Mitochondrion-Related Organelles in Free-Living Protists

Leger, Michelle M.; Kolísko, Martin; Stairs, Courtney W.; Simpson, Alastair G. B.

doi:10.1007/978-3-030-17941-0_12

Cited by 8 publications

(12 citation statements)

References 104 publications

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“…Interestingly, the lack of the GCS (as an obvious MRO-localized source of NADH) and NuoE/NuoF (as part of the NADH reoxidation mechanism) in the CL3 lineage provides additional, though indirect, evidence for our hypothesis that the MRO in E. mutabile and PCS-ghost houses the PFO enzyme. We note that previous authors reporting on fornicate pyruvate conversion enzymes were hesitant to speculate on their subcellular localization without experimental data ( Leger et al, 2017 , 2019 ), and we agree that the experimentally studied diplomonad S. salmonicida is so far the only fornicate in which the presence of PFO in its MRO has been robustly established ( Jerlström-Hultqvist et al, 2013 ). It is indeed conceivable that PFO is generally missing from fornicate MROs despite the fact that most of them are thought to possess a MRO-localized hydrogenase, as the latter would still be required for NuoE/NuoF-assisted NADH reoxidation.…”

Section: Resultssupporting

confidence: 83%

“…These in silico analyses indicate that like in other fornicates, including G. intestinalis with its highly reduced mitosomes ( Leger et al, 2019 ; Tachezy and Šmíd, 2019 ), one of the apparent reasons for having MROs retained in the CL3 lineage is their role in supplying the cells with Fe-S clusters critical for the function of various proteins (in cellular compartments beyond the MRO itself). Particularly notable is the presence of homologs of the mitochondrial import machinery and ISC pathway components in I. spirale , which provides strong evidence that this organism does possess a MRO, despite the fact that it has not yet been discerned in TEM preparations ( Yubuki et al, 2017 ).…”

Section: Resultsmentioning

confidence: 82%

“…The so-called ISC pathway for the assembly of iron-sulfur (Fe-S) clusters is the most widespread mitochondrial functionality retained, even in most highly reduced MRO forms ( Tachezy and Šmíd, 2019 ; Braymer et al, 2021 ), although exceptions do exist ( Santos et al, 2018 ; Leger et al, 2019 ; Lill and Freibert, 2020 ). The transcriptome assemblies of the three CL3 representatives were queried and indeed, all of them possessed homologs of essential components of the ISC pathway, including cysteine desulfurase (IscS), the scaffold protein for Fe-S cluster assembly (IscU), the ISC pathway-specific DnaJ domain-containing regulator of mtHsp70 (Jac1), and [2Fe-2S]ferredoxin (Fdx, also called Yah1), which provides reducing power to the ISC pathway in mitochondria and MROs ( Figure 4 and Supplementary Table 2 ).…”

Section: Resultsmentioning

confidence: 99%

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Evidence for an Independent Hydrogenosome-to-Mitosome Transition in the CL3 Lineage of Fornicates

et al. 2022

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Fornicata, a lineage of a broader and ancient anaerobic eukaryotic clade Metamonada, contains diverse taxa that are ideally suited for evolutionary studies addressing various fundamental biological questions, such as the evolutionary trajectory of mitochondrion-related organelles (MROs), the transition between free-living and endobiotic lifestyles, and the derivation of alternative genetic codes. To this end, we conducted detailed microscopic and transcriptome analyses in a poorly documented strain of an anaerobic free-living marine flagellate, PCS, in the so-called CL3 fornicate lineage. Fortuitously, we discovered that the original culture contained two morphologically similar and closely related CL3 representatives, which doubles the taxon representation within this lineage. We obtained a monoeukaryotic culture of one of them and formally describe it as a new member of the family Caviomonadidae, Euthynema mutabile gen. et sp. nov. In contrast to previously studied caviomonads, the endobiotic Caviomonas mobilis and Iotanema spirale, E. mutabile possesses an ultrastructurally discernible MRO. We sequenced and assembled the transcriptome of E. mutabile, and by sequence subtraction, obtained transcriptome data from the other CL3 clade representative present in the original PCS culture, denoted PCS-ghost. Transcriptome analyses showed that the reassignment of only one of the UAR stop codons to encode Gln previously reported from I. spirale does not extend to its free-living relatives and is likely due to a unique amino acid substitution in I. spirale’s eRF1 protein domain responsible for termination codon recognition. The backbone fornicate phylogeny was robustly resolved in a phylogenomic analysis, with the CL3 clade amongst the earliest branching lineages. Metabolic and MRO functional reconstructions of CL3 clade members revealed that all three, including I. spirale, encode homologs of key components of the mitochondrial protein import apparatus and the ISC pathway, indicating the presence of a MRO in all of them. In silico evidence indicates that the organelles of E. mutabile and PCS-ghost host ATP and H2 production, unlike the cryptic MRO of I. spirale. These data suggest that the CL3 clade has experienced a hydrogenosome-to-mitosome transition independent from that previously documented for the lineage leading to Giardia.

