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Anaeramoebae are a divergent lineage of eukaryotes that shed light on the transition from anaerobic mitochondria to hydrogenosomes

Stairs, Courtney W LU orcid ; Táborský, Petr ; Salomaki, Eric D ; Kolisko, Martin ; Pánek, Tomáš ; Eme, Laura ; Hradilová, Miluše ; Vlček, Čestmír ; Jerlström-Hultqvist, Jon and Roger, Andrew J , et al. (2021) In Current biology : CB 31(24). p.5-5612
Abstract

Discoveries of diverse microbial eukaryotes and their inclusion in comprehensive phylogenomic analyses have crucially re-shaped the eukaryotic tree of life in the 21st century.1 At the deepest level, eukaryotic diversity comprises 9-10 "supergroups." One of these supergroups, the Metamonada, is particularly important to our understanding of the evolutionary dynamics of eukaryotic cells, including the remodeling of mitochondrial function. All metamonads thrive in low-oxygen environments and lack classical aerobic mitochondria, instead possessing mitochondrion-related organelles (MROs) with metabolisms that are adapted to low-oxygen conditions. These MROs lack an organellar genome, do not participate in the Krebs cycle and oxidative... (More)

Discoveries of diverse microbial eukaryotes and their inclusion in comprehensive phylogenomic analyses have crucially re-shaped the eukaryotic tree of life in the 21st century.1 At the deepest level, eukaryotic diversity comprises 9-10 "supergroups." One of these supergroups, the Metamonada, is particularly important to our understanding of the evolutionary dynamics of eukaryotic cells, including the remodeling of mitochondrial function. All metamonads thrive in low-oxygen environments and lack classical aerobic mitochondria, instead possessing mitochondrion-related organelles (MROs) with metabolisms that are adapted to low-oxygen conditions. These MROs lack an organellar genome, do not participate in the Krebs cycle and oxidative phosphorylation,2 and often synthesize ATP by substrate-level phosphorylation coupled to hydrogen production.3,4 The events that occurred during the transition from an oxygen-respiring mitochondrion to a functionally streamlined MRO early in metamonad evolution remain largely unknown. Here, we report transcriptomes of two recently described, enigmatic, anaerobic protists from the genus Anaeramoeba.5 Using phylogenomic analysis, we show that these species represent a divergent, phylum-level lineage in the tree of metamonads, emerging as a sister group of the Parabasalia and reordering the deep branching order of the metamonad tree. Metabolic reconstructions of the Anaeramoeba MROs reveal many "classical" mitochondrial features previously not seen in metamonads, including a disulfide relay import system, propionate production, and amino acid metabolism. Our findings suggest that the cenancestor of Metamonada likely had MROs with more classical mitochondrial features than previously anticipated and demonstrate how discoveries of novel lineages of high taxonomic rank continue to transform our understanding of early eukaryote evolution.

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organization
publishing date
type
Contribution to journal
publication status
published
subject
in
Current biology : CB
volume
31
issue
24
pages
5 - 5612
publisher
Elsevier
external identifiers
  • pmid:34710348
  • scopus:85121250096
ISSN
1879-0445
DOI
10.1016/j.cub.2021.10.010
language
English
LU publication?
yes
additional info
Copyright © 2021 The Author(s). Published by Elsevier Inc. All rights reserved.
id
13031f68-f590-441c-a3a5-6e714233b9c0
date added to LUP
2021-10-31 21:02:32
date last changed
2024-06-16 22:08:12
@article{13031f68-f590-441c-a3a5-6e714233b9c0,
  abstract     = {{<p>Discoveries of diverse microbial eukaryotes and their inclusion in comprehensive phylogenomic analyses have crucially re-shaped the eukaryotic tree of life in the 21st century.1 At the deepest level, eukaryotic diversity comprises 9-10 "supergroups." One of these supergroups, the Metamonada, is particularly important to our understanding of the evolutionary dynamics of eukaryotic cells, including the remodeling of mitochondrial function. All metamonads thrive in low-oxygen environments and lack classical aerobic mitochondria, instead possessing mitochondrion-related organelles (MROs) with metabolisms that are adapted to low-oxygen conditions. These MROs lack an organellar genome, do not participate in the Krebs cycle and oxidative phosphorylation,2 and often synthesize ATP by substrate-level phosphorylation coupled to hydrogen production.3,4 The events that occurred during the transition from an oxygen-respiring mitochondrion to a functionally streamlined MRO early in metamonad evolution remain largely unknown. Here, we report transcriptomes of two recently described, enigmatic, anaerobic protists from the genus Anaeramoeba.5 Using phylogenomic analysis, we show that these species represent a divergent, phylum-level lineage in the tree of metamonads, emerging as a sister group of the Parabasalia and reordering the deep branching order of the metamonad tree. Metabolic reconstructions of the Anaeramoeba MROs reveal many "classical" mitochondrial features previously not seen in metamonads, including a disulfide relay import system, propionate production, and amino acid metabolism. Our findings suggest that the cenancestor of Metamonada likely had MROs with more classical mitochondrial features than previously anticipated and demonstrate how discoveries of novel lineages of high taxonomic rank continue to transform our understanding of early eukaryote evolution.</p>}},
  author       = {{Stairs, Courtney W and Táborský, Petr and Salomaki, Eric D and Kolisko, Martin and Pánek, Tomáš and Eme, Laura and Hradilová, Miluše and Vlček, Čestmír and Jerlström-Hultqvist, Jon and Roger, Andrew J and Čepička, Ivan}},
  issn         = {{1879-0445}},
  language     = {{eng}},
  month        = {{10}},
  number       = {{24}},
  pages        = {{5--5612}},
  publisher    = {{Elsevier}},
  series       = {{Current biology : CB}},
  title        = {{Anaeramoebae are a divergent lineage of eukaryotes that shed light on the transition from anaerobic mitochondria to hydrogenosomes}},
  url          = {{http://dx.doi.org/10.1016/j.cub.2021.10.010}},
  doi          = {{10.1016/j.cub.2021.10.010}},
  volume       = {{31}},
  year         = {{2021}},
}