Abstract
The eukaryotic organelles mitochondrion and plastid originated from eubacterial endosymbionts. Here we propose that, in both cases, prokaryote-to-organelle conversion was driven by the internalization of host-encoded factors progressing from the outer membrane of the endosymbionts towards the intermembrane space, inner membrane and finally the organelle interior. This was made possible by an outside-to-inside establishment in the endosymbionts of host-controlled protein-sorting components, which enabled the gradual integration of organelle functions into the nuclear genome. Such a convergent trajectory for mitochondrion and plastid establishment suggests a novel paradigm for organelle evolution that affects theories of eukaryogenesis.
This is a preview of subscription content, access via your institution
Access options
Subscribe to this journal
Receive 12 print issues and online access
$189.00 per year
only $15.75 per issue
Rent or buy this article
Prices vary by article type
from$1.95
to$39.95
Prices may be subject to local taxes which are calculated during checkout
Similar content being viewed by others
References
Bhattacharya, D., Archibald, J. M., Weber, A. P. & Reyes-Prieto, A. How do endosymbionts become organelles? Understanding early events in plastid evolution. Bioessays 29, 1239–1246 (2007).
Reyes-Prieto, A., Weber, A. P. & Bhattacharya, D. The origin and establishment of the plastid in algae and plants. Annu. Rev. Genet. 41, 147–168 (2007).
de Duve, C. The origin of eukaryotes: a reappraisal. Nature Rev. Genet. 8, 395–403 (2007).
Dolezal, P., Likic, V., Tachezy, J. & Lithgow, T. Evolution of the molecular machines for protein import into mitochondria. Science 313, 314–318 (2006).
Dyall, S. D., Brown, M. T. & Johnson, P. J. Ancient invasions: from endosymbionts to organelles. Science 304, 253–257 (2004).
Cavalier-Smith, T. Origin of mitochondria by intracellular enslavement of a photosynthetic purple bacterium. Proc. Biol. Sci. 273, 1943–1952 (2006).
Martin, W. & Muller, M. The hydrogen hypothesis for the first eukaryote. Nature 392, 37–41 (1998).
Martin, W. & Koonin, E. V. Introns and the origin of nucleus–cytosol compartmentalization. Nature 440, 41–45 (2006).
Yoon, H. S., Hackett, J. D., Ciniglia, C., Pinto, G. & Bhattacharya, D. A molecular timeline for the origin of photosynthetic eukaryotes. Mol. Biol. Evol. 21, 809–818 (2004).
Martin, W. & Herrmann, R. G. Gene transfer from organelles to the nucleus: how much, what happens, and why? Plant Physiol. 118, 9–17 (1998).
Kurland, C. G. & Andersson, S. G. Origin and evolution of the mitochondrial proteome. Microbiol. Mol. Biol. Rev. 64, 786–820 (2000).
Andersson, S. G., Karlberg, O., Canback, B. & Kurland, C. G. On the origin of mitochondria: a genomics perspective. Philos. Trans. R. Soc. Lond. B 358, 165–177 (2003); discussion 177–179.
Richly, E. & Leister, D. An improved prediction of chloroplast proteins reveals diversities and commonalities in the chloroplast proteomes of Arabidopsis and rice. Gene 329, 11–16 (2004).
Panigrahi, A. K. et al. A comprehensive analysis of Trypanosoma brucei mitochondrial proteome. Proteomics 9, 434–450 (2009).
Moran, N. A. Accelerated evolution and Muller's rachet in endosymbiotic bacteria. Proc. Natl Acad. Sci. USA 93, 2873–2878 (1996).
Reyes-Prieto, A., Hackett, J. D., Soares, M. B., Bonaldo, M. F. & Bhattacharya, D. Cyanobacterial contribution to algal nuclear genomes is primarily limited to plastid functions. Curr. Biol. 16, 2320–2325 (2006).
Tyra, H. M., Linka, M., Weber, A. P. & Bhattacharya, D. Host origin of plastid solute transporters in the first photosynthetic eukaryotes. Genome Biol. 8, R212 (2007).
Moustafa, A., Reyes-Prieto, A. & Bhattacharya, D. Chlamydiae has contributed at least 55 genes to Plantae with predominantly plastid functions. PLoS ONE 3, e2205 (2008).
Reumann, S. & Keegstra, K. The endosymbiotic origin of the protein import machinery of chloroplastic envelope membranes. Trends Plant Sci. 4, 302–307 (1999).
Reumann, S., Inoue, K. & Keegstra, K. Evolution of the general protein import pathway of plastids (review). Mol. Membr. Biol. 22, 73–86 (2005).
Gross, J. & Bhattacharya, D. Revaluating the evolution of the Toc and Tic protein translocons. Trends Plant Sci. 14, 13–20 (2009).
Neupert, W. & Herrmann, J. M. Translocation of proteins into mitochondria. Annu. Rev. Biochem. 76, 723–749 (2007).
Kutik, S., Guiard, B., Meyer, H. E., Wiedemann, N. & Pfanner, N. Cooperation of translocase complexes in mitochondrial protein import. J. Cell Biol. 179, 585–591 (2007).
Lister, R., Hulett, J. M., Lithgow, T. & Whelan, J. Protein import into mitochondria: origins and functions today (review). Mol. Membr. Biol. 22, 87–100 (2005).
Herrmann, J. M. Converting bacteria to organelles: evolution of mitochondrial protein sorting. Trends Microbiol. 11, 74–79 (2003).
Ruiz, N., Kahne, D. & Silhavy, T. J. Advances in understanding bacterial outer-membrane biogenesis. Nature Rev. Microbiol. 4, 57–66 (2006).
