The Toxoplasma monocarboxylate transporters are involved in the metabolism within the apicoplast and are linked to parasite survival
The apicoplast is a four-membrane plastid found in the apicomplexans, which harbors biosynthesis and organelle housekeeping activities in the matrix. However, the mechanism driving the flux of metabolites, in and out, remains unknown. Here, we used TurboID and genome engineering to identify apicopla...
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| Format: | Article |
| Language: | English |
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eLife Sciences Publications Ltd
2024-03-01
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| Series: | eLife |
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| Online Access: | https://elifesciences.org/articles/88866 |
| _version_ | 1797257133560954880 |
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| author | Hui Dong Jiong Yang Kai He Wen-Bin Zheng De-Hua Lai Jing Liu Hui-Yong Ding Rui-Bin Wu Kevin M Brown Geoff Hide Zhao-Rong Lun Xing-Quan Zhu Shaojun Long |
| author_facet | Hui Dong Jiong Yang Kai He Wen-Bin Zheng De-Hua Lai Jing Liu Hui-Yong Ding Rui-Bin Wu Kevin M Brown Geoff Hide Zhao-Rong Lun Xing-Quan Zhu Shaojun Long |
| author_sort | Hui Dong |
| collection | DOAJ |
| description | The apicoplast is a four-membrane plastid found in the apicomplexans, which harbors biosynthesis and organelle housekeeping activities in the matrix. However, the mechanism driving the flux of metabolites, in and out, remains unknown. Here, we used TurboID and genome engineering to identify apicoplast transporters in Toxoplasma gondii. Among the many novel transporters, we show that one pair of apicomplexan monocarboxylate transporters (AMTs) appears to have evolved from a putative host cell that engulfed a red alga. Protein depletion showed that AMT1 and AMT2 are critical for parasite growth. Metabolite analyses supported the notion that AMT1 and AMT2 are associated with biosynthesis of isoprenoids and fatty acids. However, stronger phenotypic defects were observed for AMT2, including in the inability to establish T. gondii parasite virulence in mice. This study clarifies, significantly, the mystery of apicoplast transporter composition and reveals the importance of the pair of AMTs in maintaining the apicoplast activity in apicomplexans. |
| first_indexed | 2024-04-24T22:32:48Z |
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| id | doaj.art-8397a5d62a4d4a6b99f4c420622439eb |
| institution | Directory Open Access Journal |
| issn | 2050-084X |
| language | English |
| last_indexed | 2024-04-24T22:32:48Z |
| publishDate | 2024-03-01 |
| publisher | eLife Sciences Publications Ltd |
| record_format | Article |
| series | eLife |
| spelling | doaj.art-8397a5d62a4d4a6b99f4c420622439eb2024-03-19T16:25:37ZengeLife Sciences Publications LtdeLife2050-084X2024-03-011210.7554/eLife.88866The Toxoplasma monocarboxylate transporters are involved in the metabolism within the apicoplast and are linked to parasite survivalHui Dong0https://orcid.org/0000-0002-3250-871XJiong Yang1Kai He2https://orcid.org/0000-0002-2252-4855Wen-Bin Zheng3De-Hua Lai4https://orcid.org/0000-0002-4709-1507Jing Liu5Hui-Yong Ding6Rui-Bin Wu7Kevin M Brown8Geoff Hide9https://orcid.org/0000-0002-3608-0175Zhao-Rong Lun10Xing-Quan Zhu11https://orcid.org/0000-0003-2530-4628Shaojun Long12https://orcid.org/0000-0002-5409-2831National Key Laboratory of Veterinary Public Health Safety, and College of Veterinary Medicine, China Agricultural University, Beijing, China; National Animal Protozoa Laboratory and School of Veterinary Medicine, China Agricultural University, Beijing, ChinaMOE Key Laboratory of Gene Function and Regulation, State Key Laboratory of Biocontrol and Guangdong Provincial Key Laboratory of Aquatic Economic Animals, School of Life Sciences, Sun Yat-Sen University, Guangzhou, ChinaNational Key Laboratory of Veterinary Public Health Safety, and College of Veterinary Medicine, China Agricultural University, Beijing, China; National Animal Protozoa Laboratory and School of Veterinary Medicine, China Agricultural University, Beijing, ChinaCollege of Veterinary Medicine, Shanxi Agricultural University, Taigu, ChinaMOE Key Laboratory of Gene Function and Regulation, State Key Laboratory of Biocontrol and Guangdong Provincial Key Laboratory of Aquatic Economic Animals, School of Life