Convergent Evolution of Hydrogenosomes from Mitochondria by Gene Transfer and Loss

Abstract 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...

Full description

Saved in:
Bibliographic Details
Published in:Molecular biology and evolution 2020-02, Vol.37 (2), p.524-539
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 Martin
Format: Article
Language:English
Subjects:
Aerobiosis
anaerobic metabolism
Anaerobiosis
Ciliophora - classification
Ciliophora - physiology
Discoveries
evolution
Evolution, Molecular
Gene Expression Profiling - methods
Gene Transfer, Horizontal
Genome, Mitochondrial
genomics
Hydrogen - metabolism
hydrogenosomes
microbial eukaryotes
mitochondria
Mitochondria - genetics
Phylogeny
Sequence Analysis, DNA - methods
Sequence Analysis, RNA
Citations: Items that this one cites
Items that cite this one
Online Access:Get full text
Tags: Add Tag
No Tags, Be the first to tag this record!
Description
Summary:Abstract 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.
ISSN:0737-4038
1537-1719
1537-1719
DOI:10.1093/molbev/msz239