Divergent mitochondrial respiratory chains in phototrophic relatives of apicomplexan parasites

Pavel Flegontov; Jan Michálek; Jan Janouškovec; De Hua Lai; Milan Jirků; Eva Hajdušková; Aleš Tomčala; Thomas D. Otto; Patrick J. Keeling; Arnab Pain; Miroslav Oborník; J. Lukeš

doi:10.1093/molbev/msv021

Divergent mitochondrial respiratory chains in phototrophic relatives of apicomplexan parasites

Pavel Flegontov, Jan Michálek, Jan Janouškovec, De Hua Lai, Milan Jirků, Eva Hajdušková, Aleš Tomčala, Thomas D. Otto, Patrick J. Keeling, Arnab Pain, Miroslav Oborník, J. Lukeš

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67 Scopus citations

Abstract

Four respiratory complexes and ATP-synthase represent central functional units in mitochondria. In some mitochondria and derived anaerobic organelles, a few or all of these respiratory complexes have been lost during evolution. We show that the respiratory chain of Chromera velia, a phototrophic relative of parasitic apicomplexans, lacks complexes I and III, making it a uniquely reduced aerobic mitochondrion. In Chromera, putative lactate:cytochrome c oxidoreductases are predicted to transfer electrons from lactate to cytochrome c, rendering complex III unnecessary. The mitochondrial genome of Chromera has the smallest known protein-coding capacity of all mitochondria, encoding just cox1 and cox3 on heterogeneous linear molecules. In contrast, another photosynthetic relative of apicomplexans, Vitrella brassicaformis, retains the same set of genes as apicomplexans and dinoflagellates (cox1, cox3, and cob). © The Author 2015. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution.

Original language	English (US)
Pages (from-to)	1115-1131
Number of pages	17
Journal	Molecular Biology and Evolution
Volume	32
Issue number	5
DOIs	https://doi.org/10.1093/molbev/msv021
State	Published - Feb 6 2015

Bibliographical note

KAUST Repository Item: Exported on 2020-10-01
Acknowledged KAUST grant number(s): FIC/2010/09
Acknowledgements: The authors thank the KAUST Bioscience Core Laboratory personnel for sequencing Illumina libraries used in this project, Evgeny S. Gerasimov (Institute for Information Transmission Problems, Russian Academy of Sciences, Moscow) and Martin Kolisko (University of British Columbia, Vancouver) for help with sequence analysis, Oldrich Benada (Institute of Microbiology, Prague) for help with electron microscopy, Anton Horvath (Comenius University, Bratislava), Dave Speijer (University of Amsterdam, Amsterdam), and Ivan Hrdy (Charles University, Prague) for useful comments. This work was supported by Czech Science Foundation grants P506/12/1522, 13-33039S (support for J.M.) and P501/12/G055 (support for A.T.) to M.O., project Algatech (CZ.1.05/2.1.00/03.0110) to M.O., FP7 agreement 316304 to M.O. and J.L., the KAUST award FIC/2010/09 to A.P., M.O. and J.L., and by a grant from the Canadian Institutes for Health Research to P.J.K. and J.L. is also supported by the Praemium Academiae, and P.F. by a grant of the Moravian-Silesian region (project MSK2013-DT1) and by Russian Foundation for Basic Research (project 14-04-31936). P.J.K. and J.L. are Senior Fellows and J.J. is a Global Scholar at the Canadian Institute for Advanced Research, and P.J.K. was supported by a Fellowship from the John Simon Guggenheim Foundation.

ASJC Scopus subject areas

Ecology, Evolution, Behavior and Systematics
Genetics
Molecular Biology

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10.1093/molbev/msv021

Cite this

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title = "Divergent mitochondrial respiratory chains in phototrophic relatives of apicomplexan parasites",

abstract = "Four respiratory complexes and ATP-synthase represent central functional units in mitochondria. In some mitochondria and derived anaerobic organelles, a few or all of these respiratory complexes have been lost during evolution. We show that the respiratory chain of Chromera velia, a phototrophic relative of parasitic apicomplexans, lacks complexes I and III, making it a uniquely reduced aerobic mitochondrion. In Chromera, putative lactate:cytochrome c oxidoreductases are predicted to transfer electrons from lactate to cytochrome c, rendering complex III unnecessary. The mitochondrial genome of Chromera has the smallest known protein-coding capacity of all mitochondria, encoding just cox1 and cox3 on heterogeneous linear molecules. In contrast, another photosynthetic relative of apicomplexans, Vitrella brassicaformis, retains the same set of genes as apicomplexans and dinoflagellates (cox1, cox3, and cob). {\textcopyright} The Author 2015. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution.",

author = "Pavel Flegontov and Jan Mich{\'a}lek and Jan Janou{\v s}kovec and Lai, {De Hua} and Milan Jirků and Eva Hajdu{\v s}kov{\'a} and Ale{\v s} Tom{\v c}ala and Otto, {Thomas D.} and Keeling, {Patrick J.} and Arnab Pain and Miroslav Oborn{\'i}k and J. Luke{\v s}",