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Section: Resultssupporting

confidence: 83%

Section: Resultsmentioning

confidence: 82%

Section: Resultsmentioning

confidence: 99%

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Evidence for an Independent Hydrogenosome-to-Mitosome Transition in the CL3 Lineage of Fornicates

et al. 2022

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Section: Introductionmentioning

confidence: 99%

“…Giardia intestinalis is a microaerophilic parasitic protist that lives in the epithelium of the small intestine of mammals, where it causes giardiasis (1). It belongs to the Metamonada supergroup of eukaryotes that typically contain mitochondria-related organelles (MRO) that lack organellar genomes and cristae and that are adapted to life with little or no oxygen (2). The so-called mitosomes of G. intestinalis are one of the simplest MROs known among eukaryotes, as they contain only a single metabolic pathway for iron-sulfur (Fe-S) cluster synthesis (ISC) (3–5).…”

Section: Introductionmentioning

confidence: 99%

The late ISC pathway interactome reveals mitosomal-cytoplasmic crosstalk in Giardia intestinalis

Motyčková

Voleman

Najdrová

et al. 2022

Preprint

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Mitochondrial metabolism is entirely dependent on the biosynthesis of the [4Fe-4S] clusters, which are part of the subunits of the respiratory chain. The mitochondrial late ISC pathway mediates the formation of these clusters from simpler [2Fe-2S] molecules and transfers them to client proteins. Here, we characterized the late ISC pathway in one of the simplest mitochondria, mitosomes, of the anaerobic protist Giardia intestinalis that lost the respiratory chain and other hallmarks of mitochondria. Identification of the late ISC interactome revealed unexpected involvement of the aerobic marker protein BolA and specific interaction of IscA with the outer mitosomal membrane. Although we confirmed that the synthesis of the Fe-S cluster remained the only metabolic role of mitosomes, we also showed that mitosomes lack client proteins that require the [4Fe-4S] cluster. Instead, by knocking out the bolA gene from the G. intestinalis genome, we showed that, unlike aerobic mitochondria, the late ISC mitosomal pathway is involved in the assembly of cytosolic [4Fe-4S] clusters. Thus, this work reveals an unexpected link between the formation of mitochondrial and cytosolic [4Fe- 4S] clusters. This may either be a consequence of mitochondrial adaptation to life without oxygen, or it represents a general metabolic coupling that has not been previously observed in the complex mitochondrial metabolism of aerobes.

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Vestiges of the Bacterial Signal Recognition Particle-Based Protein Targeting in Mitochondria

Pyrih

Pánek

Durante

et al. 2021

Molecular Biology and Evolution

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The main bacterial pathway for inserting proteins into the plasma membrane relies on the signal recognition particle (SRP), composed of the Ffh protein and an associated RNA component, and the SRP-docking protein FtsY. Eukaryotes use an equivalent system of archaeal origin to deliver proteins into the endoplasmic reticulum, whereas a bacteria-derived SRP and FtsY function in the plastid. Here we report on the presence of homologs of the bacterial Ffh and FtsY proteins in various unrelated plastid-lacking unicellular eukaryotes, namely Heterolobosea, Alveida, Goniomonas, and Hemimastigophora. The monophyly of novel eukaryotic Ffh and FtsY groups, predicted mitochondrial localization experimentally confirmed for Naegleria gruberi, and a strong alphaproteobacterial affinity of the Ffh group, collectively suggest they constitute parts of an ancestral mitochondrial signal peptide-based protein-targeting system inherited from the last eukaryotic common ancestor, but lost from the majority of extant eukaryotes. The ability of putative signal peptides, predicted in a subset of mitochondrial-encoded N. gruberi proteins, to target a reporter fluorescent protein into the endoplasmic reticulum of Trypanosoma brucei, likely through their interaction with the cytosolic SRP, provided further support for this notion. We also illustrate that known mitochondrial ribosome-interacting proteins implicated in membrane protein targeting in opisthokonts (Mba1, Mdm38, and Mrx15) are broadly conserved in eukaryotes and non-redundant with the mitochondrial SRP system. Finally, we identified a novel mitochondrial protein (MAP67) present in diverse eukaryotes and related to the signal peptide-binding domain of Ffh, which may well be a hitherto unrecognized component of the mitochondrial membrane protein-targeting machinery.

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Mitochondrion-Related Organelles in Free-Living Protists

Cited by 8 publications

References 104 publications

Evidence for an Independent Hydrogenosome-to-Mitosome Transition in the CL3 Lineage of Fornicates

Evidence for an Independent Hydrogenosome-to-Mitosome Transition in the CL3 Lineage of Fornicates

The late ISC pathway interactome reveals mitosomal-cytoplasmic crosstalk in Giardia intestinalis

Vestiges of the Bacterial Signal Recognition Particle-Based Protein Targeting in Mitochondria

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