The free-living flagellate Paratrimastix pyriformis uses a distinct mitochondrial carrier to balance adenine nucleotide pools

Zítek, Justyna; King, Martin S.; Peña-Diaz, Priscila; Pyrihová, Eva; King, Alannah; Kunji, Edmund R. S.; Hampl, Vladimı́r

doi:10.1016/j.abb.2023.109638

Cited by 4 publications

(2 citation statements)

References 52 publications

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“…Indeed, PAPYR_2826 was recently confirmed by proteomics to be MRO-associated in P. pyriformis [17]. Finally, the search recovered homologues of mitochondrial matrix chaperones Cpn60 and Cpn10 and homologues of mitochondrial carrier family proteins used for export or import ATP and other metabolites [28]. Bacterial-type (NTT-like) nucleotide transporters [29], sporadically used for ATP transport, were not recovered neither by this search nor by targeted BLAST searches.…”

Section: Plos Geneticsmentioning

confidence: 98%

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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Section: Plos Geneticsmentioning

confidence: 98%

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

Novák,

Treitli,

Pyrih

et al. 2023

PLoS Genet

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“…MCF transporters transfer small molecules between mitochondria and cytosol. To gain insights into which moieties could be transferred in Archamoebae, we searched in their datasets for 53 MCF transporters previously identified in human [92] and placed them into the phylogenetic tree including transporters from yeast, Arabidopsis thaliana, Acanthamoeba castellanii and Dictyostelium discoideum [1,93,94]. Not surprisingly, the number of transporters was significantly smaller (Fig.…”

Section: Transportersmentioning

confidence: 99%

Comparative analysis of mitochondrion-related organelles in anaerobic amoebozoans

Záhonová,

Füssy,

Stairs

et al. 2023

Microbial Genomics

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Archamoebae comprises free-living or endobiotic amoebiform protists that inhabit anaerobic or microaerophilic environments and possess mitochondrion-related organelles (MROs) adapted to function anaerobically. We compared in silico reconstructed MRO proteomes of eight species (six genera) and found that the common ancestor of Archamoebae possessed very few typical components of the protein translocation machinery, electron transport chain and tricarboxylic acid cycle. On the other hand, it contained a sulphate activation pathway and bacterial iron–sulphur (Fe-S) assembly system of MIS-type. The metabolic capacity of the MROs, however, varies markedly within this clade. The glycine cleavage system is widely conserved among Archamoebae, except in Entamoeba, probably owing to its role in catabolic function or one-carbon metabolism. MRO-based pyruvate metabolism was dispensed within subgroups Entamoebidae and Rhizomastixidae, whereas sulphate activation could have been lost in isolated cases of Rhizomastix libera, Mastigamoeba abducta and Endolimax sp. The MIS (Fe-S) assembly system was duplicated in the common ancestor of Mastigamoebidae and Pelomyxidae, and one of the copies took over Fe-S assembly in their MRO. In Entamoebidae and Rhizomastixidae, we hypothesize that Fe-S cluster assembly in both compartments may be facilitated by dual localization of the single system. We could not find evidence for changes in metabolic functions of the MRO in response to changes in habitat; it appears that such environmental drivers do not strongly affect MRO reduction in this group of eukaryotes.

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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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The free-living flagellate Paratrimastix pyriformis uses a distinct mitochondrial carrier to balance adenine nucleotide pools

Cited by 4 publications

References 52 publications

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

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

Comparative analysis of mitochondrion-related organelles in anaerobic amoebozoans

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

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