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Extreme mitochondrial reduction in a novel group of free-living metamonads

Williams, Shelby K. ; Jerlström Hultqvist, Jon ; Eglit, Yana ; Salas-Leiva, Dayana E. ; Curtis, Bruce ; Orr, Russell J.S. ; Stairs, Courtney W. LU orcid ; Atalay, Tuğba N. ; MacMillan, Naomi and Simpson, Alastair G.B. , et al. (2024) In Nature Communications 15.
Abstract

Metamonads are a diverse group of heterotrophic microbial eukaryotes adapted to living in hypoxic environments. All metamonads but one harbour metabolically altered ‘mitochondrion-related organelles’ (MROs) with reduced functions, however the degree of reduction varies. Here, we generate high-quality draft genomes, transcriptomes, and predicted proteomes for five recently discovered free-living metamonads. Phylogenomic analyses placed these organisms in a group we name the ‘BaSk’ (Barthelonids+Skoliomonads) clade, a deeply branching sister group to the Fornicata, a phylum that includes parasitic and free-living flagellates. Bioinformatic analyses of gene models shows that these organisms are predicted to have extremely reduced MRO... (More)

Metamonads are a diverse group of heterotrophic microbial eukaryotes adapted to living in hypoxic environments. All metamonads but one harbour metabolically altered ‘mitochondrion-related organelles’ (MROs) with reduced functions, however the degree of reduction varies. Here, we generate high-quality draft genomes, transcriptomes, and predicted proteomes for five recently discovered free-living metamonads. Phylogenomic analyses placed these organisms in a group we name the ‘BaSk’ (Barthelonids+Skoliomonads) clade, a deeply branching sister group to the Fornicata, a phylum that includes parasitic and free-living flagellates. Bioinformatic analyses of gene models shows that these organisms are predicted to have extremely reduced MRO proteomes in comparison to other free-living metamonads. Loss of the mitochondrial iron-sulfur cluster assembly system in some organisms in this group appears to be linked to the acquisition in their common ancestral lineage of a SUF-like minimal system Fe/S cluster pathway by lateral gene transfer. One of the isolates, Skoliomonas litria, appears to have lost all other known MRO pathways. No proteins were confidently assigned to the predicted MRO proteome of this organism suggesting that the organelle has been lost. The extreme mitochondrial reduction observed within this free-living anaerobic protistan clade demonstrates that mitochondrial functions may be completely lost even in free-living organisms.

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publication status
published
subject
in
Nature Communications
volume
15
article number
6805
publisher
Nature Publishing Group
external identifiers
  • pmid:39122691
  • scopus:85200850483
ISSN
2041-1723
DOI
10.1038/s41467-024-50991-w
language
English
LU publication?
yes
id
fa4eddef-0670-4ca8-9384-6e34d92ccc56
date added to LUP
2024-08-26 11:58:59
date last changed
2024-09-09 13:11:02
@article{fa4eddef-0670-4ca8-9384-6e34d92ccc56,
  abstract     = {{<p>Metamonads are a diverse group of heterotrophic microbial eukaryotes adapted to living in hypoxic environments. All metamonads but one harbour metabolically altered ‘mitochondrion-related organelles’ (MROs) with reduced functions, however the degree of reduction varies. Here, we generate high-quality draft genomes, transcriptomes, and predicted proteomes for five recently discovered free-living metamonads. Phylogenomic analyses placed these organisms in a group we name the ‘BaSk’ (Barthelonids+Skoliomonads) clade, a deeply branching sister group to the Fornicata, a phylum that includes parasitic and free-living flagellates. Bioinformatic analyses of gene models shows that these organisms are predicted to have extremely reduced MRO proteomes in comparison to other free-living metamonads. Loss of the mitochondrial iron-sulfur cluster assembly system in some organisms in this group appears to be linked to the acquisition in their common ancestral lineage of a SUF-like minimal system Fe/S cluster pathway by lateral gene transfer. One of the isolates, Skoliomonas litria, appears to have lost all other known MRO pathways. No proteins were confidently assigned to the predicted MRO proteome of this organism suggesting that the organelle has been lost. The extreme mitochondrial reduction observed within this free-living anaerobic protistan clade demonstrates that mitochondrial functions may be completely lost even in free-living organisms.</p>}},
  author       = {{Williams, Shelby K. and Jerlström Hultqvist, Jon and Eglit, Yana and Salas-Leiva, Dayana E. and Curtis, Bruce and Orr, Russell J.S. and Stairs, Courtney W. and Atalay, Tuğba N. and MacMillan, Naomi and Simpson, Alastair G.B. and Roger, Andrew J.}},
  issn         = {{2041-1723}},
  language     = {{eng}},
  month        = {{08}},
  publisher    = {{Nature Publishing Group}},
  series       = {{Nature Communications}},
  title        = {{Extreme mitochondrial reduction in a novel group of free-living metamonads}},
  url          = {{http://dx.doi.org/10.1038/s41467-024-50991-w}},
  doi          = {{10.1038/s41467-024-50991-w}},
  volume       = {{15}},
  year         = {{2024}},
}