The evolution of ERMIONE in mitochondrial biogenesis and lipid homeostasis: An evolutionary view from comparative cell biology

Wideman, Jeremy G.; Muñoz-Gómez, Sergio A.

doi:10.1016/j.bbalip.2016.01.015

Cited by 46 publications

(41 citation statements)

References 144 publications

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“…The lack of observable mitochondrial fusion and the responsible molecular machinery in Excavata indicates that the lack of fusion is an ancestral trait. The components of both recently described ER-tethering complexes can be found in all five supergroups of eukaryotes and thus they were likely present in the LECA [76]. Despite the secondary loss of these complexes, G. intestinalis mitosomes maintain association with the ER throughout the cell cycle, indicating the presence of yet unknown tethering mechanisms, perhaps including lipid metabolism enzymes such as LACS4.…”

Section: Resultsmentioning

confidence: 99%

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

et al. 2017

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BackgroundMitochondria 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.ResultsIn 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.ConclusionsThis 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 materialThe online version of this article (doi:10.1186/s12915-017-0361-y) contains supplementary material, which is available to authorized users.

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Section: Resultsmentioning

confidence: 99%

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

et al. 2017

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“…This network also involves endoplasmic reticulum (ER)-mitochondria contact sites. The ER-mitochondria encounter structure (ERMES) connects ER and the mitochondrial outer membrane and plays a role in maintaining the shape of mitochondria and promoting phospholipid transfer between both organelles (Burgess et al, 1994;Sogo and Yaffe, 1994;Berger et al, 1997;Kornmann et al, 2009;Kopec et al, 2010;Voss et al, 2012;Elbaz-Alon et al, 2014;Schauder et al, 2014;Wideman and Muñoz-Gómez, 2016). Figure 4 depicts a remarkable connection between the SAM complex and ERMES.…”

Section: Protein Translocases and Mitochondrial Architecturementioning

confidence: 99%

“…The network is not limited to mitochondria but includes contact sites with the ER, leading to a three membrane-spanning network termed ERMIONE (van der Laan et al, 2012;Wideman and Muñoz-Gómez, 2016). We propose that ERMIONE serves as an organizing center for coordinating a broad variety of tasks from protein and lipid biogenesis to mitochondrial architecture and membrane remodeling.…”

Section: Conclusion and Open Questionsmentioning

confidence: 99%

“…Recent studies led to the identification of a large protein complex that is enriched at crista junctions and termed the mitochondrial contact site and cristae organizing system (MICOS) (Harner et al, 2011(Harner et al, , 2014Hoppins et al, 2011;von der Malsburg et al, 2011;Alkhaja et al, 2012;Pfanner et al, 2014;Friedman et al, 2015;Wideman and Muñoz-Gómez, 2016). The MICOS complex is crucial for maintaining the architecture of the inner membrane.…”

Section: Protein Translocases and Mitochondrial Architecturementioning

confidence: 99%

“…These findings reveal that in vivo protein translocases and morphology machineries do not function as independent entities, but they are embedded into a large regulatory network that controls mitochondrial architecture and biogenesis. We termed this dynamic network spanning across three membranes the ER-mitochondria organizing network (ERMIONE) (van der Laan et al, 2012;Wideman and Muñoz-Gómez, 2016).…”

Section: Protein Translocases and Mitochondrial Architecturementioning

confidence: 99%

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Dynamic organization of the mitochondrial protein import machinery

Straub

Stiller

Wiedemann

et al. 2016

Biological Chemistry

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Mitochondria contain elaborate machineries for the import of precursor proteins from the cytosol. The translocase of the outer mitochondrial membrane (TOM) performs the initial import of precursor proteins and transfers the precursors to downstream translocases, including the presequence translocase and the carrier translocase of the inner membrane, the mitochondrial import and assembly machinery of the intermembrane space, and the sorting and assembly machinery of the outer membrane. Although the protein translocases can function as separate entities in vitro, recent studies revealed a close and dynamic cooperation of the protein import machineries to facilitate efficient transfer of precursor proteins in vivo. In addition, protein translocases were found to transiently interact with distinct machineries that function in the respiratory chain or in the maintenance of mitochondrial membrane architecture. Mitochondrial protein import is embedded in a regulatory network that ensures protein biogenesis, membrane dynamics, bioenergetic activity and quality control.

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