Ancient Homology of the Mitochondrial Contact Site and Cristae Organizing System Points to an Endosymbiotic Origin of Mitochondrial Cristae

Published on Jun 1, 2015in Current Biology 9.25
· DOI :10.1016/j.cub.2015.04.006
Sergio A. Muñoz-Gómez6
Estimated H-index: 6
(Dalhousie University),
Claudio H. Slamovits26
Estimated H-index: 26
(Canadian Institute for Advanced Research)
+ 3 AuthorsJeremy G. Wideman12
Estimated H-index: 12
(University of Alberta)
Abstract
Summary Mitochondria are eukaryotic organelles that originated from an endosymbiotic α-proteobacterium. As an adaptation to maximize ATP production through oxidative phosphorylation, mitochondria contain inner membrane invaginations called cristae. Recent work has characterized a multi-protein complex in yeast and animal mitochondria called MICOS (mitochondrial contact site and cristae organizing system), responsible for the determination and maintenance of cristae [1–4]. However, the origin and evolution of these characteristic mitochondrial features remain obscure. We therefore conducted a comprehensive search for MICOS components across the major groups that encompass eukaryotic diversity to determine the extent of conservation of this complex. We detected homologs for the majority of MICOS components among opisthokonts (the group containing animals and fungi), but only Mic60 and Mic10 were consistently identified outside this group. The conservation of Mic60 and Mic10 in eukaryotes is consistent with their central role in MICOS function [5–7], indicating that the basic mechanism for cristae determination arose early in evolution and has remained relatively unchanged. We found that eukaryotes with ultrastructurally simplified anaerobic mitochondria that lack cristae have also lost MICOS. We then searched for a prokaryotic MICOS and identified a homolog of Mic60 present only in α-proteobacteria, providing evidence for the endosymbiotic origin of mitochondrial cristae. Our study clarifies the origins of mitochondrial cristae and their subsequent evolutionary history, provides evidence for a general mechanism of cristae formation and maintenance in eukaryotes, and points to a new potential factor involved in membrane differentiation in prokaryotes.
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References52
Published on May 1, 1988in Journal of Clinical Microbiology 4.05
Charles H. Zierdt20
Estimated H-index: 20
,
C T Donnolley1
Estimated H-index: 1
+ 1 AuthorsG Constantopoulos1
Estimated H-index: 1
This study was prompted by the paradox of strong presence of mitochondria in an anaerobic protozoan, recently reclassified from the yeasts. Stemming from publication in 1911 to 1912, Blastocystis hominis has been generally accepted as a harmless intestinal yeast of humans, with short standardized textbook (parasitology) descriptions, even to the present day. Reports since 1967 have changed the classification of B. hominis from yeast to protozoan (Sarcodina), and this has been followed by interes...
49 Citations
Published on Nov 2, 2011in The EMBO Journal 10.56
Max Harner6
Estimated H-index: 6
(Max Planck Society),
Christian Körner3
Estimated H-index: 3
(Max Planck Society)
+ 7 AuthorsWalter Neupert102
Estimated H-index: 102
(Max Planck Society)
Mitochondria are organelles with a complex architecture. They are bounded by an envelope consisting of the outer membrane and the inner boundary membrane (IBM). Narrow crista junctions (CJs) link the IBM to the cristae. OMs and IBMs are firmly connected by contact sites (CS). The molecular nature of the CS remained unknown. Using quantitative high-resolution mass spectrometry we identified a novel complex, the mitochondrial contact site (MICOS) complex, formed by a set of mitochondrial membrane ...
236 Citations Source Cite
Published on Sep 1, 2012in Journal of Molecular Biology 4.89
Ralf M. Zerbes11
Estimated H-index: 11
(University of Freiburg),
Maria Bohnert20
Estimated H-index: 20
(University of Freiburg)
+ 10 AuthorsMarten Veenhuis71
Estimated H-index: 71
(University of Groningen)
Abstract The mitochondrial inner membrane contains a large protein complex crucial for membrane architecture, the mitochondrial inner membrane organizing system (MINOS). MINOS is required for keeping cristae membranes attached to the inner boundary membrane via crista junctions and interacts with protein complexes of the mitochondrial outer membrane. To study if outer membrane interactions and maintenance of cristae morphology are directly coupled, we generated mutant forms of mitofilin/Fcj1 (fo...
