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

Vargová, Romana; Hanousková, Pavla; Salamonová, Jana; Žihala, David; Silberman, Jeffrey D.; Eliáš, Marek; Čepička, Ivan

doi:10.3389/fmicb.2022.866459

Cited by 4 publications

(4 citation statements)

References 79 publications

(196 reference statements)

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“…These components were only detected in the less reduced MROs of parabasalids (e.g., Trichomonas vaginalis ) and in anaeramoebids [ 60 ]. Of course, additional components can be identified in the species with incomplete genomic data, yet these results likely demonstrate the ancestral adaptation of the late ISC pathway in Metamonada that involved the loss of Iba57 and IscA1 proteins [ 62 ].…”

Section: Resultsmentioning

confidence: 99%

Adaptation of the late ISC pathway in the anaerobic mitochondrial organelles of Giardia intestinalis

Motyčková,

Voleman,

Najdrová

et al. 2023

PLoS Pathog

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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. In addition to IscA2, Nfu1 and Grx5 we identified a novel BolA1 homologue in G. intestinalis mitosomes. It specifically interacts with Grx5 and according to the high-affinity pulldown also with other core mitosomal components. Using CRISPR/Cas9 we were able to establish full bolA1 knock out, the first cell line lacking a mitosomal protein. Despite the ISC pathway being the only metabolic role of the mitosome no significant changes in the mitosome biology could be observed as neither the number of the mitosomes or their capability to form [2Fe-2S] clusters in vitro was affected. We failed to identify natural client proteins that would require the [2Fe-2S] or [4Fe-4S] cluster within the mitosomes, with the exception of [2Fe-2S] ferredoxin, which is itself part of the ISC pathway. The overall uptake of iron into the cellular proteins remained unchanged as also observed for the grx5 knock out cell line. The pull-downs of all late ISC components were used to build the interactome of the pathway showing specific position of IscA2 due to its interaction with the outer mitosomal membrane proteins. Finally, the comparative analysis across Metamonada species suggested that the adaptation of the late ISC pathway identified in G. intestinalis occurred early in the evolution this of supergroup of eukaryotes.

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Section: Resultsmentioning

confidence: 99%

Adaptation of the late ISC pathway in the anaerobic mitochondrial organelles of Giardia intestinalis

Motyčková,

Voleman,

Najdrová

et al. 2023

PLoS Pathog

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“…All five Preaxostyla species contain ACS, while neither ASCT nor SCS were identified. ACS has a complicated evolutionary history in Metamonada characterized by multiple LGT events and gene losses (Leger et al 2017; Yazaki et al 2020; Vargová et al 2022). The majority of ACS homologs in Metamonada are predicted to function in the cytosol, with the only exception of the ACS2 isoform from S. salmonicida which functions in the MRO (Jerlström-Hultqvist et al 2013; Leger et al 2017).…”

Section: Resultsmentioning

confidence: 99%

“…The LGT events and gene losses [5,11,55]. The majority of ACS homologues in Metamonada are predicted to function in the cytosol, with the only exception of the ACS2 isoform from S. salmonicida that functions in the MRO [5,56].…”

Section: Inventory Of Enzymes For Extended Glycolysis Shows a Richer ...mentioning

confidence: 99%

Genomics of Preaxostyla Flagellates Illuminates the Path Towards the Loss of Mitochondria

Novák

Treitli

Pyrih

et al. 2022

Preprint

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Until recently, mitochondria were considered essential organelles impossible to truly lose in a lineage. This view changed in 2016, with the report that the oxymonadMonocercomonoides exilis, was the first known eukaryote without any mitochondrion. Questions remain, however, about whether this extends to the entire lineage and how this transition took place. Oxymonadida are a group of gut endobionts of insects, reptiles, and mammals. They are housed in the Preaxostyla (Metamonada), a protistan group that also contains free-living flagellates of generaTrimastixandParatrimastix. These latter two taxa harbor conspicuous mitochondrion-related organelles (MROs), while no mitochondria were reported for any oxymonad. Here we report genomic data sets of two Preaxostyla representatives, the free-livingParatrimastix pyriformisand the oxymonadBlattamonas nauphoetae. We note thatP. pyriformispossesses a set of unique or ancestral features among metamonads or eukaryotes, e.g.,p-cresol synthesis, UFMylation system, NAD+synthesis, selenium volatilization, or mercury methylation, demonstrating the biochemical versatility of this protist lineage. We performed thorough comparisons among all available genomic and transcriptomic data of Preaxostyla to corroborate both the absence of MRO in Oxymonadida and the nature of MROs present in other Preaxostyla and to decipher the evolutionary transition towards amitochondriality and endobiosis. Our results provide insights into the metabolic and endomembrane evolution, but most strikingly the data confirm the complete loss of mitochondria and every protein that has ever participated in the mitochondrion function for all three oxymonad species (M. exilis,B. nauphoetae, andStreblomastix strix) extending the amitochondriate status to the whole Oxymonadida.

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“…All five Preaxostyla species contain ACS, while neither ASCT nor SCS was identified. ACS has a complicated evolutionary history in Metamonada characterized by multiple LGT events and gene losses [5,11,55]. The majority of ACS homologues in Metamonada are predicted to function in the cytosol, with the only exception of the ACS2 isoform from S. salmonicida that functions in the MRO [5,56].…”

Section: Plos Geneticsmentioning

confidence: 99%

Genomics of Preaxostyla Flagellates Illuminates the Path Towards the Loss of Mitochondria

Novák,

Treitli,

Pyrih

et al. 2023

PLoS Genet

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The notion that mitochondria cannot be lost was shattered with the report of an oxymonad Monocercomonoides exilis, the first eukaryote arguably without any mitochondrion. Yet, questions remain about whether this extends beyond the single species and how this transition took place. The Oxymonadida is a group of gut endobionts taxonomically housed in the Preaxostyla which also contains free-living flagellates of the genera Trimastix and Paratrimastix. The latter two taxa harbour conspicuous mitochondrion-related organelles (MROs). Here we report high-quality genome and transcriptome assemblies of two Preaxostyla representatives, the free-living Paratrimastix pyriformis and the oxymonad Blattamonas nauphoetae. We performed thorough comparisons among all available genomic and transcriptomic data of Preaxostyla to further decipher the evolutionary changes towards amitochondriality, endobiosis, and unstacked Golgi. Our results provide insights into the metabolic and endomembrane evolution, but most strikingly the data confirm the complete loss of mitochondria for all three oxymonad species investigated (M. exilis, B. nauphoetae, and Streblomastix strix), suggesting the amitochondriate status is common to a large part if not the whole group of Oxymonadida. This observation moves this unique loss to 100 MYA when oxymonad lineage diversified.

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

Cited by 4 publications

References 79 publications

Adaptation of the late ISC pathway in the anaerobic mitochondrial organelles of Giardia intestinalis

Adaptation of the late ISC pathway in the anaerobic mitochondrial organelles of Giardia intestinalis

Genomics of Preaxostyla Flagellates Illuminates the Path Towards the Loss of Mitochondria

Genomics of Preaxostyla Flagellates Illuminates the Path Towards the Loss of Mitochondria

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