Essential role of the conserved oligomeric Golgi complex in Toxoplasma gondii
ABSTRACTSurvival of the apicomplexan parasite Toxoplasma gondii depends on the proper functioning of many glycosylated proteins. Glycosylation is performed in the major membranous organelles ER and Golgi apparatus that constitute a significant portion of the intracellular secretory system. The secre...
| Main Authors: | , , , , , , , |
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| Format: | Article |
| Language: | English |
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American Society for Microbiology
2023-12-01
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| Series: | mBio |
| Subjects: | |
| Online Access: | https://journals.asm.org/doi/10.1128/mbio.02513-23 |
| _version_ | 1797378891066638336 |
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| author | Clem Marsilia Mrinalini Batra Irina D. Pokrovskaya Changqi Wang Dale Chaput Daria A. Naumova Vladimir V. Lupashin Elena S. Suvorova |
| author_facet | Clem Marsilia Mrinalini Batra Irina D. Pokrovskaya Changqi Wang Dale Chaput Daria A. Naumova Vladimir V. Lupashin Elena S. Suvorova |
| author_sort | Clem Marsilia |
| collection | DOAJ |
| description | ABSTRACTSurvival of the apicomplexan parasite Toxoplasma gondii depends on the proper functioning of many glycosylated proteins. Glycosylation is performed in the major membranous organelles ER and Golgi apparatus that constitute a significant portion of the intracellular secretory system. The secretory pathway is bidirectional: cargo is delivered to target organelles in the anterograde direction, while retrograde flow maintains the membrane balance and proper localization of glycosylation machinery. Despite the vital role of the Golgi in parasite infectivity, little is known about its biogenesis in apicomplexan parasites. In this study, we examined the T. gondii conserved oligomeric Golgi (COG) complex and determined that contrary to predictions, T. gondii expresses the entire eight-subunit complex and that each complex subunit is essential for tachyzoite growth. Deprivation of the COG complex induces a pronounced effect on Golgi and ER membranes, which suggests that the T. gondii COG complex has a wider role in intracellular membrane trafficking. We demonstrated that besides its conservative role in retrograde intra-Golgi trafficking, the COG complex also interacted with anterograde and novel transport machinery. Furthermore, we identified coccidian-specific components of the Golgi transport system: TgUlp1 and TgGlp1. Protein structure and phylogenetic analyses revealed that TgUlp1 is an adaptation of the conservative Golgi tethering factor Uso1/p115. TgUlp1 and together with Golgi-localized TgGlp1 showed dominant interactions with the trafficking machinery that was predicted to operate endosome-to-Golgi recycling. Together, our study showed that T. gondii has expanded the function of the conservative Golgi tethering COG complex and evolved additional regulators of transport that are likely to serve parasite-specific secretory organelles.IMPORTANCEThe Golgi is an essential eukaryotic organelle and a major place for protein sorting and glycosylation. Among apicomplexan parasites, Toxoplasma gondii retains the most developed Golgi structure and produces many glycosylated factors necessary for parasite survival. Despite its importance, Golgi function received little attention in the past. In the current study, we identified and characterized the conserved oligomeric Golgi complex and its novel partners critical for protein transport in T. gondii tachyzoites. Our results suggest that T. gondii broadened the role of the conserved elements and reinvented the missing components of the trafficking machinery to accommodate the specific needs of the opportunistic parasite T. gondii. |
| first_indexed | 2024-03-08T20:14:10Z |
| format | Article |
| id | doaj.art-8b17efa4fcee4d43b024e78374b08cb9 |
| institution | Directory Open Access Journal |
| issn | 2150-7511 |
| language | English |
| last_indexed | 2024-03-08T20:14:10Z |
| publishDate | 2023-12-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | mBio |
