Most cited article - PubMed ID 36898426
Ancient and pervasive expansion of adaptin-related vesicle coat machinery across Parabasalia
The early evolution of eukaryotes and their adaptations to low-oxygen environments are fascinating open questions in biology. Genome-scale data from novel eukaryotes, and particularly from free-living lineages, are the key to answering these questions. The Parabasalia are a major group of anaerobic eukaryotes that form the most speciose lineage of Metamonada. The most well-studied are parasitic parabasalids, including Trichomonas vaginalis and Tritrichomonas foetus, but very little genome-scale data are available for free-living members of the group. Here, we sequenced the transcriptome of Pseudotrichomonas keilini, a free-living parabasalian. Comparative genomic analysis indicated that P. keilini possesses a metabolism and gene complement that are in many respects similar to its parasitic relative T. vaginalis and that in the time since their most recent common ancestor, it is the T. vaginalis lineage that has experienced more genomic change, likely due to the transition to a parasitic lifestyle. Features shared between P. keilini and T. vaginalis include a hydrogenosome (anaerobic mitochondrial homolog) that we predict to function much as in T. vaginalis and a complete glycolytic pathway that is likely to represent one of the primary means by which P. keilini obtains ATP. Phylogenomic analysis indicates that P. keilini branches within a clade of endobiotic parabasalids, consistent with the hypothesis that different parabasalid lineages evolved toward parasitic or free-living lifestyles from an endobiotic, anaerobic, or microaerophilic common ancestor.
Symbiotic relationships between eukaryotes and prokaryotes played pivotal roles in the evolution of life and drove the emergence of specialized symbiotic structures in animals, plants and fungi. The host-evolved symbiotic structures of microbial eukaryotes - the vast majority of such hosts in nature - remain largely unstudied. Here we describe highly structured symbiosomes within three free-living anaerobic protists (Anaeramoeba spp.). We dissect this symbiosis using complete genome sequencing and transcriptomics of host and symbiont cells coupled with fluorescence in situ hybridization, and 3D reconstruction using focused-ion-beam scanning electron microscopy. The emergence of the symbiosome is underpinned by expansion of gene families encoding regulators of membrane trafficking and phagosomal maturation and extensive bacteria-to-eukaryote lateral transfer. The symbionts reside deep within a symbiosomal membrane network that enables metabolic syntrophy by precisely positioning sulfate-reducing bacteria alongside host hydrogenosomes. Importantly, the symbionts maintain connections to the Anaeramoeba plasma membrane, blurring traditional boundaries between ecto- and endosymbiosis.
Early endosomes sort transmembrane cargo either for lysosomal degradation or retrieval to the plasma membrane or the Golgi complex. Endosomal retrieval in eukaryotes is governed by the anciently homologous retromer or retriever complexes. Each comprises a core tri-protein subcomplex, membrane-deformation proteins and interacting partner complexes, together retrieving a variety of known cargo proteins. Trichomonas vaginalis, a sexually transmitted human parasite, uses the endomembrane system for pathogenesis. It has massively and selectively expanded its endomembrane protein complement, the evolutionary path of which has been largely unexplored. Our molecular evolutionary study of retromer, retriever and associated machinery in parabasalids and its free-living sister lineage of Anaeramoeba demonstrates specific expansion of the retromer machinery, contrasting with the retriever components. We also observed partial loss of the Commander complex and sorting nexins in Parabasalia but complete retention in Anaeramoeba. Notably, we identified putative parabasalid sorting nexin analogs. Finally, we report the first retriever protein localization in a non-metazoan group along with retromer protein localization in T. vaginalis.
- Keywords
- Endomembrane, Evolution, Parabasalids, Phylogenomics, Retriever, Retromer,
- MeSH
- Endosomes * metabolism MeSH
- Phylogeny MeSH
- Golgi Apparatus metabolism MeSH
- Humans MeSH
- Evolution, Molecular MeSH
- Protozoan Proteins metabolism genetics MeSH
- Protein Transport MeSH
- Trichomonas vaginalis metabolism genetics MeSH
- Sorting Nexins metabolism genetics MeSH
- Animals MeSH
- Check Tag
- Humans MeSH
- Animals MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
- Names of Substances
- Protozoan Proteins MeSH
- Sorting Nexins MeSH
