The Organellar Genome and Metabolic Potential of the Hydrogen-Producing Mitochondrion of Nyctotherus ovalis

Graaf, R.M. de; Ricard, Guénola; Alen, Theo A. van; Duarte, Isabel Margarida; Dutilh, Bas E.; Burgtorf, Carola; Kuiper, Jan Willem; Staay, G.W.M. van der; Tielens, Aloysius G.M.; Huynen, Martijn A.; Hackstein, J.H.P.

doi:10.1093/molbev/msr059

Cited by 74 publications

(94 citation statements)

References 72 publications

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“…At that time, oligoadenylation of transcripts probably evolved. A similar substantial genome reduction also occurred in the anaerobic ciliate Nyctotherus ovalis, whose mitochondrion was transformed into a hydrogenosome (de Graaf et al 2011). This organelle produces hydrogen, which is utilized by methane-producing archaea living together with Nyctotherus as endosymbionts in the hindgut of cockroaches (de Graaf et al 2011).…”

Section: Dinoflagellate Mitogenome Structurementioning

confidence: 77%

Peculiarities within peculiarities – dinoflagellates and their mitochondrial genomes

Gagat

Mackiewicz

2017

Mitochondrial DNA Part B

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After the establishment of an endosymbiotic relationship between a proto-mitochondrion and its probable archaeal host, mitochondrial genomes underwent a spectacular reductive evolution. An interesting pathway was chosen by mitogenomes of unicellular protists called dinoflagellates, which experienced an additional wave of reduction followed by amplification and rearrangement leading to their secondary complexity. The former resulted in a mitogenome consisting of only three protein-coding genes, the latter in their multiple copies being scattered across numerous chromosomes and the evolution of complex processes for their expression. These stunning features raise a question about the future of the dinoflagellate mitochondrial genome. ARTICLE HISTORY

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Section: Dinoflagellate Mitogenome Structurementioning

confidence: 77%

Peculiarities within peculiarities – dinoflagellates and their mitochondrial genomes

Gagat

Mackiewicz

2017

Mitochondrial DNA Part B

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“…The hydrogen-producing mitochondrion of Nyctotherus appears to generate a proton gradient (49), possibly involving complex I of the electron transport chain. This proton gradient is probably not used for ATP synthesis, as a gene encoding an ATP synthase seems to be lacking (101). The inferred metabolism of Nyctotherus is remarkably similar to the (also inferred) organellar metabolism of the phylogenetically distant anaerobic stramenopile Blastocystis (101).…”

Section: Alveolates and Stramenopilesmentioning

confidence: 79%

“…This proton gradient is probably not used for ATP synthesis, as a gene encoding an ATP synthase seems to be lacking (101). The inferred metabolism of Nyctotherus is remarkably similar to the (also inferred) organellar metabolism of the phylogenetically distant anaerobic stramenopile Blastocystis (101).…”

Section: Alveolates and Stramenopilesmentioning

confidence: 79%

“…Characterizations of respiratory chain components of this hydrogen-producing organelle uncovered biochemical features characteristic of anaerobic mitochondria (49). Furthermore, the organelle was shown to possess a typical ciliate mitochondrial genome (48,49,101); this finding established once and for all the evolutionary identity of mitochondria and hydrogenosomes as different manifestations of one and the same organelle.…”

Section: Alveolates and Stramenopilesmentioning

confidence: 85%

“…Nyctotherus was shown to consume glucose as a substrate and to excrete acetate, succinate, lactate, and ethanol as end products (49). Acetate and succinate are probably produced within the hydrogen-producing mitochondrion, in which succinate production occurs via a part of the Krebs cycle (malate-fumarate-succinate), used in a reductive direction (101). Acetate is produced from pyruvate, which is converted to acetyl-CoA by pyruvate dehydrogenase (PDH) and subsequently to acetate by an acetate:succinate CoA-transferase (ASCT) belonging to subfamily 1A, with sequence similarity to the ASCT from Trypanosoma brucei (503).…”

