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A new lineage of Eukaryotes illuminates early Mitochondrial Genome Reduction.

A new lineage of Eukaryotes illuminates early Mitochondrial Genome Reduction.
A new lineage of Eukaryotes illuminates early Mitochondrial Genome Reduction.
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, 4, 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.
3717-3724
Janouškovec, Jan
fbaa4a5d-872e-465b-b2c3-bb35df455cc6
Tikhonenkov, Denis V.
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Burki, F
f0b7504b-e486-47c1-a648-d24a94641917
Howe, Alexis T.
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Rohwer, Forest L.
4b9c98f5-83f0-4aa4-aa0c-8bd0780bc17c
Mylnikov, Alexander P.
ba6dced3-1dcf-4879-aca5-36782fceee35
Keeling, Patrick J.
fd51c2ef-1daa-442d-b186-71001aa7ca7d
Janouškovec, Jan
fbaa4a5d-872e-465b-b2c3-bb35df455cc6
Tikhonenkov, Denis V.
a1c998c0-e960-4269-b711-70f098020d96
Burki, F
f0b7504b-e486-47c1-a648-d24a94641917
Howe, Alexis T.
3e3b79df-ebfd-40e4-bb77-9b45eb8c4ef0
Rohwer, Forest L.
4b9c98f5-83f0-4aa4-aa0c-8bd0780bc17c
Mylnikov, Alexander P.
ba6dced3-1dcf-4879-aca5-36782fceee35
Keeling, Patrick J.
fd51c2ef-1daa-442d-b186-71001aa7ca7d

Janouškovec, Jan, Tikhonenkov, Denis V., Burki, F, Howe, Alexis T., Rohwer, Forest L., Mylnikov, Alexander P. and Keeling, Patrick J. (2017) A new lineage of Eukaryotes illuminates early Mitochondrial Genome Reduction. Current biology : CB, 27 (23), 3717-3724, [e.5]. (doi:10.1016/j.cub.2017.10.051).

Record type: Article

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, 4, 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.

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More information

Published date: 22 November 2017
Additional Information: https://www.elsevier.com/about/policies/open-access-licenses/elsevier-user-license

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Local EPrints ID: 458216
URI: http://eprints.soton.ac.uk/id/eprint/458216
PURE UUID: f16ab54f-cbaa-4c24-b633-49b1b90d59ca
ORCID for Jan Janouškovec: ORCID iD orcid.org/0000-0001-6547-749X

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Date deposited: 30 Jun 2022 17:34
Last modified: 17 Mar 2024 04:11

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Contributors

Author: Jan Janouškovec ORCID iD
Author: Denis V. Tikhonenkov
Author: F Burki
Author: Alexis T. Howe
Author: Forest L. Rohwer
Author: Alexander P. Mylnikov
Author: Patrick J. Keeling

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