note = "KAUST Repository Item: Exported on 2020-10-01 Acknowledged KAUST grant number(s): FIC/2010/09 Acknowledgements: The authors thank the KAUST Bioscience Core Laboratory personnel for sequencing Illumina libraries used in this project, Evgeny S. Gerasimov (Institute for Information Transmission Problems, Russian Academy of Sciences, Moscow) and Martin Kolisko (University of British Columbia, Vancouver) for help with sequence analysis, Oldrich Benada (Institute of Microbiology, Prague) for help with electron microscopy, Anton Horvath (Comenius University, Bratislava), Dave Speijer (University of Amsterdam, Amsterdam), and Ivan Hrdy (Charles University, Prague) for useful comments. This work was supported by Czech Science Foundation grants P506/12/1522, 13-33039S (support for J.M.) and P501/12/G055 (support for A.T.) to M.O., project Algatech (CZ.1.05/2.1.00/03.0110) to M.O., FP7 agreement 316304 to M.O. and J.L., the KAUST award FIC/2010/09 to A.P., M.O. and J.L., and by a grant from the Canadian Institutes for Health Research to P.J.K. and J.L. is also supported by the Praemium Academiae, and P.F. by a grant of the Moravian-Silesian region (project MSK2013-DT1) and by Russian Foundation for Basic Research (project 14-04-31936). P.J.K. and J.L. are Senior Fellows and J.J. is a Global Scholar at the Canadian Institute for Advanced Research, and P.J.K. was supported by a Fellowship from the John Simon Guggenheim Foundation.",

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language = "English (US)",

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T1 - Divergent mitochondrial respiratory chains in phototrophic relatives of apicomplexan parasites

AU - Flegontov, Pavel

AU - Michálek, Jan

AU - Janouškovec, Jan

AU - Lai, De Hua

AU - Jirků, Milan

AU - Hajdušková, Eva

AU - Tomčala, Aleš

AU - Otto, Thomas D.

AU - Keeling, Patrick J.

AU - Pain, Arnab

AU - Oborník, Miroslav

AU - Lukeš, J.

N1 - KAUST Repository Item: Exported on 2020-10-01 Acknowledged KAUST grant number(s): FIC/2010/09 Acknowledgements: The authors thank the KAUST Bioscience Core Laboratory personnel for sequencing Illumina libraries used in this project, Evgeny S. Gerasimov (Institute for Information Transmission Problems, Russian Academy of Sciences, Moscow) and Martin Kolisko (University of British Columbia, Vancouver) for help with sequence analysis, Oldrich Benada (Institute of Microbiology, Prague) for help with electron microscopy, Anton Horvath (Comenius University, Bratislava), Dave Speijer (University of Amsterdam, Amsterdam), and Ivan Hrdy (Charles University, Prague) for useful comments. This work was supported by Czech Science Foundation grants P506/12/1522, 13-33039S (support for J.M.) and P501/12/G055 (support for A.T.) to M.O., project Algatech (CZ.1.05/2.1.00/03.0110) to M.O., FP7 agreement 316304 to M.O. and J.L., the KAUST award FIC/2010/09 to A.P., M.O. and J.L., and by a grant from the Canadian Institutes for Health Research to P.J.K. and J.L. is also supported by the Praemium Academiae, and P.F. by a grant of the Moravian-Silesian region (project MSK2013-DT1) and by Russian Foundation for Basic Research (project 14-04-31936). P.J.K. and J.L. are Senior Fellows and J.J. is a Global Scholar at the Canadian Institute for Advanced Research, and P.J.K. was supported by a Fellowship from the John Simon Guggenheim Foundation.

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Y1 - 2015/2/6

N2 - Four respiratory complexes and ATP-synthase represent central functional units in mitochondria. In some mitochondria and derived anaerobic organelles, a few or all of these respiratory complexes have been lost during evolution. We show that the respiratory chain of Chromera velia, a phototrophic relative of parasitic apicomplexans, lacks complexes I and III, making it a uniquely reduced aerobic mitochondrion. In Chromera, putative lactate:cytochrome c oxidoreductases are predicted to transfer electrons from lactate to cytochrome c, rendering complex III unnecessary. The mitochondrial genome of Chromera has the smallest known protein-coding capacity of all mitochondria, encoding just cox1 and cox3 on heterogeneous linear molecules. In contrast, another photosynthetic relative of apicomplexans, Vitrella brassicaformis, retains the same set of genes as apicomplexans and dinoflagellates (cox1, cox3, and cob). © The Author 2015. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution.

AB - Four respiratory complexes and ATP-synthase represent central functional units in mitochondria. In some mitochondria and derived anaerobic organelles, a few or all of these respiratory complexes have been lost during evolution. We show that the respiratory chain of Chromera velia, a phototrophic relative of parasitic apicomplexans, lacks complexes I and III, making it a uniquely reduced aerobic mitochondrion. In Chromera, putative lactate:cytochrome c oxidoreductases are predicted to transfer electrons from lactate to cytochrome c, rendering complex III unnecessary. The mitochondrial genome of Chromera has the smallest known protein-coding capacity of all mitochondria, encoding just cox1 and cox3 on heterogeneous linear molecules. In contrast, another photosynthetic relative of apicomplexans, Vitrella brassicaformis, retains the same set of genes as apicomplexans and dinoflagellates (cox1, cox3, and cob). © The Author 2015. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution.

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DO - 10.1093/molbev/msv021

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JO - Molecular Biology and Evolution

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Divergent mitochondrial respiratory chains in phototrophic relatives of apicomplexan parasites

Abstract

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