A cytosolic ferredoxin-independent hydrogenase possibly mediates hydrogen uptake in Trichomonas vaginalis

Smutná, Tamara; Dohnálková, Alena; Šuták, Robert; Narayanasamy, Ravi Kumar; Tachezy, Jan

doi:10.1016/j.cub.2021.10.050

Cited by 11 publications

(11 citation statements)

References 91 publications

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“…intestinalis (Lloyd et al, 2002;Smutná et al, 2022). The lack of evidence for the MRO localisation of HydA is consistent with the apparent lack of PFOs and ferredoxins in this compartment and indicates that the pathway of extended glycolysis has cytosolic localisation in P. pyriformis.…”

Section: Discussionsupporting

confidence: 61%

“…Confusingly enough, the third maturase HydG was robustly classified as cytosolic together with four paralogues of HydA; one HydA remained unclassified and four were not detected by LOPIT. It is unclear, how the maturation of cytosolic HydA is achieved if the set of maturases is distributed across two compartments, however, a similar situation has been reported already in T. vaginalis and G. intestinalis (Lloyd et al, 2002; Smutná et al, 2022). The lack of evidence for the MRO localisation of HydA is consistent with the apparent lack of PFOs and ferredoxins in this compartment and indicates that the pathway of extended glycolysis has cytosolic localisation in P. pyriformis .…”

Section: Discussionmentioning

confidence: 63%

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Reduced mitochondria provide an essential function for the cytosolic methionine cycle

Zítek

Füssy

Treitli

et al. 2022

Preprint

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It has been long hypothesised that mitochondrial reduction is intrinsically related to the remodelling of Fe-S clusters assembly. Yet as our knowledge of divergent free-living protists broadens, so does the spectrum of variability within the range of mitochondrial-related organelles (MROs) fundamental functions. We resolved to high precision the MRO proteome of Paratrimastix pyriformis using Localisation of Organelle Proteins by Isotope Tagging (LOPIT) and demonstrate its role in the synthesis of folate derivates bearing one-carbon (1C) units, its link to the glycine cleavage system (GCS) and their only conceivable role as suppliers for the cytosolic methionine cycle, involved in recycling of S-adenosine methionine. This observation provides congruity to the presence of GCS in MROs of free-living anaerobes and its absence in endobionts, which typically lose the methionine cycle and, in the case of oxymonads, also mitochondria.

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Section: Discussionsupporting

confidence: 61%

Section: Discussionmentioning

confidence: 63%

Reduced mitochondria provide an essential function for the cytosolic methionine cycle

Zítek

Füssy

Treitli

et al. 2022

Preprint

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“…We cannot completely rule out the possibility that the maturation factors are encoded, but with an expression level too low (at the conditions used for obtaining the transcriptome data) to detect their presence. Nevertheless, the absence of the maturation factors in several hydrogenase-carrying eukaryotes has been noted before ( Stairs et al, 2015 ; Leger et al, 2017 ; Yazaki et al, 2020 ) and there is growing biochemical evidence that hydrogenases can attain enzymatic activity without the aid of these factors ( Berto et al, 2011 ; Kuchenreuther et al, 2012 ; Smutná et al, 2022 ). Hence, despite various uncertainties inherent to the nature of the data analyzed and the solely in silico methodology employed, the results of our examinations are best interpreted such that the MROs of both PCS-ghost and E. mutabile contain a functional hydrogenase enzyme ( Figure 5B ), consistent with the inferred presence of PFO (and thus a source of reduced ferredoxin) in the same compartments.…”

Section: Resultsmentioning

confidence: 95%

“…Reduced ferredoxin resulting from the reaction of PFO needs to be reoxidized, which in MROs is typically achieved by passing the electrons to protons in a reaction catalyzed by [FeFe]-hydrogenase (HydA), yielding H 2 ( Stairs et al, 2015 ). Metamonads commonly possess multiple HydA versions, with their predicted or experimentally demonstrated localization to either MROs or the cytoplasm ( Jerlström-Hultqvist et al, 2013 ; Leger et al, 2017 ; Stairs et al, 2021 ; Smutná et al, 2022 ). Unsurprisingly, each CL3 lineage representative encodes multiple HydA isoforms, but only one, a protein from E. mutabile , was predicted to be MRO-localized ( Supplementary Table 3 ).…”

Section: Resultsmentioning

confidence: 99%

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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“…Reduced ferredoxin is reoxidized by the activity of [FeFe] hydrogenase (Bui & Johnson, 1996; Payne et al, 1993), which couples protons with ferredoxin‐carried electrons and forms molecular hydrogen that is released as a waste product. The hydrogenosomal proteome contains at least five [FeFe] hydrogenase paralogs (Schneider et al, 2011; Smutná et al, 2022) that differ in molecular weight, conservation of catalytic H‐cluster‐binding motif, and arrangement of FeS clusters that are involved in electron transfer (Smutná et al, 2022); thus, these enzymes possibly participate in different redox processes.…”

Section: Biochemistry Of Hydrogenosomesmentioning

confidence: 99%

The hydrogenosome of Trichomonas vaginalis

Tachezy

Makki

2022

J Eukaryotic Microbiology

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This review is dedicated to the 50th anniversary of the discovery of hydrogenosomes by Miklós Müller and Donald Lindmark, which we will celebrate the following year. It was a long journey from the first observation of enigmatic rows of granules in trichomonads at the end of the 19th century to their first biochemical characterization in 1973. The key experiments by Müller and Lindmark revealed that the isolated granules contain hydrogen‐producing hydrogenase, similar to some anaerobic bacteria—a discovery that gave birth to the field of hydrogenosomes. It is also important to acknowledge the parallel work of the team of Apolena Čerkasovová, Jiří Čerkasov, and Jaroslav Kulda, who demonstrated that these granules, similar to mitochondria, produce ATP. However, the evolutionary origin of hydrogenosomes remained enigmatic until the turn of the millennium, when it was finally accepted that hydrogenosomes and mitochondria evolved from a common ancestor. After a historical introduction, the review provides an overview of hydrogenosome biogenesis, hydrogenosomal protein import, and the relationship between the peculiar structure of membrane translocases and its low inner membrane potential due to the lack of respiratory complexes. Next, it summarizes the current state of knowledge on energy metabolism, the oxygen defense system, and iron/sulfur cluster assembly.

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A cytosolic ferredoxin-independent hydrogenase possibly mediates hydrogen uptake in Trichomonas vaginalis

Cited by 11 publications

References 91 publications

Reduced mitochondria provide an essential function for the cytosolic methionine cycle

Reduced mitochondria provide an essential function for the cytosolic methionine cycle

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

The hydrogenosome of Trichomonas vaginalis

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