69 Citations Source Cite
Published on Feb 1, 1976in Journal of Eukaryotic Microbiology 2.54
F. J. R. Taylor11
Estimated H-index: 11
(University of British Columbia)
SYNOPSIS. Information relating to the ultrastructure of 4 organellar systems of flagellates—nuclei (including mitosis), flagella, mitochondria and chloroplasts—is examined for bearing on the probable phylogeny of the principal flagellate groups, first considered singly and then in combination. The mitotic mechanism has not proved to be as conservative a character as might be hoped, but still remains characteristic for the average condition in many of the groups. Flagellar features are useful if ...
126 Citations Source Cite
Ramya Purkanti1
Estimated H-index: 1
(National Centre for Biological Sciences),
Mukund Thattai12
Estimated H-index: 12
(National Centre for Biological Sciences)
Eukaryotic cells use dynamins—mechano-chemical GTPases—to drive the division of endosymbiotic organelles. Here we probe early steps of mitochondrial and chloroplast endosymbiosis by tracing the evolution of dynamins. We develop a parsimony-based phylogenetic method for protein sequence reconstruction, with deep time resolution. Using this, we demonstrate that dynamins diversify through the punctuated transformation of sequence segments on the scale of secondary-structural elements. We find examp...
21 Citations Source Cite
Published on Dec 1, 2003in Nature 41.58
Stefan A. Paschen12
Estimated H-index: 12
(Ludwig Maximilian University of Munich),
Thomas Waizenegger9
Estimated H-index: 9
(Ludwig Maximilian University of Munich)
+ 5 AuthorsWalter Neupert102
Estimated H-index: 102
The outer membranes of mitochondria and chloroplasts are distinguished by the presence of β-barrel membrane proteins1, 2. The outer membrane of Gram-negative bacteria also harbours β-barrel proteins3. In mitochondria these proteins fulfil a variety of functions such as transport of small molecules (porin/VDAC), translocation of proteins (Tom40) and regulation of mitochondrial morphology (Mdm10)4, 5, 6, 7. These proteins are encoded by the nucleus, synthesized in the cytosol, targeted to mitochon...
336 Citations Source Cite
Published on Mar 7, 2003in Journal of Biological Chemistry 4.01
Aurélien Olichon9
Estimated H-index: 9
,
Laurent Baricault7
Estimated H-index: 7
+ 4 AuthorsGuy Lenaers27
Estimated H-index: 27
Abstract OPA1 encodes a large GTPase related to dynamins, anchored to the mitochondrial cristae inner membrane, facing the intermembrane space. OPA1haplo-insufficiency is responsible for the most common form of autosomal dominant optic atrophy (ADOA, MIM165500), a neuropathy resulting from degeneration of the retinal ganglion cells and optic nerve atrophy. Here we show that down-regulation of OPA1 in HeLa cells using specific small interfering RNA (siRNA) leads to fragmentation of the mitochondr...
728 Citations Source Cite
Published on Jan 1, 1987in Parasitology Research 2.56
Shigehiko Uni21
Estimated H-index: 21
(Osaka City University),
Motohiro Iseki12
Estimated H-index: 12
(Osaka City University)
+ 2 AuthorsSuehisa Takada9
Estimated H-index: 9
(Osaka City University)
The ultrastructure of Cryptosporidium muris, which parasitizes the stomach of mice, was studied by transmission electron microscopy. The entire development of the parasite occurred in the microvilli of the surface mucus cells in the gastric glands. The ultrastructural features of the attachment site of C. muris to the host cell differed remarkably from those of C. parvum and its closely related species, which parasitize the intestine of various animals. The size of C. muris was greater at almost...
53 Citations Source Cite
Published on Jun 24, 2014in PLOS Biology 9.16
Patrick J. Keeling69
Estimated H-index: 69
(University of British Columbia),
Fabien Burki25
Estimated H-index: 25
(University of British Columbia)
+ 78 AuthorsCallum J. Bell11
Estimated H-index: 11
(National Center for Genome Resources)
Current sampling of genomic sequence data from eukaryotes is relatively poor, biased, and inadequate to address important questions about their biology, evolution, and ecology; this Community Page describes a resource of 700 transcriptomes from marine microbial eukaryotes to help understand their role in the world's oceans.
