Retortamonadida (with Notes on Carpediemonas-Like Organisms and Caviomonadidae)

Kulda, Jaroslav; Nohýnková, Eva; Čepička, Ivan

doi:10.1007/978-3-319-28149-0_3

Cited by 7 publications

(14 citation statements)

References 62 publications

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“…and Giardia intestinalis (figure 2), but statistical support was equivocal (MLBP 56%; BPP 0.86). This possible affinity between Barthelona and fornicates in the SSU rDNA phylogeny is provocative, as both lineages thrive in oxygen-poor environments and possess double-membrane-bounded MROs instead of typical mitochondria (see figure 4a for the putative MRO in strain PAP020) [43][44][45][46][47][48]. Thus, we took a phylogenomic approach to resolve the position of barthelonids more robustly within the tree of eukaryotes.…”

Section: Resultsmentioning

confidence: 99%

Barthelonids represent a deep-branching metamonad clade with mitochondrion-related organelles predicted to generate no ATP

et al. 2020

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We here report the phylogenetic position of barthelonids, small anaerobic flagellates previously examined using light microscopy alone. Barthelona spp. were isolated from geographically distinct regions and we established five laboratory strains. Transcriptomic data generated from one Barthelona strain (PAP020) were used for large-scale, multi-gene phylogenetic (phylogenomic) analyses. Our analyses robustly placed strain PAP020 at the base of the Fornicata clade, indicating that barthelonids represent a deep-branching metamonad clade. Considering the anaerobic/microaerophilic nature of barthelonids and preliminary electron microscopy observations on strain PAP020, we suspected that barthelonids possess functionally and structurally reduced mitochondria (i.e. mitochondrion-related organelles or MROs). The metabolic pathways localized in the MRO of strain PAP020 were predicted based on its transcriptomic data and compared with those in the MROs of fornicates. We here propose that strain PAP020 is incapable of generating ATP in the MRO, as no mitochondrial/MRO enzymes involved in substrate-level phosphorylation were detected. Instead, we detected a putative cytosolic ATP-generating enzyme (acetyl-CoA synthetase), suggesting that strain PAP020 depends on ATP generated in the cytosol. We propose two separate losses of substrate-level phosphorylation from the MRO in the clade containing barthelonids and (other) fornicates.

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Section: Resultsmentioning

confidence: 99%

Barthelonids represent a deep-branching metamonad clade with mitochondrion-related organelles predicted to generate no ATP

et al. 2020

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“…2), but statistical support was equivocal (MLBP 56%; BPP 0.86). This possible affinity between Barthelona and fornicates in the SSU rDNA phylogeny is provocative, as both lineages thrive in oxygen-poor environments and possess double-membrane bound MROs instead of typical mitochondria (Simpson and Patterson 1999; Tovar et al 2003; Yubuki et al 2007; Yubuki et al 2013; Kulda et al 2017; see Fig. S2 for the putative MRO in strain PAP020).…”

Section: Resultsmentioning

confidence: 99%

Barthelonids represent a deep-branching Metamonad clade with mitochondrion-related organelles generating no ATP

Yazaki

Kume

Shiratori

et al. 2019

Preprint

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23Running head: Phylogeny and putative MRO functions in a new metamonad clade. 25Abstract 28 We here report the phylogenetic position of barthelonids, small anaerobic flagellates 29 previously examined using light microscopy alone. Barthelona spp. were isolated from 30 geographically distinct regions and we established five laboratory strains. Transcriptomic data 31 generated from one Barthelona strain (PAP020) was used for large-scale, multi-gene 32 phylogenetic (phylogenomic) analyses. Our analyses robustly placed strain PAP020 at the 33 base of the Fornicata clade, indicating that barthelonids represent a deep-branching 34 Metamonad clade. Considering the anaerobic/microaerophilic nature of barthelonids and 35 preliminary electron microscopy observations on strain PAP020, we suspected that 36 barthelonids possess functionally and structurally reduced mitochondria (i.e. mitochondrion-37 related organelles or MROs). The metabolic pathways localized in the MRO of strain PAP020 38 were predicted based on its transcriptomic data and compared with those in the MROs of 39 fornicates. Strain PAP020 is most likely incapable of generating ATP in the MRO, as no 40 mitochondrial/MRO enzymes involved in substrate-level phosphorylation were detected. 41 Instead, we detected the putative cytosolic ATP-generating enzyme (acetyl-CoA synthetase), 42 suggesting that strain PAP020 depends on ATP generated in the cytosol. We propose two 43 separate losses of substrate-level phosphorylation from the MRO in the clade containing 44 barthelonids and (other) fornicates.45 46

