Highly flexible metabolism of the marine euglenozoan protist Diplonema papillatum

Abstract Background The phylum Euglenozoa is a group of flagellated protists comprising the diplonemids, euglenids, symbiontids, and kinetoplastids. The diplonemids are highly abundant and speciose, and recent tools have rendered the best studied representative, Diplonema papillatum, genetically tra...

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Autores principales:	Ingrid Škodová-Sveráková, Kristína Záhonová, Valéria Juricová, Maksym Danchenko, Martin Moos, Peter Baráth, Galina Prokopchuk, Anzhelika Butenko, Veronika Lukáčová, Lenka Kohútová, Barbora Bučková, Aleš Horák, Drahomíra Faktorová, Anton Horváth, Petr Šimek, Julius Lukeš
Formato:	article
Lenguaje:	EN
Publicado:	BMC 2021
Materias:	Diplonema Metabolism Multiomics Hypoxia Mitochondrion Euglenozoa Biology (General) QH301-705.5
Acceso en línea:	https://doaj.org/article/271336d2cbc443b595c066575c3d5367
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spelling	oai:doaj.org-article:271336d2cbc443b595c066575c3d53672021-11-28T12:41:15ZHighly flexible metabolism of the marine euglenozoan protist Diplonema papillatum10.1186/s12915-021-01186-y1741-7007https://doaj.org/article/271336d2cbc443b595c066575c3d53672021-11-01T00:00:00Zhttps://doi.org/10.1186/s12915-021-01186-yhttps://doaj.org/toc/1741-7007Abstract Background The phylum Euglenozoa is a group of flagellated protists comprising the diplonemids, euglenids, symbiontids, and kinetoplastids. The diplonemids are highly abundant and speciose, and recent tools have rendered the best studied representative, Diplonema papillatum, genetically tractable. However, despite the high diversity of diplonemids, their lifestyles, ecological functions, and even primary energy source are mostly unknown. Results We designed a metabolic map of D. papillatum cellular bioenergetic pathways based on the alterations of transcriptomic, proteomic, and metabolomic profiles obtained from cells grown under different conditions. Comparative analysis in the nutrient-rich and nutrient-poor media, as well as the absence and presence of oxygen, revealed its capacity for extensive metabolic reprogramming that occurs predominantly on the proteomic rather than the transcriptomic level. D. papillatum is equipped with fundamental metabolic routes such as glycolysis, gluconeogenesis, TCA cycle, pentose phosphate pathway, respiratory complexes, β-oxidation, and synthesis of fatty acids. Gluconeogenesis is uniquely dominant over glycolysis under all surveyed conditions, while the TCA cycle represents an eclectic combination of standard and unusual enzymes. Conclusions The identification of conventional anaerobic enzymes reflects the ability of this protist to survive in low-oxygen environments. Furthermore, its metabolism quickly reacts to restricted carbon availability, suggesting a high metabolic flexibility of diplonemids, which is further reflected in cell morphology and motility, correlating well with their extreme ecological valence.Ingrid Škodová-SverákováKristína ZáhonováValéria JuricováMaksym DanchenkoMartin MoosPeter BaráthGalina ProkopchukAnzhelika ButenkoVeronika LukáčováLenka KohútováBarbora BučkováAleš HorákDrahomíra FaktorováAnton HorváthPetr ŠimekJulius LukešBMCarticleDiplonemaMetabolismMultiomicsHypoxiaMitochondrionEuglenozoaBiology (General)QH301-705.5ENBMC Biology, Vol 19, Iss 1, Pp 1-21 (2021)
institution	DOAJ
collection	DOAJ
language	EN
topic	Diplonema Metabolism Multiomics Hypoxia Mitochondrion Euglenozoa Biology (General) QH301-705.5
spellingShingle	Diplonema Metabolism Multiomics Hypoxia Mitochondrion Euglenozoa Biology (General) QH301-705.5 Ingrid Škodová-Sveráková Kristína Záhonová Valéria Juricová Maksym Danchenko Martin Moos Peter Baráth Galina Prokopchuk Anzhelika Butenko Veronika Lukáčová Lenka Kohútová Barbora Bučková Aleš Horák Drahomíra Faktorová Anton Horváth Petr Šimek Julius Lukeš Highly flexible metabolism of the marine euglenozoan protist Diplonema papillatum
description	Abstract Background The phylum Euglenozoa is a group of flagellated protists comprising the diplonemids, euglenids, symbiontids, and kinetoplastids. The diplonemids are highly abundant and speciose, and recent tools have rendered the best studied representative, Diplonema papillatum, genetically tractable. However, despite the high diversity of diplonemids, their lifestyles, ecological functions, and even primary energy source are mostly unknown. Results We designed a metabolic map of D. papillatum cellular bioenergetic pathways based on the alterations of transcriptomic, proteomic, and metabolomic profiles obtained from cells grown under different conditions. Comparative analysis in the nutrient-rich and nutrient-poor media, as well as the absence and presence of oxygen, revealed its capacity for extensive metabolic reprogramming that occurs predominantly on the proteomic rather than the transcriptomic level. D. papillatum is equipped with fundamental metabolic routes such as glycolysis, gluconeogenesis, TCA cycle, pentose phosphate pathway, respiratory complexes, β-oxidation, and synthesis of fatty acids. Gluconeogenesis is uniquely dominant over glycolysis under all surveyed conditions, while the TCA cycle represents an eclectic combination of standard and unusual enzymes. Conclusions The identification of conventional anaerobic enzymes reflects the ability of this protist to survive in low-oxygen environments. Furthermore, its metabolism quickly reacts to restricted carbon availability, suggesting a high metabolic flexibility of diplonemids, which is further reflected in cell morphology and motility, correlating well with their extreme ecological valence.
format	article
author	Ingrid Škodová-Sveráková Kristína Záhonová Valéria Juricová Maksym Danchenko Martin Moos Peter Baráth Galina Prokopchuk Anzhelika Butenko Veronika Lukáčová Lenka Kohútová Barbora Bučková Aleš Horák Drahomíra Faktorová Anton Horváth Petr Šimek Julius Lukeš
author_facet	Ingrid Škodová-Sveráková Kristína Záhonová Valéria Juricová Maksym Danchenko Martin Moos Peter Baráth Galina Prokopchuk Anzhelika Butenko Veronika Lukáčová Lenka Kohútová Barbora Bučková Aleš Horák Drahomíra Faktorová Anton Horváth Petr Šimek Julius Lukeš
author_sort	Ingrid Škodová-Sveráková
title	Highly flexible metabolism of the marine euglenozoan protist Diplonema papillatum
title_short	Highly flexible metabolism of the marine euglenozoan protist Diplonema papillatum
title_full	Highly flexible metabolism of the marine euglenozoan protist Diplonema papillatum
title_fullStr	Highly flexible metabolism of the marine euglenozoan protist Diplonema papillatum
title_full_unstemmed	Highly flexible metabolism of the marine euglenozoan protist Diplonema papillatum
title_sort	highly flexible metabolism of the marine euglenozoan protist diplonema papillatum
publisher	BMC
publishDate	2021
url	https://doaj.org/article/271336d2cbc443b595c066575c3d5367
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Highly flexible metabolism of the marine euglenozoan protist Diplonema papillatum

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