Section: Alveolates and Stramenopilesmentioning

confidence: 99%

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Biochemistry and Evolution of Anaerobic Energy Metabolism in Eukaryotes

Müller

Mentel

Hellemond

et al. 2012

Microbiol Mol Biol Rev

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695

904

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SUMMARY Major insights into the phylogenetic distribution, biochemistry, and evolutionary significance of organelles involved in ATP synthesis (energy metabolism) in eukaryotes that thrive in anaerobic environments for all or part of their life cycles have accrued in recent years. All known eukaryotic groups possess an organelle of mitochondrial origin, mapping the origin of mitochondria to the eukaryotic common ancestor, and genome sequence data are rapidly accumulating for eukaryotes that possess anaerobic mitochondria, hydrogenosomes, or mitosomes. Here we review the available biochemical data on the enzymes and pathways that eukaryotes use in anaerobic energy metabolism and summarize the metabolic end products that they generate in their anaerobic habitats, focusing on the biochemical roles that their mitochondria play in anaerobic ATP synthesis. We present metabolic maps of compartmentalized energy metabolism for 16 well-studied species. There are currently no enzymes of core anaerobic energy metabolism that are specific to any of the six eukaryotic supergroup lineages; genes present in one supergroup are also found in at least one other supergroup. The gene distribution across lineages thus reflects the presence of anaerobic energy metabolism in the eukaryote common ancestor and differential loss during the specialization of some lineages to oxic niches, just as oxphos capabilities have been differentially lost in specialization to anoxic niches and the parasitic life-style. Some facultative anaerobes have retained both aerobic and anaerobic pathways. Diversified eukaryotic lineages have retained the same enzymes of anaerobic ATP synthesis, in line with geochemical data indicating low environmental oxygen levels while eukaryotes arose and diversified.

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Mitochondrial Genome Evolution

Bernt

Machné²,

Sahyoun

et al. 2013

Encyclopedia of Life Sciences

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Mitochondria are membrane‐enclosed organelles present in most eukaryotic cells that generate most of the cell's adenosine triphosphate (ATP) supply. Derived from a proteobacterial ancestor, mitochondria harbour their own, drastically reduced genome. Starting from a prokaryote‐like ancestral state encoding a complete ribosomal ribonucleic acid (rRNA) operon, a complete set of transfer RNAs (tRNAs) required for translation, and key enzymes of the respiratory chain as well as some ribosomal proteins, the mitogenome has been dramatically restructured and further reduced in many of the eukaryotic lineages. The loss and transfer to the nucleus of mitochondrial genes is a common trend in most phyla, in particular in Metazoa and Alveolata. In extreme, phylogenetically dispersed cases, often associated with parasitic or anaerobic life styles, mitochondria have been transformed to the so‐called mitosomes or hydrogenosomes devoid of their own genetic material. Ancestrally a single circular deoxyribonucleic acid (DNA) , mitogenomes have evolved to complex, fragmented architectures in particular in Euglenozoa. Key Concepts: Mitochondria have an endosymbiotic origin deriving from a proteobacterial ancestor. Various evolutionary mechanisms operate on mitochondrial genomes. Mitochondrial genomes have developed very diverse properties during eukaryote evolution. Mitogenomic gene content declines in most eukaryotic lineages by horizontal transfer to the nuclear genome. Complex idiosyncratic genome organisations have independently evolved in several eukaryotic phyla.

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The Organellar Genome and Metabolic Potential of the Hydrogen-Producing Mitochondrion of Nyctotherus ovalis

Cited by 74 publications

References 72 publications

Peculiarities within peculiarities – dinoflagellates and their mitochondrial genomes

Peculiarities within peculiarities – dinoflagellates and their mitochondrial genomes

Biochemistry and Evolution of Anaerobic Energy Metabolism in Eukaryotes

Mitochondrial Genome Evolution

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