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....
Autores principales: | , , , , , , , , , |
---|---|
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 |