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 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.

Parallel functional reduction in the mitochondria of apicomplexan parasites

“…2,28,[30][31][32]44,48,60 For anerobic metabolic proteins, the PDH complex, ETC complex I, and MICOS proteins, that are not found apicomplexans or chromerids, BLASTp searches were conducted using ciliate and stramenopile queries. 40,48,73,74 The resulting hits were manually parsed to retain top hits from apicomplexans and chromerids, as well as dinoflagellates, ciliates and stramenopiles. The parsed hits were then aligned with MAFFT v. 7.212.…”

Genomics of New Ciliate Lineages Provides Insight into the Evolution of Obligate Anaerobiosis

“…Nevertheless, studying the metabolism of an endobiont without an available comparison to its free-living relatives significantly obscures the complete image of the evolutionary adaptations to anoxic conditions, because it is difficult to distinguish adaptations associated with the transition to endobiosis from those associated with the adoption of an anaerobic lifestyle. Authors of a recent publication [21] have broadened the dataset with mitochondrial genomes and transcriptomes of four free-living anaerobic ciliates from the same class as the endobiotic N. ovalis (Armophorea), showing their common traits in encoding proton-pumping complex I but likely lacking functional complexes III and V of the ETC, therefore having lost the capacity for ATP synthesis via oxidative phosphorylation. In silico analyses indicate that all of them produce ATP by substrate-level phosphorylation via acetate:succinyl coenzyme A (CoA) transferase (ASCT) and succinyl-CoA synthetase (SCS).…”

Characterization and Comparative Analyses of Mitochondrial Genomes in Single-Celled Eukaryotes to Shed Light on the Diversity and Evolution of Linear Molecular Architecture

“…In the years since those seminal discoveries, more ciliate mitogenomes have been characterized, including 20 mitogenomes from species in the class Oligohymenophorea ( Tetrahymena pyriformis , T. thermophila , T. malaccensis , T. paravorax , T. pigmentosa , T. rostrata , Ichthyophthirius multifiliis , Uronema marinum , Paramecium caudatum , P. aurelia , P. tetraurelia , P. sexaurelia , P. multimicronucleatum , P. biaurelia , P. octaurelia , P. novaurelia , P. decaurelia , P. dodecaurelia , P. quadecaurelia , and P. jenningsi ) [ 28 , 29 , 30 , 31 , 32 , 33 , 34 , 35 , 36 ], eight mitogenomes of species in the class Spirotrichea ( Oxytricha trifallax , Laurentiella strenua , Stylonychia lemnae , Paraurostyla sp., Urostyla grandis , Pseudourostyla cristata , Euplotes minuta , and E. crassus ) [ 37 , 38 , 39 ], two mitogenomes in the class Heterotrichea ( Stentor coeruleus and Gruberia lanceolata ) [ 20 , 40 ], as well as seven hydrogenosomal genomes of anerobic ciliates ( Nyctotherus ovalis , Metopus contortus , Metopus es , Metopid sp., Heterometopus sp., Parablepharisma sp., and Muranothrix gubernata ) [ 41 , 42 , 43 ]. Ciliate mitogenomes are generally in size of 20–70 kb, with high A+T content (58.53% for N. ovalis ~81.51% for I. multifiliis ) and relatively large gene complements (20–30 protein-coding genes) [ 39 , 41 , 44 ].…”