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“…1 Retortamonads fall into two separate groups among Fornicata, with vertebrate commensals R. caviae and R. dobelli branching sister to Diplomonada. A, schematic tree based on SSU rDNA phylogeny from [ 1 ], also corroborated by multi-gene analyses [ 2 ]. B, phase-contrast light micrographs of retortamonads from this work; scale bar = 2 μm.…”

Section: Introductionmentioning

confidence: 90%

“…The recurrent flagellum is decorated by lateral vanes, passes through the cytostomal pouch and propels food particles into the cytopharynx, whereas the smooth anterior flagellum (or flagella) serves cell locomotion. Under adverse conditions or to disperse, Retortamonadida retract their flagella, develop a sturdy cell wall composed of filamentous material, and encyst [ 1 ]. Despite having ultrastructural similarities, Retortamonadida are polyphyletic, with Chilomastix and insect Retortamonas species being sister lineages and branching among Carpediemonas -like organisms, whereas Retortamonas species from vertebrate hosts are in fact sister to Diplomonadida ( Fig.…”

Section: Introductionmentioning

confidence: 99%

“…Most often, retortamonads are found as endocommensals in the digestive tracts of vertebrates and invertebrates, and a single known free-living species, Chilomastix cuspidata , inhabits hypoxic water sediments. Only two species are considered potentially pathogenic, C. mesnili and C. gallinarum [ 1 ]. The subjects of this work are known as vertebrate commensals.…”

Section: Introductionmentioning

confidence: 99%

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Retortamonads from vertebrate hosts share features of anaerobic metabolism and pre-adaptations to parasitism with diplomonads

Füssy

Vinopalová

Treitli

et al. 2021

Parasitology International

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Although the mitochondria of extant eukaryotes share a single origin, functionally these organelles diversified to a great extent, reflecting lifestyles of the organisms that host them. In anaerobic protists of the group Metamonada, mitochondria are present in reduced forms (also termed hydrogenosomes or mitosomes) and a complete loss of mitochondrion in Monocercomonoides exilis (Metamonada:Preaxostyla) has also been reported. Within metamonads, retortamonads from the gastrointestinal tract of vertebrates form a sister group to parasitic diplomonads (e.g. Giardia and Spironucleus ) and have also been hypothesized to completely lack mitochondria. We obtained transcriptomic data from Retortamonas dobelli and R. caviae and searched for enzymes of the core metabolism as well as mitochondrion- and parasitism-related proteins. Our results indicate that retortamonads have a streamlined metabolism lacking pathways for metabolites they are probably capable of obtaining from prey bacteria or their environment, reminiscent of the biochemical arrangement in other metamonads. Retortamonads were surprisingly found do encode homologs of components of Giardia ‘s remarkable ventral disk, as well as homologs of regulatory NEK kinases and secreted lytic enzymes known for involvement in host colonization by Giardia . These can be considered pre-adaptations of these intestinal microorganisms to parasitism. Furthermore, we found traces of the mitochondrial metabolism represented by iron‑sulfur cluster assembly subunits, subunits of mitochondrial translocation and chaperone machinery and, importantly, [FeFe]‑hydrogenases and hydrogenase maturases (HydE, HydF and HydG). Altogether, our results strongly suggest that a remnant mitochondrion is still present.

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Retortamonadida (with Notes on Carpediemonas-Like Organisms and Caviomonadidae)

Cited by 7 publications

References 62 publications

Barthelonids represent a deep-branching metamonad clade with mitochondrion-related organelles predicted to generate no ATP

Barthelonids represent a deep-branching metamonad clade with mitochondrion-related organelles predicted to generate no ATP

Barthelonids represent a deep-branching Metamonad clade with mitochondrion-related organelles generating no ATP

Retortamonads from vertebrate hosts share features of anaerobic metabolism and pre-adaptations to parasitism with diplomonads

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