Diplonemids – A Review on "New" Flagellates on the Oceanic Block

Tashyreva, Daria; Simpson, Alastair G. B.; Prokopchuk, Galina; Škodová-Sveráková, Ingrid; Butenko, Anzhelika; Hammond, Michael; George, Emma E.; Flegontova, Olga; Záhonová, Kristína; Faktorová, Drahomíra; Yabuki, Akinori; Horák, Aleš; Keeling, Patrick J.; Lukeš, Julius

doi:10.1016/j.protis.2022.125868

Cited by 18 publications

(20 citation statements)

References 91 publications

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“…A comparable although more complicated situation is found in the distantly related diplonemid H. phaeocysticola (Tashyreva et al, 2022) where we identified six putative PFK sequences in its transcriptome database (not shown). Two belong to the 'Long' clade, with one possessing a PTS1 (-AHL) and being mostly similar to the D. papillatum β-PFK1 and less to E. gracilis β-PFK (51 and 31% identity, respectively).…”

Section: Figuresupporting

confidence: 61%

“…If it was in a common ancestor of Diplonemea and Kinetoplastea in which glycolysis became uniquely compartmentalised within peroxisomes, then it is reasonable to estimate that this ancestor lived >600 million years ago, most likely in the oceans, at a point in Earth’s history when only the uppermost regions of the oceans were considered oxygenated ( Holland, 2006 ; Mills et al, 2022 ). Diplonemid life cycles turn to be surprisingly complex ( Tahyreva et al, 2022 ). Environmental change is likely a cue for cellular differentiation, as it is in many microbial eukaryotes.…”

Section: Introductionmentioning

confidence: 99%

“… 1 Note: Diplonemid diversity has only begun to be truly recognised during the last 12–15 years. Consequently, taxonomic reassignment should see reclassification of Diplonema papillatum to Paradiplonema papillatum , separate from other species in the genus Diplonema ( Tahyreva et al, 2022 ). Here, we use nomenclature still in use.…”

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confidence: 99%

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Delineating transitions during the evolution of specialised peroxisomes: Glycosome formation in kinetoplastid and diplonemid protists

Andrade-Alviárez

Bonive-Boscan

Cáceres

et al. 2022

Front. Cell Dev. Biol.

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One peculiarity of protists belonging to classes Kinetoplastea and Diplonemea within the phylum Euglenozoa is compartmentalisation of most glycolytic enzymes within peroxisomes that are hence called glycosomes. This pathway is not sequestered in peroxisomes of the third Euglenozoan class, Euglenida. Previous analysis of well-studied kinetoplastids, the ‘TriTryps’ parasites Trypanosoma brucei, Trypanosoma cruzi and Leishmania spp., identified within glycosomes other metabolic processes usually not present in peroxisomes. In addition, trypanosomatid peroxins, i.e. proteins involved in biogenesis of these organelles, are divergent from human and yeast orthologues. In recent years, genomes, transcriptomes and proteomes for a variety of euglenozoans have become available. Here, we track the possible evolution of glycosomes by querying these databases, as well as the genome of Naegleria gruberi, a non-euglenozoan, which belongs to the same protist supergroup Discoba. We searched for orthologues of TriTryps proteins involved in glycosomal metabolism and biogenesis. Predicted cellular location(s) of each metabolic enzyme identified was inferred from presence or absence of peroxisomal-targeting signals. Combined with a survey of relevant literature, we refine extensively our previously postulated hypothesis about glycosome evolution. The data agree glycolysis was compartmentalised in a common ancestor of the kinetoplastids and diplonemids, yet additionally indicates most other processes found in glycosomes of extant trypanosomatids, but not in peroxisomes of other eukaryotes were either sequestered in this ancestor or shortly after separation of the two lineages. In contrast, peroxin divergence is evident in all euglenozoans. Following their gain of pathway complexity, subsequent evolution of peroxisome/glycosome function is complex. We hypothesize compartmentalisation in glycosomes of glycolytic enzymes, their cofactors and subsequently other metabolic enzymes provided selective advantage to kinetoplastids and diplonemids during their evolution in changing marine environments. We contend two specific properties derived from the ancestral peroxisomes were key: existence of nonselective pores for small solutes and the possibility of high turnover by pexophagy. Critically, such pores and pexophagy are characterised in extant trypanosomatids. Increasing amenability of free-living kinetoplastids and recently isolated diplonemids to experimental study means our hypothesis and interpretation of bioinformatic data are suited to experimental interrogation.

