Convergent Evolution of Hydrogenosomes from Mitochondria by Gene Transfer and Loss

Author:

Lewis William H123,Lind Anders E2,Sendra Kacper M1,Onsbring Henning23,Williams Tom A4,Esteban Genoveva F5,Hirt Robert P1,Ettema Thijs J G23,Embley T Martin1

Affiliation:

1. Institute for Cell and Molecular Biosciences, Newcastle University, Newcastle-Upon-Tyne, United Kingdom

2. Department of Cell and Molecular Biology, Uppsala University, Uppsala, Sweden

3. Laboratory of Microbiology, Department of Agrotechnology and Food Sciences, Wageningen University, Wageningen, The Netherlands

4. School of Biological Sciences, University of Bristol, Bristol, United Kingdom

5. Department of Life and Environmental Sciences, Bournemouth University, Poole, United Kingdom

Abstract

AbstractHydrogenosomes 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.

Funder

National Genomics Infrastructure

Science for Life Laboratory at Uppsala University

Swedish Research Council

Knut and Alice Wallenberg Foundation

Swedish National Infrastructure for Computing

SNIC

European Research Council

ERC

Swedish Foundation for Strategic Research

Wellcome Trust

Royal Society University Research Fellowship

Natural Environment Research Council

Alice Ellen Cooper Dean Trust

Publisher

Oxford University Press (OUP)

Subject

Genetics,Molecular Biology,Ecology, Evolution, Behavior and Systematics

Reference118 articles.

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