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.2020 Sep 9;287(1934):20201538.
doi: 10.1098/rspb.2020.1538. Epub 2020 Sep 2.

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

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

Euki Yazaki et al. Proc Biol Sci..

Abstract

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 oneBarthelona 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.

Keywords: metamonada; mitochondrion-related organelles; phylogenomics.

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Conflict of interest statement

We declare we have no competing interests.

Figures

Figure 1.
Figure 1.
Light micrographs ofBarthelona spp. examined in this study. Strains PAP020, FB11, LRM2, EYP1702 and PCE are shown in (a–e), respectively. Flagella are marked by arrowheads. Scale bars, 10 µm.
Figure 2.
Figure 2.
Global eukaryotic phylogeny inferred from small subunit ribosomal DNA sequences. The tree topology was inferred using the ML method and MLBPs and BPPs were mapped on the ML tree. The nodes marked by dots were supported by MLBPs of 100% and BPPs of 1.0. MLBPs less than 70% are not shown unless related to the position ofBarthelona spp. BPPs of 0.95 or more are marked by diamonds. (Online version in colour.)
Figure 3.
Figure 3.
Global eukaryotic phylogeny inferred from a 148-gene alignment. (a) The tree topology inferred using the ML method. MLBPs and BPPs were mapped on the ML tree. The Bayesian analysis recovered an identical overall topology. The nodes marked by dots were supported by MLBPs of 98% or more, and BPPs of 0.95 or more. MLBPs less than 60% and BPPs below 0.80 are not shown outside Metamonada. The bar graph for each taxon indicates the per cent coverage of the amino acid positions in the 148-gene analyses. (b) The results of an AU test comparing the ML tree and four trees that represent alternative positions ofBarthelona sp. strain PAP020. (Online version in colour.)
Figure 4.
Figure 4.
Predicted function of the MRO ofBarthelona sp. strain PAP020. (a) Transmission electron micrograph image of MRO of strain PAP020. MROs are shown by arrowheads. The nucleus is labelled as ‘N.’ Scale bar, 500 nm. (b) MRO protein candidates in strain PAP020. The candidates were mapped on H2-synthesis (labelled as ‘1’), pyruvate metabolism (2), substrate-level phosphorylation (3), amino acid metabolism (4), Fe–S cluster assembly (5), the antioxidant system (6) and protein modification (7) in theTrichomonas hydrogenosome (see electronic supplementary material, figure S4). As we predict that neither pyruvate metabolism nor substrate-level phosphorylation is present in the MRO, the two pathways are shown in white arrows. For the same reason, the MRO enzymes involved in pyruvate metabolism and substrate-level phosphorylation are omitted. Purple ellipses (dark grey ellipses in the grey-scale figure) indicate that the transcripts encoding hydrogenosomal/MRO protein candidates were detected in the PAP020 RNA-seq data. In the case of the ellipses surrounded by borders, their N-termini were predicted as transit peptides for mitochondria/MRO by MitoFates [41] and/or NommPred [42]. The purple/dark grey ellipses with no border indicate putative hydrogenosomal/MRO protein candidates lacking N-terminal sequence information or those with N-terminal extensions that were not predicted as mitochondria/MRO localizing by MitoFates or NommPred. For the proteins represented by grey ellipses (light grey ellipses in the grey-scale figure), we detected no corresponding transcript in the RNA-seq data. Two MEs found in this study were fused with MDH (shown as ‘ME*’). In this figure, we assume that pyruvate metabolism occurs in the cytosol of strain PAP020 (labelled as ‘2′’). Nevertheless, the MRO localizations of both MDH–ME and PFO cannot be discarded (see Discussion). See electronic supplementary material, table S2 for the complete protein names. Ala, alanine; Asp, aspartic acid; Cys, cysteine; Glu, glutamic acid; Gly, glycine; α-KG, α-ketoglutaric acid; Trp, tryptophan; OAA, oxaloacetic acid. (Online version in colour.)
Figure 5.
Figure 5.
Evolution of ATP generation in barthelonids, parabasalids and selected fornicates. In the clade of fornicates and barthelonids (Fornicata+ clade), substrate-level phosphorylation (blue) was lost on two separate branches. The cytosolic ACS2 (yellow), which was established at the base of the Fornicata + clade, was replaced by an evolutionarily distinct type of ACS (ACS1; red) during the evolution of fornicates.
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References

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