Cargando…

Giardia intestinalis mitosomes undergo synchronized fission but not fusion and are constitutively associated with the endoplasmic reticulum

BACKGROUND: Mitochondria of opisthokonts undergo permanent fission and fusion throughout the cell cycle. Here, we investigated the dynamics of the mitosomes, the simplest forms of mitochondria, in the anaerobic protist parasite Giardia intestinalis, a member of the Excavata supergroup of eukaryotes....

Descripción completa

Detalles Bibliográficos
Autores principales: Voleman, Luboš, Najdrová, Vladimíra, Ástvaldsson, Ásgeir, Tůmová, Pavla, Einarsson, Elin, Švindrych, Zdeněk, Hagen, Guy M., Tachezy, Jan, Svärd, Staffan G., Doležal, Pavel
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2017
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5377515/
https://www.ncbi.nlm.nih.gov/pubmed/28372543
http://dx.doi.org/10.1186/s12915-017-0361-y
_version_ 1782519328410697728
author Voleman, Luboš
Najdrová, Vladimíra
Ástvaldsson, Ásgeir
Tůmová, Pavla
Einarsson, Elin
Švindrych, Zdeněk
Hagen, Guy M.
Tachezy, Jan
Svärd, Staffan G.
Doležal, Pavel
author_facet Voleman, Luboš
Najdrová, Vladimíra
Ástvaldsson, Ásgeir
Tůmová, Pavla
Einarsson, Elin
Švindrych, Zdeněk
Hagen, Guy M.
Tachezy, Jan
Svärd, Staffan G.
Doležal, Pavel
author_sort Voleman, Luboš
collection PubMed
description BACKGROUND: Mitochondria of opisthokonts undergo permanent fission and fusion throughout the cell cycle. Here, we investigated the dynamics of the mitosomes, the simplest forms of mitochondria, in the anaerobic protist parasite Giardia intestinalis, a member of the Excavata supergroup of eukaryotes. The mitosomes have abandoned typical mitochondrial traits such as the mitochondrial genome and aerobic respiration and their single role known to date is the formation of iron–sulfur clusters. RESULTS: In live experiments, no fusion events were observed between the mitosomes in G. intestinalis. Moreover, the organelles were highly prone to becoming heterogeneous. This suggests that fusion is either much less frequent or even absent in mitosome dynamics. Unlike in mitochondria, division of the mitosomes was absolutely synchronized and limited to mitosis. The association of the nuclear and the mitosomal division persisted during the encystation of the parasite. During the segregation of the divided mitosomes, the subset of the organelles between two G. intestinalis nuclei had a prominent role. Surprisingly, the sole dynamin-related protein of the parasite seemed not to be involved in mitosomal division. However, throughout the cell cycle, mitosomes associated with the endoplasmic reticulum (ER), although none of the known ER-tethering complexes was present. Instead, the ER–mitosome interface was occupied by the lipid metabolism enzyme long-chain acyl-CoA synthetase 4. CONCLUSIONS: This study provides the first report on the dynamics of mitosomes. We show that together with the loss of metabolic complexity of mitochondria, mitosomes of G. intestinalis have uniquely streamlined their dynamics by harmonizing their division with mitosis. We propose that this might be a strategy of G. intestinalis to maintain a stable number of organelles during cell propagation. The lack of mitosomal fusion may also be related to the secondary reduction of the organelles. However, as there are currently no reports on mitochondrial fusion in the whole Excavata supergroup, it is possible that the absence of mitochondrial fusion is an ancestral trait common to all excavates. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12915-017-0361-y) contains supplementary material, which is available to authorized users.
format Online
Article
Text
id pubmed-5377515
institution National Center for Biotechnology Information
language English
publishDate 2017
publisher BioMed Central
record_format MEDLINE/PubMed
spelling pubmed-53775152017-04-07 Giardia intestinalis mitosomes undergo synchronized fission but not fusion and are constitutively associated with the endoplasmic reticulum Voleman, Luboš Najdrová, Vladimíra Ástvaldsson, Ásgeir Tůmová, Pavla Einarsson, Elin Švindrych, Zdeněk Hagen, Guy M. Tachezy, Jan Svärd, Staffan G. Doležal, Pavel BMC Biol Research Article BACKGROUND: Mitochondria of opisthokonts undergo permanent fission and fusion throughout the cell cycle. Here, we investigated the dynamics of the mitosomes, the simplest forms of mitochondria, in the anaerobic protist parasite Giardia intestinalis, a member of the Excavata supergroup of eukaryotes. The mitosomes have abandoned typical mitochondrial traits such as the mitochondrial genome and aerobic respiration and their single role known to date is the formation of iron–sulfur clusters. RESULTS: In live experiments, no fusion events were observed