department of Biochemistry and Molecular Biology, Dalhousie University, Halifax, NS, Canada, B3H 4R2
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Jon Jerlström-Hultqvist
1Centre for Comparative Genomics and Evolutionary Bioinformatics (CGEB), Department of Biochemistry and Molecular Biology, Dalhousie University, Halifax, NS, Canada, B3H 4R2
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Martin Kolisko
4Institute of Parasitology Biology Centre, Czech Acad. Sci, České Budějovice, Czech Republic
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Zhenzhen Yi
5Guangzhou Key Laboratory of Subtropical Biodiversity and Biomonitoring, School of Life Science, South China Normal University, Guangzhou 510631, China
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Joan S. Salas-Leiva
6CONACyT-Centro de Investigación en Materiales Avanzados, Departamento de medio ambiente y energía, Miguel de Cervantes 120, Complejo Industrial Chihuahua, 31136 Chihuahua, Chih., México
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Lucie Gallot-Lavallée
1Centre for Comparative Genomics and Evolutionary Bioinformatics (CGEB), Department of Biochemistry and Molecular Biology, Dalhousie University, Halifax, NS, Canada, B3H 4R2
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Geert J. P. L. Kops
3Oncode Institute, Hubrecht Institute – KNAW (Royal Netherlands Academy of Arts and Sciences) and University Medical Centre Utrecht, Utrecht, The Netherlands
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John M. Archibald
1Centre for Comparative Genomics and Evolutionary Bioinformatics (CGEB), Department of Biochemistry and Molecular Biology, Dalhousie University, Halifax, NS, Canada, B3H 4R2
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Alastair G. B. Simpson
7Centre for Comparative Genomics and Evolutionary Bioinformatics (CGEB), Department of Biology, Dalhousie University, Halifax, NS, Canada, B3H 4R2
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Andrew J. Roger
1Centre for Comparative Genomics and Evolutionary Bioinformatics (CGEB), Department of Biochemistry and Molecular Biology, Dalhousie University, Halifax, NS, Canada, B3H 4R2
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  • For correspondence: Andrew.Roger@dal.ca
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Abstract

Cells must replicate and segregate their DNA with precision. In eukaryotes, these processes are part of a regulated cell-cycle that begins at S-phase with the replication of DNA and ends after M-phase. Previous studies showed that these processes were present in the last eukaryotic common ancestor and the core parts of their molecular systems are conserved across eukaryotic diversity. However, some unicellular parasites, such as the metamonad Giardia intestinalis, have secondarily lost components of the DNA processing and segregation apparatuses. To clarify the evolutionary history of these systems in these unusual eukaryotes, we generated a high-quality draft genome assembly for the free-living metamonad Carpediemonas membranifera and carried out a comparative genomics analysis. We found that parasitic and free-living metamonads harbor a conspicuously incomplete set of canonical proteins for processing and segregating DNA. Unexpectedly, Carpediemonas species are further streamlined, completely lacking the origin recognition complex, Cdc6 and other replisome components, most structural kinetochore subunits including the Ndc80 complex, as well as several canonical cell-cycle checkpoint proteins. Carpediemonas is the first eukaryote known to have lost this large suite of conserved complexes, suggesting that it has a highly unusual cell cycle and that unlike any other known eukaryote, it must rely on a novel set of mechanisms to carry out these fundamental processes.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • http://perun.biochem.dal.ca/downloads/dsalas/SuppInfo.tar.gz

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The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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A free-living protist that lacks canonical eukaryotic DNA replication and segregation systems
Dayana E. Salas-Leiva, Eelco C. Tromer, Bruce A. Curtis, Jon Jerlström-Hultqvist, Martin Kolisko, Zhenzhen Yi, Joan S. Salas-Leiva, Lucie Gallot-Lavallée, Geert J. P. L. Kops, John M. Archibald, Alastair G. B. Simpson, Andrew J. Roger
bioRxiv 2021.03.14.435266; doi: https://doi.org/10.1101/2021.03.14.435266
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A free-living protist that lacks canonical eukaryotic DNA replication and segregation systems
Dayana E. Salas-Leiva, Eelco C. Tromer, Bruce A. Curtis, Jon Jerlström-Hultqvist, Martin Kolisko, Zhenzhen Yi, Joan S. Salas-Leiva, Lucie Gallot-Lavallée, Geert J. P. L. Kops, John M. Archibald, Alastair G. B. Simpson, Andrew J. Roger
bioRxiv 2021.03.14.435266; doi: https://doi.org/10.1101/2021.03.14.435266

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