Convergent Evolution of Hydrogenosomes from Mitochondria by Gene Transfer and Loss

Hydrogenosomes are H2-producing mitochondrial homologs found in some anaerobic microbial eukaryotes that provide a rare intracellular niche for H2-utilizing endosymbiotic archaea. Among ciliates, anaerobic and aerobic lineages are interspersed, demonstrating that the switch to an anaerobic lifestyle with hydrogenosomes has occurred repeatedly and independently. To investigate the molecular details of this transition, we generated genomic and transcriptomic data sets from anaerobic ciliates representing three distinct lineages. Our data demonstrate that hydrogenosomes have evolved from ancestral mitochondria in each case and reveal different degrees of independent mitochondrial genome and proteome reductive evolution, including the first example of complete mitochondrial genome loss in ciliates. Intriguingly, the FeFe-hydrogenase used for generating H2 has a unique domain structure among eukaryotes and appears to have been present, potentially through a single lateral gene transfer from an unknown donor, in the common aerobic ancestor of all three lineages. The early acquisition and retention of FeFe-hydrogenase helps to explain the facility whereby mitochondrial function can be so radically modified within this diverse and ecologically important group of microbial eukaryotes.

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Main Authors: Lewis, William H., Lind, Anders E., Sendra, Kacper M., Onsbring, Henning, Williams, Tom A., Esteban, Genoveva F., Hirt, Robert P., Ettema, Thijs J.G., Embley, T.M.
Format: Article/Letter to editor biblioteca
Language:English
Subjects:anaerobic metabolism, evolution, genomics, hydrogenosomes, microbial eukaryotes, mitochondria,
Online Access:https://research.wur.nl/en/publications/convergent-evolution-of-hydrogenosomes-from-mitochondria-by-gene-
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spelling dig-wur-nl-wurpubs-5614162024-10-02 Lewis, William H. Lind, Anders E. Sendra, Kacper M. Onsbring, Henning Williams, Tom A. Esteban, Genoveva F. Hirt, Robert P. Ettema, Thijs J.G. Embley, T.M. Article/Letter to editor Molecular Biology and Evolution 37 (2020) 2 ISSN: 0737-4038 Convergent Evolution of Hydrogenosomes from Mitochondria by Gene Transfer and Loss 2020 Hydrogenosomes are H2-producing mitochondrial homologs found in some anaerobic microbial eukaryotes that provide a rare intracellular niche for H2-utilizing endosymbiotic archaea. Among ciliates, anaerobic and aerobic lineages are interspersed, demonstrating that the switch to an anaerobic lifestyle with hydrogenosomes has occurred repeatedly and independently. To investigate the molecular details of this transition, we generated genomic and transcriptomic data sets from anaerobic ciliates representing three distinct lineages. Our data demonstrate that hydrogenosomes have evolved from ancestral mitochondria in each case and reveal different degrees of independent mitochondrial genome and proteome reductive evolution, including the first example of complete mitochondrial genome loss in ciliates. Intriguingly, the FeFe-hydrogenase used for generating H2 has a unique domain structure among eukaryotes and appears to have been present, potentially through a single lateral gene transfer from an unknown donor, in the common aerobic ancestor of all three lineages. The early acquisition and retention of FeFe-hydrogenase helps to explain the facility whereby mitochondrial function can be so radically modified within this diverse and ecologically important group of microbial eukaryotes. en application/pdf https://research.wur.nl/en/publications/convergent-evolution-of-hydrogenosomes-from-mitochondria-by-gene- 10.1093/molbev/msz239 https://edepot.wur.nl/514938 anaerobic metabolism evolution genomics hydrogenosomes microbial eukaryotes mitochondria https://creativecommons.org/licenses/by/4.0/ Wageningen University & Research
institution WUR NL
collection DSpace
country Países bajos
countrycode NL
component Bibliográfico
access En linea
databasecode dig-wur-nl
tag biblioteca
region Europa del Oeste
libraryname WUR Library Netherlands
language English
topic anaerobic metabolism
evolution
genomics
hydrogenosomes
microbial eukaryotes
mitochondria
anaerobic metabolism
evolution
genomics
hydrogenosomes
microbial eukaryotes
mitochondria
spellingShingle anaerobic metabolism
evolution
genomics
hydrogenosomes
microbial eukaryotes
mitochondria
anaerobic metabolism
evolution
genomics
hydrogenosomes
microbial eukaryotes
mitochondria
Lewis, William H.
Lind, Anders E.
Sendra, Kacper M.
Onsbring, Henning
Williams, Tom A.
Esteban, Genoveva F.
Hirt, Robert P.
Ettema, Thijs J.G.
Embley, T.M.
Convergent Evolution of Hydrogenosomes from Mitochondria by Gene Transfer and Loss
description Hydrogenosomes are H2-producing mitochondrial homologs found in some anaerobic microbial eukaryotes that provide a rare intracellular niche for H2-utilizing endosymbiotic archaea. Among ciliates, anaerobic and aerobic lineages are interspersed, demonstrating that the switch to an anaerobic lifestyle with hydrogenosomes has occurred repeatedly and independently. To investigate the molecular details of this transition, we generated genomic and transcriptomic data sets from anaerobic ciliates representing three distinct lineages. Our data demonstrate that hydrogenosomes have evolved from ancestral mitochondria in each case and reveal different degrees of independent mitochondrial genome and proteome reductive evolution, including the first example of complete mitochondrial genome loss in ciliates. Intriguingly, the FeFe-hydrogenase used for generating H2 has a unique domain structure among eukaryotes and appears to have been present, potentially through a single lateral gene transfer from an unknown donor, in the common aerobic ancestor of all three lineages. The early acquisition and retention of FeFe-hydrogenase helps to explain the facility whereby mitochondrial function can be so radically modified within this diverse and ecologically important group of microbial eukaryotes.
format Article/Letter to editor
topic_facet anaerobic metabolism
evolution
genomics
hydrogenosomes
microbial eukaryotes
mitochondria
author Lewis, William H.
Lind, Anders E.
Sendra, Kacper M.
Onsbring, Henning
Williams, Tom A.
Esteban, Genoveva F.
Hirt, Robert P.
Ettema, Thijs J.G.
Embley, T.M.
author_facet Lewis, William H.
Lind, Anders E.
Sendra, Kacper M.
Onsbring, Henning
Williams, Tom A.
Esteban, Genoveva F.
Hirt, Robert P.
Ettema, Thijs J.G.
Embley, T.M.
author_sort Lewis, William H.
title Convergent Evolution of Hydrogenosomes from Mitochondria by Gene Transfer and Loss
title_short Convergent Evolution of Hydrogenosomes from Mitochondria by Gene Transfer and Loss
title_full Convergent Evolution of Hydrogenosomes from Mitochondria by Gene Transfer and Loss
title_fullStr Convergent Evolution of Hydrogenosomes from Mitochondria by Gene Transfer and Loss
title_full_unstemmed Convergent Evolution of Hydrogenosomes from Mitochondria by Gene Transfer and Loss
title_sort convergent evolution of hydrogenosomes from mitochondria by gene transfer and loss
url https://research.wur.nl/en/publications/convergent-evolution-of-hydrogenosomes-from-mitochondria-by-gene-
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