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A New Lineage of Eukaryotes Illuminates Early Mitochondrial Genome Reduction

Janouskovec, J; Tikhonenkov, DV; Burki, F; Howe, AT; Rohwer, FL; Mylnikov, AP; Keeling, PJ; (2017) A New Lineage of Eukaryotes Illuminates Early Mitochondrial Genome Reduction. Current Biology , 27 (23) , Article e5. 10.1016/j.cub.2017.10.051. Green open access

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Abstract

The origin of eukaryotic cells represents a key transition in cellular evolution and is closely tied to outstanding questions about mitochondrial endosymbiosis [1, 2]. For example, gene-rich mitochondrial genomes are thought to be indicative of an ancient divergence, but this relies on unexamined assumptions about endosymbiont-to-host gene transfer [3–5]. Here, we characterize Ancoracysta twista, a new predatory flagellate that is not closely related to any known lineage in 201-protein phylogenomic trees and has a unique morphology, including a novel type of extrusome (ancoracyst). The Ancoracysta mitochondrion has a gene-rich genome with a coding capacity exceeding that of all other eukaryotes except the distantly related jakobids and Diphylleia, and it uniquely possesses heterologous, nucleus-, and mitochondrion-encoded cytochrome c maturase systems. To comprehensively examine mitochondrial genome reduction, we also assembled mitochondrial genomes from picozoans and colponemids and re-annotated existing mitochondrial genomes using hidden Markov model gene profiles. This revealed over a dozen previously overlooked mitochondrial genes at the level of eukaryotic supergroups. Analysis of trends over evolutionary time demonstrates that gene transfer to the nucleus was non-linear, that it occurred in waves of exponential decrease, and that much of it took place comparatively early, massively independently, and with lineage-specific rates. This process has led to differential gene retention, suggesting that gene-rich mitochondrial genomes are not a product of their early divergence. Parallel transfer of mitochondrial genes and their functional replacement by new nuclear factors are important in models for the origin of eukaryotes, especially as major gaps in our knowledge of eukaryotic diversity at the deepest level remain unfilled.

Type: Article
Title: A New Lineage of Eukaryotes Illuminates Early Mitochondrial Genome Reduction
Open access status: An open access version is available from UCL Discovery
DOI: 10.1016/j.cub.2017.10.051
Publisher version: http://doi.org/10.1016/j.cub.2017.10.051
Language: English
Additional information: This version is the author accepted manuscript. For information on re-use, please refer to the publisher’s terms and conditions.
Keywords: Origin of eukaryotes, mitochondrial genome evolution, cytochrome c maturation, gene transfer, phylogenomics, microbial diversity, cell ultrastructure, ancoracyst, Ancoracysta twista
UCL classification: UCL
UCL > Provost and Vice Provost Offices > School of Life and Medical Sciences
UCL > Provost and Vice Provost Offices > School of Life and Medical Sciences > Faculty of Life Sciences
UCL > Provost and Vice Provost Offices > School of Life and Medical Sciences > Faculty of Life Sciences > Div of Biosciences
UCL > Provost and Vice Provost Offices > School of Life and Medical Sciences > Faculty of Life Sciences > Div of Biosciences > Genetics, Evolution and Environment
URI: https://discovery.ucl.ac.uk/id/eprint/10042942
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