321 Citations Source Cite
Published on May 24, 1991in Science 41.06
A Lupas1
Estimated H-index: 1
(Princeton University),
Mm Van Dyke2
Estimated H-index: 2
(Princeton University),
Jeff Stock30
Estimated H-index: 30
(Princeton University)
The probability that a residue in a protein is part of a coiled-coil structure was assessed by comparison of its flanking sequences with sequences of known coiled-coil proteins. This method was used to delineate coiled-coil domains in otherwise globular proteins, such as the leucine zipper domains in transcriptional regulators, and to predict regions of discontinuity within coiled-coil structures, such as the hinge region in myosin
3,247 Citations Source Cite
  • References (52)
  • Citations (30)
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Cited By30
Published on Jan 1, 2016in Biochimica et Biophysica Acta 3.44
Martijn A. Huynen60
Estimated H-index: 60
(Radboud University Nijmegen),
Mareike Mühlmeister5
Estimated H-index: 5
(Radboud University Nijmegen)
+ 2 AuthorsUlrich Brandt58
Estimated H-index: 58
(Goethe University Frankfurt)
We have analyzed the distribution of mitochondrial contact site and cristae organizing system (MICOS) complex proteins and mitochondrial intermembrane space bridging complex (MIB) proteins over (sub)complexes and over species. The MICOS proteins are associated with the formation and maintenance of mitochondrial cristae. Indeed, the presence of MICOS genes in genomes correlates well with the presence of cristae: all cristae containing species have at least one MICOS gene and cristae-less species ...
43 Citations Source Cite
Published on Aug 1, 2016in Biochimica et Biophysica Acta 3.44
Jeremy G. Wideman12
Estimated H-index: 12
(University of Exeter),
Sergio A. Muñoz-Gómez6
Estimated H-index: 6
(Dalhousie University)
Abstract The ER–mitochondria organizing network (ERMIONE) in Saccharomyces cerevisiae is involved in maintaining mitochondrial morphology and lipid homeostasis. ERMES and MICOS are two scaffolding complexes of ERMIONE that contribute to these processes. ERMES is ancient but has been lost in several lineages including animals, plants, and SAR (stramenopiles, alveolates and rhizaria). On the other hand, MICOS is ancient and has remained present in all organisms bearing mitochondrial cristae. The E...
21 Citations Source Cite
Published on Mar 1, 2016in Trends in Biochemical Sciences 15.68
Sara Cogliati3
Estimated H-index: 3
(Centro Nacional de Investigaciones Cardiovasculares),
José Antonio Enríquez47
Estimated H-index: 47
(University of Zaragoza),
Luca Scorrano66
Estimated H-index: 66
(University of Padua)
Mitochondrial cristae are dynamic bioenergetic compartments whose shape changes under different physiological conditions. Recent discoveries have unveiled the relation between cristae shape and oxidative phosphorylation (OXPHOS) function, suggesting that membrane morphology modulates the organization and function of the OXPHOS system, with a direct impact on cellular metabolism. As a corollary, cristae-shaping proteins have emerged as potential modulators of mitochondrial bioenergetics, a concep...
112 Citations Source Cite
Published on Mar 1, 2016in Current Biology 9.25
Morgane Michaud9
Estimated H-index: 9
(Centre national de la recherche scientifique),
Valérie Gros28
Estimated H-index: 28
(Centre national de la recherche scientifique)
+ 10 AuthorsDenis Falconet18
Estimated H-index: 18
(Centre national de la recherche scientifique)
The mitochondrion is an organelle originating from an endosymbiotic event and playing a role in several fundamental processes such as energy production, metabolite syntheses, and programmed cell death. This organelle is delineated by two membranes whose synthesis requires an extensive exchange of phospholipids with other cellular organelles such as endoplasmic reticulum (ER) and vacuolar membranes in yeast. These transfers of phospholipids are thought to occur by a non-vesicular pathway at conta...