Sciences, Sun Yat-Sen University, Guangzhou, ChinaNational Key Laboratory of Veterinary Public Health Safety, and College of Veterinary Medicine, China Agricultural University, Beijing, China; National Animal Protozoa Laboratory and School of Veterinary Medicine, China Agricultural University, Beijing, ChinaNational Key Laboratory of Veterinary Public Health Safety, and College of Veterinary Medicine, China Agricultural University, Beijing, China; National Animal Protozoa Laboratory and School of Veterinary Medicine, China Agricultural University, Beijing, ChinaNational Key Laboratory of Veterinary Public Health Safety, and College of Veterinary Medicine, China Agricultural University, Beijing, China; National Animal Protozoa Laboratory and School of Veterinary Medicine, China Agricultural University, Beijing, ChinaDepartment of Microbiology and Immunology, University of Oklahoma Health Sciences Center, Oklahoma City, United StatesBiomedical Research and Innovation Centre and Environmental Research and Innovation Centre, School of Science, Engineering and Environment, University of Salford, Salford, United KingdomMOE Key Laboratory of Gene Function and Regulation, State Key Laboratory of Biocontrol and Guangdong Provincial Key Laboratory of Aquatic Economic Animals, School of Life Sciences, Sun Yat-Sen University, Guangzhou, ChinaCollege of Veterinary Medicine, Shanxi Agricultural University, Taigu, ChinaNational Key Laboratory of Veterinary Public Health Safety, and College of Veterinary Medicine, China Agricultural University, Beijing, China; National Animal Protozoa Laboratory and School of Veterinary Medicine, China Agricultural University, Beijing, ChinaThe apicoplast is a four-membrane plastid found in the apicomplexans, which harbors biosynthesis and organelle housekeeping activities in the matrix. However, the mechanism driving the flux of metabolites, in and out, remains unknown. Here, we used TurboID and genome engineering to identify apicoplast transporters in Toxoplasma gondii. Among the many novel transporters, we show that one pair of apicomplexan monocarboxylate transporters (AMTs) appears to have evolved from a putative host cell that engulfed a red alga. Protein depletion showed that AMT1 and AMT2 are critical for parasite growth. Metabolite analyses supported the notion that AMT1 and AMT2 are associated with biosynthesis of isoprenoids and fatty acids. However, stronger phenotypic defects were observed for AMT2, including in the inability to establish T. gondii parasite virulence in mice. This study clarifies, significantly, the mystery of apicoplast transporter composition and reveals the importance of the pair of AMTs in maintaining the apicoplast activity in apicomplexans.https://elifesciences.org/articles/88866apicomplexansToxoplasma gondiiapicoplasttransportersmonocarboxylate transportersparasite physiology |
| spellingShingle | Hui Dong Jiong Yang Kai He Wen-Bin Zheng De-Hua Lai Jing Liu Hui-Yong Ding Rui-Bin Wu Kevin M Brown Geoff Hide Zhao-Rong Lun Xing-Quan Zhu Shaojun Long The Toxoplasma monocarboxylate transporters are involved in the metabolism within the apicoplast and are linked to parasite survival eLife apicomplexans Toxoplasma gondii apicoplast transporters monocarboxylate transporters parasite physiology |
| title | The Toxoplasma monocarboxylate transporters are involved in the metabolism within the apicoplast and are linked to parasite survival |
| title_full | The Toxoplasma monocarboxylate transporters are involved in the metabolism within the apicoplast and are linked to parasite survival |
| title_fullStr | The Toxoplasma monocarboxylate transporters are involved in the metabolism within the apicoplast and are linked to parasite survival |
| title_full_unstemmed | The Toxoplasma monocarboxylate transporters are involved in the metabolism within the apicoplast and are linked to parasite survival |
| title_short | The Toxoplasma monocarboxylate transporters are involved in the metabolism within the apicoplast and are linked to parasite survival |
| title_sort | toxoplasma monocarboxylate transporters are involved in the metabolism within the apicoplast and are linked to parasite survival |
| topic | apicomplexans Toxoplasma gondii apicoplast transporters monocarboxylate transporters parasite physiology |
| url | https://elifesciences.org/articles/88866 |
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