Combined nanometric and phylogenetic analysis of unique endocytic compartments in Giardia lamblia sheds light on the evolution of endocytosis in Metamonada
Abstract Background Giardia lamblia, a parasitic protist of the Metamonada supergroup, has evolved one of the most diverged endocytic compartment systems investigated so far. Peripheral endocytic compartments, currently known as peripheral vesicles or vacuoles (PVs), perform bulk uptake of fluid pha...
| Main Authors: | , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
BMC
2022-09-01
|
| Series: | BMC Biology |
| Subjects: | |
| Online Access: | https://doi.org/10.1186/s12915-022-01402-3 |
| _version_ | 1828175419071791104 |
|---|---|
| author | Rui Santos Ásgeir Ástvaldsson Shweta V. Pipaliya Jon Paulin Zumthor Joel B. Dacks Staffan Svärd Adrian B. Hehl Carmen Faso |
| author_facet | Rui Santos Ásgeir Ástvaldsson Shweta V. Pipaliya Jon Paulin Zumthor Joel B. Dacks Staffan Svärd Adrian B. Hehl Carmen Faso |
| author_sort | Rui Santos |
| collection | DOAJ |
| description | Abstract Background Giardia lamblia, a parasitic protist of the Metamonada supergroup, has evolved one of the most diverged endocytic compartment systems investigated so far. Peripheral endocytic compartments, currently known as peripheral vesicles or vacuoles (PVs), perform bulk uptake of fluid phase material which is then digested and sorted either to the cell cytosol or back to the extracellular space. Results Here, we present a quantitative morphological characterization of these organelles using volumetric electron microscopy and super-resolution microscopy (SRM). We defined a morphological classification for the heterogenous population of PVs and performed a comparative analysis of PVs and endosome-like organelles in representatives of phylogenetically related taxa, Spironucleus spp. and Tritrichomonas foetus. To investigate the as-yet insufficiently understood connection between PVs and clathrin assemblies in G. lamblia, we further performed an in-depth search for two key elements of the endocytic machinery, clathrin heavy chain (CHC) and clathrin light chain (CLC), across different lineages in Metamonada. Our data point to the loss of a bona fide CLC in the last Fornicata common ancestor (LFCA) with the emergence of a protein analogous to CLC (GlACLC) in the Giardia genus. Finally, the location of clathrin in the various compartments was quantified. Conclusions Taken together, this provides the first comprehensive nanometric view of Giardia’s endocytic system architecture and sheds light on the evolution of GlACLC analogues in the Fornicata supergroup and, specific to Giardia, as a possible adaptation to the formation and maintenance of stable clathrin assemblies at PVs. |
| first_indexed | 2024-04-12T04:27:50Z |
| format | Article |
| id | doaj.art-935919f8ee174cad894572d8814a70b2 |
| institution | Directory Open Access Journal |
| issn | 1741-7007 |
| language | English |
| last_indexed | 2024-04-12T04:27:50Z |
| publishDate | 2022-09-01 |
| publisher | BMC |
| record_format | Article |
| series | BMC Biology |
| spelling | doaj.art-935919f8ee174cad894572d8814a70b22022-12-22T03:48:02ZengBMCBMC Biology1741-70072022-09-0120112310.1186/s12915-022-01402-3Combined nanometric and phylogenetic analysis of unique endocytic compartments in Giardia lamblia sheds light on the evolution of endocytosis in MetamonadaRui Santos0Ásgeir Ástvaldsson1Shweta V. Pipaliya2Jon Paulin Zumthor3Joel B. Dacks4Staffan Svärd5Adrian B. Hehl6Carmen Faso7Institute of Parasitology, University of ZürichDepartment of Cell and Molecular Biology, University of UppsalaDivision of Infectious Diseases, Department of Medicine, University of AlbertaAmt für Lebensmittelsicherheit und Tiergesundheit GraubündenDivision of Infectious Diseases, Department of Medicine, University of AlbertaDepartment of Cell and Molecular Biology, University of UppsalaInstitute of Parasitology, University of ZürichInstitute of Cell Biology, University of BernAbstract Background Giardia lamblia, a parasitic protist of the Metamonada supergroup, has evolved one of the most diverged endocytic compartment systems investigated so far. Peripheral endocytic compartments, currently known as peripheral vesicles or vacuoles (PVs), perform bulk uptake of fluid phase material which is then digested and sorted either to the cell cytosol or back to the extracellular space. Results Here, we