33 Citations Source Cite
Published on Feb 1, 2016in Current Opinion in Cell Biology 10.02
Vaishali Jayashankar4
Estimated H-index: 4
(University of California, Irvine),
Irina A. Mueller3
Estimated H-index: 3
(University of California, Irvine),
Susanne M. Rafelski12
Estimated H-index: 12
(University of California, Irvine)
Mitochondria are complex organelles with a highly regulated architecture across all levels of organization. The architecture of the inner mitochondrial membrane (IMM) provides a crucial platform for many mitochondrial functions while mitochondrial network architecture is crucial for coordinating these activities throughout the cell. This review summarizes the recent findings regarding the most important shaping factors that regulate IMM organization, how IMM architecture supports bioenergetic fu...
8 Citations Source Cite
Published on Nov 2, 2015in Communicative & Integrative Biology
Sergio A. Muñoz-Gómez6
Estimated H-index: 6
(Dalhousie University),
Claudio H. Slamovits26
Estimated H-index: 26
(Canadian Institute for Advanced Research)
+ 1 AuthorsJeremy G. Wideman12
Estimated H-index: 12
(University of Exeter)
The MItochondrial Contact Site and Cristae Organizing System (MICOS) is required for the biogenesis and maintenance of mitochondrial cristae as well as the proper tethering of the mitochondrial inner and outer membranes. We recently demonstrated that the core components of MICOS, Mic10 and Mic60, are near-ubiquitous eukaryotic features inferred to have been present in the last eukaryote common ancestor. We also showed that Mic60 could be traced to α-proteobacteria, which suggests that mitochondr...
12 Citations Source Cite
Published on Apr 1, 2016in Journal of Molecular Biology 4.89
Ralf M. Zerbes11
Estimated H-index: 11
(University of Freiburg),
Philipp Höß3
Estimated H-index: 3
(University of Freiburg)
+ 2 AuthorsMaria Bohnert20
Estimated H-index: 20
(University of Freiburg)
Abstract The mitochondrial inner membrane consists of two morphologically distinct domains, the inner boundary membrane and large invaginations termed cristae. Narrow membrane structures, the crista junctions, link these two domains. Maintenance of this elaborate architecture depends on the evolutionarily conserved mitochondrial contact site and cristae organizing system (MICOS), a multisubunit inner membrane protein complex. MICOS consists of two functional modules, a Mic60–Mic19 subcomplex tha...
21 Citations Source Cite
Published on Aug 1, 2016in Current Opinion in Cell Biology 10.02
Martin van der Laan35
Estimated H-index: 35
(Saarland University),
Susanne E. Horvath11
Estimated H-index: 11
(University of Freiburg),
Nikolaus Pfanner97
Estimated H-index: 97
(University of Freiburg)
Mitochondria possess two membranes of different architecture. The outer membrane surrounds the organelle, whereas the inner membrane consists of two domains. The inner boundary membrane that is adjacent to the outer membrane harbors many protein translocases. The inner membrane cristae form deep invaginations that carry respiratory chain complexes and the ATP synthase. It has remained enigmatic how crista junctions that connect inner boundary membrane and cristae are formed. The identification o...
52 Citations Source Cite
Published on Aug 1, 2016in Trends in Ecology and Evolution 15.94
Maureen A. O’Malley10
Estimated H-index: 10
(University of Bordeaux),
Jeremy G. Wideman12
Estimated H-index: 12
(University of Exeter),
Iñaki Ruiz-Trillo28
Estimated H-index: 28
(University of Barcelona)
Macroevolutionary patterns can be produced by combinations of diverse and even oppositional dynamics. A growing body of data indicates that secondary simplifications of molecular and cellular structures are common. Some major diversifications in eukaryotes have occurred because of loss and minimalisation; numerous episodes in prokaryote evolution have likewise been driven by the reduction of structure. After examining a range of examples of secondary simplification and its consequences across th...
15 Citations Source Cite
Published on Jan 1, 2017in Cell and Tissue Research 3.04
Vera Kozjak-Pavlovic16
Estimated H-index: 16
(University of Würzburg)
Mitochondria are organelles of endosymbiotic origin, surrounded by two membranes. The inner membrane forms invaginations called cristae that enhance its surface and are important for mitochondrial function. A recently described mitochondrial contact site and cristae organizing system (MICOS) in the inner mitochondrial membrane is crucial for the formation and maintenance of cristae structure. The MICOS complex in human mitochondria exhibits specificities and greater complexity in comparison to t...
31 Citations Source Cite
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