Selective loss of ATP carriers in favour of SLC25A43 orthologues in metamonad mitochondria adapted to anaerobiosis
Metamonada is a eukaryotic supergroup of free-living and parasitic anaerobic protists. Their characteristic feature is the presence of highly reduced mitochondria that have lost the ability to produce ATP by oxidative phosphorylation and in some cases even by substrate phosphorylation, with all ATP...
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The Royal Society
2025-08-01
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| Series: | Open Biology |
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| Online Access: | https://royalsocietypublishing.org/doi/10.1098/rsob.240202 |
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| author | Natalia Janowicz Vít Dohnálek Justyna Zítek Priscila Peña-Diaz Eva Pyrihová Martin S. King Michaela Husová Vojtěch Žárský Edmund Kunji Alena Zikova Vladimír Hampl Pavel Dolezal |
| author_facet | Natalia Janowicz Vít Dohnálek Justyna Zítek Priscila Peña-Diaz Eva Pyrihová Martin S. King Michaela Husová Vojtěch Žárský Edmund Kunji Alena Zikova Vladimír Hampl Pavel Dolezal |
| author_sort | Natalia Janowicz |
| collection | DOAJ |
| description | Metamonada is a eukaryotic supergroup of free-living and parasitic anaerobic protists. Their characteristic feature is the presence of highly reduced mitochondria that have lost the ability to produce ATP by oxidative phosphorylation and in some cases even by substrate phosphorylation, with all ATP being imported from the cytosol. Given this striking difference in cellular ATP metabolism when compared to aerobic mitochondria, we studied the presence of mitochondrial carrier proteins (MCPs) mediating the transport of ATP across the inner mitochondrial membrane. Our bioinformatic analyses revealed remarkable reduction of MCP repertoire in Metamonada with striking loss of the major ADP/ATP carrier (AAC). Instead, nearly all species retained carriers orthologous to human SLC25A43 protein, a little-characterized MCP. Heterologous expression of metamonad SLC25A43 carriers confirmed their mitochondrial localization, and functional analysis revealed that SLC25A43 orthologues represent a distinct group of ATP transporters, which we designate as ATP-importing carriers (AIC). Together, our findings suggest that AIC facilitate the ATP import into highly reduced anaerobic mitochondria, compensating for their diminished or absent energy metabolism. |
| format | Article |
| id | doaj-art-77f80c8c2b444f11bd744449d5a827de |
| institution | DOAJ |
| issn | 2046-2441 |
| language | English |
| publishDate | 2025-08-01 |
| publisher | The Royal Society |
| record_format | Article |
| series | Open Biology |
| spelling | doaj-art-77f80c8c2b444f11bd744449d5a827de2025-08-20T03:02:59ZengThe Royal SocietyOpen Biology2046-24412025-08-0115810.1098/rsob.240202Selective loss of ATP carriers in favour of SLC25A43 orthologues in metamonad mitochondria adapted to anaerobiosisNatalia Janowicz0Vít Dohnálek1Justyna Zítek2Priscila Peña-Diaz3Eva Pyrihová4Martin S. King5Michaela Husová6Vojtěch Žárský7Edmund Kunji8Alena Zikova9Vladimír Hampl10Pavel Dolezal11Department of Parasitology, BIOCEV, Charles University Faculty of Science, Prague, Czech RepublicDepartment of Parasitology, BIOCEV, Charles University Faculty of Science, Prague, Czech RepublicDepartment of Parasitology, BIOCEV, Charles University Faculty of Science, Prague, Czech RepublicDepartment of Parasitology, BIOCEV, Charles University Faculty of Science, Prague, Czech RepublicDepartment of Chemistry, Bioscience Environmental Engineering, University of Stavanger, Stavanger, NorwayMRC Mitochondrial Biology Unit, Cambridge Biomedical Campus, University of Cambridge, Cambridge, UKInstitute of Parasitology, Biology Centre of the Czech Academy of Sciences, České Budějovice, Czech RepublicDepartment of Parasitology, BIOCEV, Charles University Faculty of Science, Prague, Czech RepublicMRC Mitochondrial Biology Unit, Cambridge Biomedical Campus, University of Cambridge, Cambridge, UKBiology Centre, Academy of Sciences of the Czech Republic, České Budějovice, Czech RepublicDepartment of Parasitology, BIOCEV, Charles University Faculty of Science, Prague, Czech RepublicDepartment of Parasitology, BIOCEV, Charles University Faculty of Science, Prague, Czech RepublicMetamonada is a eukaryotic supergroup of free-living and parasitic anaerobic protists. Their characteristic feature is the presence of highly reduced mitochondria that have lost the ability to produce ATP by oxidative phosphorylation and in some cases even by substrate phosphorylation, with all ATP being imported from the cytosol. Given this striking difference in cellular ATP metabolism when compared to aerobic mitochondria, we studied the presence of mitochondrial carrier proteins (MCPs) mediating the transport of ATP across the inner mitochondrial membrane. Our bioinformatic analyses revealed remarkable reduction of MCP repertoire in Metamonada with striking loss of the major ADP/ATP carrier (AAC). Instead, nearly all species retained carriers orthologous to human SLC25A43 protein, a little-characterized MCP. Heterologous expression of metamonad SLC25A43 carriers confirmed their mitochondrial localization, and functional analysis revealed that SLC25A43 orthologues represent a distinct group of ATP transporters, which we designate as ATP-importing carriers (AIC). Together, our findings suggest that AIC facilitate the ATP import into highly reduced anaerobic mitochondria, compensating for their diminished or absent energy metabolism.https://royalsocietypublishing.org/doi/10.1098/rsob.240202Metamonadamitochondrial carrier proteinADP/ATP carrierSLC25A43mitochondrion-related organellemitochondrial evolution |
| spellingShingle | Natalia Janowicz Vít Dohnálek Justyna Zítek Priscila Peña-Diaz Eva Pyrihová Martin S. King Michaela Husová Vojtěch Žárský Edmund Kunji Alena Zikova Vladimír Hampl Pavel Dolezal Selective loss of ATP carriers in favour of SLC25A43 orthologues in metamonad mitochondria adapted to anaerobiosis Open Biology Metamonada mitochondrial carrier protein ADP/ATP carrier SLC25A43 mitochondrion-related organelle mitochondrial evolution |
| title | Selective loss of ATP carriers in favour of SLC25A43 orthologues in metamonad mitochondria adapted to anaerobiosis |
| title_full | Selective loss of ATP carriers in favour of SLC25A43 orthologues in metamonad mitochondria adapted to anaerobiosis |
| title_fullStr | Selective loss of ATP carriers in favour of SLC25A43 orthologues in metamonad mitochondria adapted to anaerobiosis |
| title_full_unstemmed | Selective loss of ATP carriers in favour of SLC25A43 orthologues in metamonad mitochondria adapted to anaerobiosis |
| title_short | Selective loss of ATP carriers in favour of SLC25A43 orthologues in metamonad mitochondria adapted to anaerobiosis |
| title_sort | selective loss of atp carriers in favour of slc25a43 orthologues in metamonad mitochondria adapted to anaerobiosis |
| topic | Metamonada mitochondrial carrier protein ADP/ATP carrier SLC25A43 mitochondrion-related organelle mitochondrial evolution |
| url | https://royalsocietypublishing.org/doi/10.1098/rsob.240202 |
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