A eukaryote-wide perspective on the diversity and evolution of the ARF GTPase protein family

Vargová, Romana; Wideman, Jeremy G.; Derelle, Romain; Klimeš, Vladimír; Kahn, Richard; Dacks, Joel B.; Eliáš, Marek

doi:10.1101/2020.10.31.363457

Cited by 3 publications

(3 citation statements)

References 163 publications

(239 reference statements)

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“…3, Supplementary file 6). These data, together with previously published observations (Vargová et al 2021), are indicative of Golgi bodies with multiple anterograde and retrograde pathways entering and exiting the organelle present in all Preaxostyla species.…”

Section: Resultssupporting

confidence: 88%

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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Section: Resultssupporting

confidence: 88%

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

Novák

Treitli

Pyrih

et al. 2022

Preprint

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“…The ARF family of regulatory GTPases is large, with ~30 mammalian members that are highly conserved throughout eukaryotic evolution, 16 of which are predicted to have been present in the last eukaryotic common ancestor (Vargova et al, 2021). ARFs and ARLs regulate a range of essential cellular processes including roles in membrane traffic, primary cilia, mitochondria, tubulin biogenesis, and microtubule dynamics (Cherfils, 2014;Jackson and Bouvet, 2014;Sztul et al, 2019;Casalou et al, 2020;Fisher et al, 2020).…”

Section: Introductionmentioning

confidence: 99%

The ARF GAPs ELMOD1 and ELMOD3 act at the Golgi and cilia to regulate ciliogenesis and ciliary protein traffic

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Dewees

et al. 2022

MBoC

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ELMODs are a family of three mammalian paralogs that display GTPase activating protein (GAP) activity towards a uniquely broad array of ADP-ribosylation factor (ARF) family GTPases that includes ARF-like (ARL) proteins. ELMODs are ubiquitously expressed in mammalian tissues, highly conserved across eukaryotes, and ancient in origin, being present in the last eukaryotic common ancestor. We described functions of ELMOD2 in immortalized mouse embryonic fibroblasts (MEFs) in the regulation of cell division, microtubules, ciliogenesis, and mitochondrial fusion. Here, using similar strategies with the paralogs ELMOD1 and ELMOD3, we identify novel functions and locations of these cell regulators and compare them to those of ELMOD2, allowing determination of functional redundancy among the family members. We found strong similarities in phenotypes resulting from deletion of either Elmod1 or Elmod3 and marked differences from those arising in Elmod2 deletion lines. Deletion of either Elmod1 or Elmod3 results in the decreased ability of cells to form primary cilia, loss of a subset of proteins from cilia, and accumulation of some ciliary proteins at the Golgi, predicted to result from compromised traffic from the Golgi to cilia. These phenotypes are reversed upon activating mutant expression of either ARL3 or ARL16, linking their roles to ELMOD1/3 actions.

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“…Homologs of each trafficking family were identified (1–3), and all pan-eukaryotic orthologs were identified via phylogenetic analysis with known marker sequences (4–5). Any unclassified sequences (6) were then ran in additional phylogenetic analyses (7); some formed monophyletic clades (LSPs; 8) while others remained unclassified (9). B) Summary of presumed patterns of gain and loss of LSPs in study taxa.…”

Section: Resultsmentioning

confidence: 99%

Evolution of lineage-specific trafficking proteins and a novel post-Golgi trafficking pathway in Apicomplexa

Klinger

Jiménez-Ruiz

Mourier

et al. 2022

Preprint

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The Organelle Paralogy Hypothesis (OPH) posits a mechanism to explain the evolution of non-endosymbiotically derived organelles, predicting that lineage-specific pathways organelles should result when identity-encoding membrane trafficking components duplicate and co-evolve. Here we investigate the presence of such lineage-specific membrane-trafficking machinery paralogs in the globally important lineage of parasites, the Apicomplexa. Using a new phylogenetic workflow, we are able to identify 18 novel paralogs of known membrane-trafficking machinery, the emergence of several of which correlate with the presence of new endomembrane organelles in apicomplexans or their larger lineage. Gene coregulation analysis of a large set of membrane-trafficking proteins in Toxoplasma both corroborate known molecular cell biological interactions between characterized machinery and suggest involvement of many of these new components into established pathways for biogenesis of or trafficking to the microneme and rhoptry invasion organelles. Moreover, focused molecular parasitological analysis of the apicomplexan Arf-like small GTPases, and the ArlX3 protein specifically, revealed a novel post-Golgi trafficking pathways involved in delivery of proteins to micronemes and rhoptries, with knock down demonstrating reduced invasion capacity. The totality of our data has identified an unforeseen post-Golgi trafficking pathway in apicomplexans and is consistent with the OPH mechanism acting to produce novel endomembrane pathways or organelles at various evolutionary stages across the Alveolate lineage.

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A eukaryote-wide perspective on the diversity and evolution of the ARF GTPase protein family

Cited by 3 publications

References 163 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

The ARF GAPs ELMOD1 and ELMOD3 act at the Golgi and cilia to regulate ciliogenesis and ciliary protein traffic

Evolution of lineage-specific trafficking proteins and a novel post-Golgi trafficking pathway in Apicomplexa

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