between the mitosomes in G. intestinalis. Moreover, the organelles were highly prone to becoming heterogeneous. This suggests that fusion is either much less frequent or even absent in mitosome dynamics. Unlike in mitochondria, division of the mitosomes was absolutely synchronized and limited to mitosis. The association of the nuclear and the mitosomal division persisted during the encystation of the parasite. During the segregation of the divided mitosomes, the subset of the organelles between two G. intestinalis nuclei had a prominent role. Surprisingly, the sole dynamin-related protein of the parasite seemed not to be involved in mitosomal division. However, throughout the cell cycle, mitosomes associated with the endoplasmic reticulum (ER), although none of the known ER-tethering complexes was present. Instead, the ER–mitosome interface was occupied by the lipid metabolism enzyme long-chain acyl-CoA synthetase 4. CONCLUSIONS: This study provides the first report on the dynamics of mitosomes. We show that together with the loss of metabolic complexity of mitochondria, mitosomes of G. intestinalis have uniquely streamlined their dynamics by harmonizing their division with mitosis. We propose that this might be a strategy of G. intestinalis to maintain a stable number of organelles during cell propagation. The lack of mitosomal fusion may also be related to the secondary reduction of the organelles. However, as there are currently no reports on mitochondrial fusion in the whole Excavata supergroup, it is possible that the absence of mitochondrial fusion is an ancestral trait common to all excavates. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12915-017-0361-y) contains supplementary material, which is available to authorized users. BioMed Central 2017-04-03 /pmc/articles/PMC5377515/ /pubmed/28372543 http://dx.doi.org/10.1186/s12915-017-0361-y Text en © Dolezal et al. 2017 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research Article
Voleman, Luboš
Najdrová, Vladimíra
Ástvaldsson, Ásgeir
Tůmová, Pavla
Einarsson, Elin
Švindrych, Zdeněk
Hagen, Guy M.
Tachezy, Jan
Svärd, Staffan G.
Doležal, Pavel
Giardia intestinalis mitosomes undergo synchronized fission but not fusion and are constitutively associated with the endoplasmic reticulum
title Giardia intestinalis mitosomes undergo synchronized fission but not fusion and are constitutively associated with the endoplasmic reticulum
title_full Giardia intestinalis mitosomes undergo synchronized fission but not fusion and are constitutively associated with the endoplasmic reticulum
title_fullStr Giardia intestinalis mitosomes undergo synchronized fission but not fusion and are constitutively associated with the endoplasmic reticulum
title_full_unstemmed Giardia intestinalis mitosomes undergo synchronized fission but not fusion and are constitutively associated with the endoplasmic reticulum
title_short Giardia intestinalis mitosomes undergo synchronized fission but not fusion and are constitutively associated with the endoplasmic reticulum
title_sort giardia intestinalis mitosomes undergo synchronized fission but not fusion and are constitutively associated with the endoplasmic reticulum
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5377515/
https://www.ncbi.nlm.nih.gov/pubmed/28372543
http://dx.doi.org/10.1186/s12915-017-0361-y
work_keys_str_mv AT volemanlubos giardiaintestinalismitosomesundergosynchronizedfissionbutnotfusionandareconstitutivelyassociatedwiththeendoplasmicreticulum
AT najdrovavladimira giardiaintestinalismitosomesundergosynchronizedfissionbutnotfusionandareconstitutivelyassociatedwiththeendoplasmicreticulum
AT astvaldssonasgeir giardiaintestinalismitosomesundergosynchronizedfissionbutnotfusionandareconstitutivelyassociatedwiththeendoplasmicreticulum
AT tumovapavla giardiaintestinalismitosomesundergosynchronizedfissionbutnotfusionandareconstitutivelyassociatedwiththeendoplasmicreticulum
AT einarssonelin giardiaintestinalismitosomesundergosynchronizedfissionbutnotfusionandareconstitutivelyassociatedwiththeendoplasmicreticulum
AT svindrychzdenek giardiaintestinalismitosomesundergosynchronizedfissionbutnotfusionandareconstitutivelyassociatedwiththeendoplasmicreticulum
AT hagenguym giardiaintestinalismitosomesundergosynchronizedfissionbutnotfusionandareconstitutivelyassociatedwiththeendoplasmicreticulum
AT tachezyjan giardiaintestinalismitosomesundergosynchronizedfissionbutnotfusionandareconstitutivelyassociatedwiththeendoplasmicreticulum
AT svardstaffang giardiaintestinalismitosomesundergosynchronizedfissionbutnotfusionandareconstitutivelyassociatedwiththeendoplasmicreticulum
AT dolezalpavel giardiaintestinalismitosomesundergosynchronizedfissionbutnotfusionandareconstitutivelyassociatedwiththeendoplasmicreticulum