present a quantitative morphological characterization of these organelles using volumetric electron microscopy and super-resolution microscopy (SRM). We defined a morphological classification for the heterogenous population of PVs and performed a comparative analysis of PVs and endosome-like organelles in representatives of phylogenetically related taxa, Spironucleus spp. and Tritrichomonas foetus. To investigate the as-yet insufficiently understood connection between PVs and clathrin assemblies in G. lamblia, we further performed an in-depth search for two key elements of the endocytic machinery, clathrin heavy chain (CHC) and clathrin light chain (CLC), across different lineages in Metamonada. Our data point to the loss of a bona fide CLC in the last Fornicata common ancestor (LFCA) with the emergence of a protein analogous to CLC (GlACLC) in the Giardia genus. Finally, the location of clathrin in the various compartments was quantified. Conclusions Taken together, this provides the first comprehensive nanometric view of Giardia’s endocytic system architecture and sheds light on the evolution of GlACLC analogues in the Fornicata supergroup and, specific to Giardia, as a possible adaptation to the formation and maintenance of stable clathrin assemblies at PVs.https://doi.org/10.1186/s12915-022-01402-3EndocytosisSuper-resolution microscopy (SRM)Volumetric electron microscopyPeripheral endocytic compartments (PECs)Convergent evolutionMetamonada |
| spellingShingle | Rui Santos Ásgeir Ástvaldsson Shweta V. Pipaliya Jon Paulin Zumthor Joel B. Dacks Staffan Svärd Adrian B. Hehl Carmen Faso Combined nanometric and phylogenetic analysis of unique endocytic compartments in Giardia lamblia sheds light on the evolution of endocytosis in Metamonada BMC Biology Endocytosis Super-resolution microscopy (SRM) Volumetric electron microscopy Peripheral endocytic compartments (PECs) Convergent evolution Metamonada |
| title | Combined nanometric and phylogenetic analysis of unique endocytic compartments in Giardia lamblia sheds light on the evolution of endocytosis in Metamonada |
| title_full | Combined nanometric and phylogenetic analysis of unique endocytic compartments in Giardia lamblia sheds light on the evolution of endocytosis in Metamonada |
| title_fullStr | Combined nanometric and phylogenetic analysis of unique endocytic compartments in Giardia lamblia sheds light on the evolution of endocytosis in Metamonada |
| title_full_unstemmed | Combined nanometric and phylogenetic analysis of unique endocytic compartments in Giardia lamblia sheds light on the evolution of endocytosis in Metamonada |
| title_short | Combined nanometric and phylogenetic analysis of unique endocytic compartments in Giardia lamblia sheds light on the evolution of endocytosis in Metamonada |
| title_sort | combined nanometric and phylogenetic analysis of unique endocytic compartments in giardia lamblia sheds light on the evolution of endocytosis in metamonada |
| topic | Endocytosis Super-resolution microscopy (SRM) Volumetric electron microscopy Peripheral endocytic compartments (PECs) Convergent evolution Metamonada |
| url | https://doi.org/10.1186/s12915-022-01402-3 |
| work_keys_str_mv | AT ruisantos combinednanometricandphylogeneticanalysisofuniqueendocyticcompartmentsingiardialambliashedslightontheevolutionofendocytosisinmetamonada AT asgeirastvaldsson combinednanometricandphylogeneticanalysisofuniqueendocyticcompartmentsingiardialambliashedslightontheevolutionofendocytosisinmetamonada AT shwetavpipaliya combinednanometricandphylogeneticanalysisofuniqueendocyticcompartmentsingiardialambliashedslightontheevolutionofendocytosisinmetamonada AT jonpaulinzumthor combinednanometricandphylogeneticanalysisofuniqueendocyticcompartmentsingiardialambliashedslightontheevolutionofendocytosisinmetamonada AT joelbdacks combinednanometricandphylogeneticanalysisofuniqueendocyticcompartmentsingiardialambliashedslightontheevolutionofendocytosisinmetamonada AT staffansvard combinednanometricandphylogeneticanalysisofuniqueendocyticcompartmentsingiardialambliashedslightontheevolutionofendocytosisinmetamonada AT adrianbhehl combinednanometricandphylogeneticanalysisofuniqueendocyticcompartmentsingiardialambliashedslightontheevolutionofendocytosisinmetamonada AT carmenfaso combinednanometricandphylogeneticanalysisofuniqueendocyticcompartmentsingiardialambliashedslightontheevolutionofendocytosisinmetamonada |