Cells replicate and segregate their DNA with precision. Previous studies showed that these regulated cell-cycle processes were present in the last eukaryotic common ancestor and that their core molecular parts are conserved across eukaryotes. However, some metamonad parasites 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 genome assembly for the free-living metamonad Carpediemonas membranifera and carried out a comparative genomics analysis. Here, we show that parasitic and free-living metamonads harbor an incomplete set of proteins for processing and segregating DNA. Unexpectedly, Carpediemonas species are further streamlined, lacking the origin recognition complex, Cdc6 and most structural kinetochore subunits. Carpediemonas species are thus the first known eukaryotes that appear to lack this suite of conserved complexes, suggesting that they likely rely on yet-to-be-discovered or alternative mechanisms to carry out these fundamental processes.

CONACyT Centro de Investigación en Materiales Avanzados Departamento de medio ambiente y energía Miguel de Cervantes 120 Complejo Industrial Chihuahua 31136 Chihuahua Chih México

Department of Biochemistry University of Cambridge Cambridge United Kingdom

Groningen Biomolecular Sciences and Biotechnology Institute University of Groningen Groningen Netherlands

Guangzhou Key Laboratory of Subtropical Biodiversity and Biomonitoring School of Life Science South China Normal University Guangzhou 510631 China

Institute for Comparative Genomics Department of Biochemistry and Molecular Biology Dalhousie University Halifax NS B3H 4R2 Canada

Institute for Comparative Genomics Department of Biology Dalhousie University Halifax NS B3H 4R2 Canada

Institute of Parasitology Biology Centre Czech Acad Sci České Budějovice Czech Republic

Oncode Institute Hubrecht Institute KNAW and University Medical Centre Utrecht Utrecht The Netherlands

Erratum v

Nat Commun. 2021 Dec 16;12(1):7350. doi: 10.1038/s41467-021-27605-w. PubMed

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