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Curr Biol. 2017 Dec 4;27(23):3717-3724.e5. doi: 10.1016/j.cub.2017.10.051. Epub 2017 Nov 22.

A New Lineage of Eukaryotes Illuminates Early Mitochondrial Genome Reduction.

Author information

1
University College London, Department of Genetics, Evolution and Environment, London, UK; San Diego State University, Biology Department, San Diego, CA, USA; University of British Columbia, Botany Department, Vancouver, BC, Canada. Electronic address: janjan.cz@gmail.com.
2
University of British Columbia, Botany Department, Vancouver, BC, Canada; Institute for Biology of Inland Waters, Russian Academy of Sciences, Borok, Russia. Electronic address: tikho-denis@yandex.ru.
3
University of British Columbia, Botany Department, Vancouver, BC, Canada; Science for Life Laboratory, Program in Systematic Biology, Uppsala University, Uppsala, Sweden.
4
University of British Columbia, Botany Department, Vancouver, BC, Canada.
5
San Diego State University, Biology Department, San Diego, CA, USA.
6
Institute for Biology of Inland Waters, Russian Academy of Sciences, Borok, Russia.
7
University of British Columbia, Botany Department, Vancouver, BC, Canada. Electronic address: pkeeling@mail.ubc.ca.

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.

KEYWORDS:

Ancoracysta twista; ancoracyst; cell ultrastructure; cytochrome c maturation; gene transfer; microbial diversity; mitochondrial genome evolution; origin of eukaryotes; phylogenomics

PMID:
29174886
DOI:
10.1016/j.cub.2017.10.051
[Indexed for MEDLINE]
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