| spelling | doaj.art-8b17efa4fcee4d43b024e78374b08cb92023-12-22T19:53:44ZengAmerican Society for MicrobiologymBio2150-75112023-12-0114610.1128/mbio.02513-23Essential role of the conserved oligomeric Golgi complex in Toxoplasma gondiiClem Marsilia0Mrinalini Batra1Irina D. Pokrovskaya2Changqi Wang3Dale Chaput4Daria A. Naumova5Vladimir V. Lupashin6Elena S. Suvorova7Division of Infectious Diseases, Department of Internal Medicine, Morsani College of Medicine, University of South Florida, Tampa, Florida, USADivision of Infectious Diseases, Department of Internal Medicine, Morsani College of Medicine, University of South Florida, Tampa, Florida, USADepartment of Physiology and Cell Biology, College of Medicine, University of Arkansas for Medical Sciences, Little Rock, Arkansas, USACollege of Public Health, University of South Florida, Tampa, Florida, USAProteomics Core, College of Arts and Sciences, University of South Florida, Tampa, Florida, USADivision of Infectious Diseases, Department of Internal Medicine, Morsani College of Medicine, University of South Florida, Tampa, Florida, USADepartment of Physiology and Cell Biology, College of Medicine, University of Arkansas for Medical Sciences, Little Rock, Arkansas, USADivision of Infectious Diseases, Department of Internal Medicine, Morsani College of Medicine, University of South Florida, Tampa, Florida, USAABSTRACTSurvival of the apicomplexan parasite Toxoplasma gondii depends on the proper functioning of many glycosylated proteins. Glycosylation is performed in the major membranous organelles ER and Golgi apparatus that constitute a significant portion of the intracellular secretory system. The secretory pathway is bidirectional: cargo is delivered to target organelles in the anterograde direction, while retrograde flow maintains the membrane balance and proper localization of glycosylation machinery. Despite the vital role of the Golgi in parasite infectivity, little is known about its biogenesis in apicomplexan parasites. In this study, we examined the T. gondii conserved oligomeric Golgi (COG) complex and determined that contrary to predictions, T. gondii expresses the entire eight-subunit complex and that each complex subunit is essential for tachyzoite growth. Deprivation of the COG complex induces a pronounced effect on Golgi and ER membranes, which suggests that the T. gondii COG complex has a wider role in intracellular membrane trafficking. We demonstrated that besides its conservative role in retrograde intra-Golgi trafficking, the COG complex also interacted with anterograde and novel transport machinery. Furthermore, we identified coccidian-specific components of the Golgi transport system: TgUlp1 and TgGlp1. Protein structure and phylogenetic analyses revealed that TgUlp1 is an adaptation of the conservative Golgi tethering factor Uso1/p115. TgUlp1 and together with Golgi-localized TgGlp1 showed dominant interactions with the trafficking machinery that was predicted to operate endosome-to-Golgi recycling. Together, our study showed that T. gondii has expanded the function of the conservative Golgi tethering COG complex and evolved additional regulators of transport that are likely to serve parasite-specific secretory organelles.IMPORTANCEThe Golgi is an essential eukaryotic organelle and a major place for protein sorting and glycosylation. Among apicomplexan parasites, Toxoplasma gondii retains the most developed Golgi structure and produces many glycosylated factors necessary for parasite survival. Despite its importance, Golgi function received little attention in the past. In the current study, we identified and characterized the conserved oligomeric Golgi complex and its novel partners critical for protein transport in T. gondii tachyzoites. Our results suggest that T. gondii broadened the role of the conserved elements and reinvented the missing components of the trafficking machinery to accommodate the specific needs of the opportunistic parasite T. gondii.https://journals.asm.org/doi/10.1128/mbio.02513-23apicomplexaToxoplasma gondiiGolgivesicular transportretrograde transportanterograde transport |
| spellingShingle | Clem Marsilia Mrinalini Batra Irina D. Pokrovskaya Changqi Wang Dale Chaput Daria A. Naumova Vladimir V. Lupashin Elena S. Suvorova Essential role of the conserved oligomeric Golgi complex in Toxoplasma gondii mBio apicomplexa Toxoplasma gondii Golgi vesicular transport retrograde transport anterograde transport |
| title | Essential role of the conserved oligomeric Golgi complex in Toxoplasma gondii |
| title_full | Essential role of the conserved oligomeric Golgi complex in Toxoplasma gondii |
| title_fullStr | Essential role of the conserved oligomeric Golgi complex in Toxoplasma gondii |
| title_full_unstemmed | Essential role of the conserved oligomeric Golgi complex in Toxoplasma gondii |
| title_short | Essential role of the conserved oligomeric Golgi complex in Toxoplasma gondii |
| title_sort | essential role of the conserved oligomeric golgi complex in toxoplasma gondii |
| topic | apicomplexa Toxoplasma gondii Golgi vesicular transport retrograde transport anterograde transport |
| url | https://journals.asm.org/doi/10.1128/mbio.02513-23 |
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