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Section: Figuresupporting

confidence: 61%

Section: Introductionmentioning

confidence: 99%

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Delineating transitions during the evolution of specialised peroxisomes: Glycosome formation in kinetoplastid and diplonemid protists

Andrade-Alviárez

Bonive-Boscan

Cáceres

et al. 2022

Front. Cell Dev. Biol.

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“…Here, we show that diplonemids (Diplonemea, Euglenozoa), a group of biflagellated heterotrophic protists [29–31], are capable of massive intracellular accumulation of Sr 2+ and Ba 2+ . Specifically, three cultivable diplonemids accumulate celestite and barite crystals in intracellular concentration of Sr 2+ much greater than in other organisms [10, 16].…”

Section: Introductionmentioning

confidence: 99%

Massive accumulation of strontium and barium in diplonemid protists

Pilátová

Tashyreva

Týč

et al. 2022

Preprint

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Barium (Ba) and strontium (Sr) are often used as proxies for the reconstruction of past marine productivity and global climate. The ability to accumulate Ba2+ and Sr2+ in the form of crystals is rare among eukaryotes. Here we report that unicellular heterotrophs called diplonemids (Euglenozoa), one of the most abundant groups of marine planktonic protists, accumulate conspicuous amounts of these trace elements in the form of intracellular barite (BaSO4) and celestite (SrSO4) crystals, in concentrations greater than in other known Ba/Sr-accumulating organisms. Moreover, these flagellates can uptake Sr2+ exclusively or together with Ba2+ and form (Ba,Sr)SO4. One species, Namystinia karyoxenos, is naturally capable of intracellular accumulation of Ba2+ and Sr2+ 42,000 and 10,000 times relative to the surrounding medium. Altering the amounts of both elements in the medium resulted in corresponding changes in the quantity and composition of crystals. Planktonic copepods fed with diplonemids produce celestite-rich fecal pellets, which facilitate deposition of these minerals on the seafloor. We propose that diplonemids, which emerged during the Neoproterozoic era, qualify as impactful players of Ba2+/Sr2+ cycling in the ocean that possibly contributed to sedimentary rock formation over long geological periods.

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“…They form a sister group to the mostly parasitic kinetoplastids and represent the third arm of the Euglenozoa, with representative genome and/or transcriptomes available from all lineages. Several diplonemids are bacterivorous (Prokopchuk et al, 2022), although the lifestyle of most species remains unknown, and likely ranges from phagotrophy through predation to parasitism (Tashyreva et al, 2022). Importantly, these ecologically and evolutionary highly relevant protists recently joined a rather narrow group of genetically tractable organisms (Faktorová et al, 2020a), and functions can now be studied in the model species Paradiplonema papillatum (renamed from Diplonema papillatum ) (Faktorová et al, 2020b; Tashyreva et al, 2022).…”

Section: Introductionmentioning

confidence: 99%

Functional differentiation of Sec13 paralogs in the euglenozoan protists

Faktorová

Záhonová

Benz

et al. 2022

Preprint

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The β-propeller protein Sec13 plays roles in at least three distinct processes by virtue of being a component of the COPII endoplasmic reticulum export vesicle coat, the nuclear pore complex (NPC) and the Seh1-associated (SEA)/GATOR nutrient-sensing complex, suggesting that regulatory mechanisms coordinating these cellular activities may operate via Sec13. The NPC, COPII and SEA/GATOR are all ancient features of eukaryotic cells. In the vast majority of eukaryotes, a single Sec13 gene is present, but here we report that the Euglenozoa, a lineage encompassing the diplonemid, kinetoplastid and euglenid protists contain two Sec13 paralogs. Furthermore, based on protein interactions and localization studies we show that Sec13 functions in diplonemids are divided between the Sec13a and Sec13b paralogs. Specifically, Sec13a interacts with COPII and the NPC, but Sec13b interacts with Sec16 and components of the SEA/GATOR complex. We infer that euglenozoan Sec13a is responsible for NPC functions and canonical anterograde transport activities while Sec13b acts within nutrient and autophagy-related pathways, indicating a fundamentally distinct organization of coatomer complexes in the euglenozoan flagellates.

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Diplonemids – A Review on "New" Flagellates on the Oceanic Block

Cited by 18 publications

References 91 publications

Delineating transitions during the evolution of specialised peroxisomes: Glycosome formation in kinetoplastid and diplonemid protists

Delineating transitions during the evolution of specialised peroxisomes: Glycosome formation in kinetoplastid and diplonemid protists

Massive accumulation of strontium and barium in diplonemid protists

Functional differentiation of Sec13 paralogs in the euglenozoan protists

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