Wunder, T., Martin, R., Loffelhardt, W., Schleiff, E. & Steiner, J. M. The invariant phenylalanine of precursor proteins discloses the importance of Omp85 for protein translocation into cyanelles. BMC Evol. Biol. 7, 236 (2007).
Inoue, K. & Keegstra, K. A polyglycine stretch is necessary for proper targeting of the protein translocation channel precursor to the outer envelope membrane of chloroplasts. Plant J. 34, 661–669 (2003).
Inoue, K. & Potter, D. The chloroplastic protein translocation channel Toc75 and its paralog OEP80 represent two distinct protein families and are targeted to the chloroplastic outer envelope by different mechanisms. Plant J. 39, 354–365 (2004).
Patel, R., Hsu, S. C., Bedard, J., Inoue, K. & Jarvis, P. The Omp85-related chloroplast outer envelope protein OEP80 is essential for viability in Arabidopsis. Plant Physiol. 148, 235–245 (2008).
Walther, D. M., Papic, D., Bos, M. P., Tommassen, J. & Rapaport, D. Signals in bacterial β-barrel proteins are functional in eukaryotic cells for targeting to and assembly in mitochondria. Proc. Natl Acad. Sci. USA 106, 2531–2356 (2009).
Duy, D., Soll, J. & Philippar, K. Solute channels of the outer membrane: from bacteria to chloroplasts. Biol. Chem. 388, 879–889 (2007).
Gentle, I. E. et al. Conserved motifs reveal details of ancestry and structure in the small TIM chaperones of the mitochondrial intermembrane space. Mol. Biol. Evol. 24, 1149–1160 (2007).
Alcock, F. H. et al. Conserved substrate binding by chaperones in the bacterial periplasm and the mitochondrial intermembrane space. Biochem. J. 409, 377–387 (2008).
Beverly, K. N., Sawaya, M. R., Schmid, E. & Koehler, C. M. The Tim8–Tim13 complex has multiple substrate binding sites and binds cooperatively to Tim23. J. Mol. Biol. 382, 1144–1156 (2008).
Allen, J. W., Ferguson, S. J. & Ginger, M. L. Distinctive biochemistry in the trypanosome mitochondrial intermembrane space suggests a model for stepwise evolution of the MIA pathway for import of cysteine-rich proteins. FEBS Lett. 582, 2817–2825 (2008).
Weber, A. P. & Fischer, K. Making the connections — the crucial role of metabolite transporters at the interface between chloroplast and cytosol. FEBS Lett. 581, 2215–2222 (2007).
Kunji, E. R. The role and structure of mitochondrial carriers. FEBS Lett. 564, 239–244 (2004).
Schneider, A. et al. An Arabidopsis thaliana knock-out mutant of the chloroplast triose phosphate/phosphate translocator is severely compromised only when starch synthesis, but not starch mobilisation is abolished. Plant J. 32, 685–699 (2002).
Firlej-Kwoka, E., Strittmatter, P., Soll, J. & Bolter, B. Import of preproteins into the chloroplast inner envelope membrane. Plant Mol. Biol. 68, 505–519 (2008).
Rassow, J., Dekker, P. J., van Wilpe, S., Meijer, M. & Soll, J. The preprotein translocase of the mitochondrial inner membrane: function and evolution. J. Mol. Biol. 286, 105–120 (1999).
van der Laan, M. et al. A role for Tim21 in membrane-potential-dependent preprotein sorting in mitochondria. Curr. Biol. 16, 2271–2276 (2006).
van der Laan, M. et al. Motor-free mitochondrial presequence translocase drives membrane integration of preproteins. Nature Cell Biol. 9, 1152–1159 (2007).
Popov-Celeketic, D., Mapa, K., Neupert, W. & Mokranjac, D. Active remodelling of the TIM23 complex during translocation of preproteins into mitochondria. EMBO J. 27, 1469–1480 (2008).
Gruhler, A. et al. N-terminal hydrophobic sorting signals of preproteins confer mitochondrial hsp70 independence for import into mitochondria. J. Biol. Chem. 272, 17410–17415 (1997).
Wiedemann, N., van der Laan, M., Hutu, D. P., Rehling, P. & Pfanner, N. Sorting switch of mitochondrial presequence translocase involves coupling of motor module to respiratory chain. J. Cell Biol. 179, 1115–1122 (2007).
Acin-Perez, R., Fernandez-Silva, P., Peleato, M. L., Perez-Martos, A. & Enriquez, J. A. Respiratory active mitochondrial supercomplexes. Mol. Cell 32, 529–539 (2008).
Richter, O. M. & Ludwig, B. Cytochrome c oxidase — structure, function, and physiology of a redox-driven molecular machine. Rev. Physiol. Biochem. Pharmacol. 147, 47–74 (2003).
Cardol, P. et al. The mitochondrial oxidative phosphorylation proteome of Chlamydomonas reinhardtii deduced from the Genome Sequencing Project. Plant Physiol. 137, 447–459 (2005).
Brandt, U. et al. Structure–function relationships in mitochondrial complex I of the strictly aerobic yeast Yarrowia lipolytica. Biochem. Soc. Trans. 33, 840–844 (2005).
Zara, V., Conte, L. & Trumpower, B. L. Biogenesis of the yeast cytochrome bc1 complex. Biochim. Biophys. Acta 1793, 89–96 (2009).
Lazarou, M., Thorburn, D. R., Ryan, M. T. & McKenzie, M. Assembly of mitochondrial complex I and defects in disease. Biochim. Biophys. Acta 1793, 78–88 (2009).
Fontanesi, F., Soto, I. C., Horn, D. & Barrientos, A. Assembly of mitochondrial cytochrome c-oxidase, a complicated and highly regulated cellular process. Am. J. Physiol. Cell Physiol. 291, C1129–C1147 (2006).
Howell, K. A. et al. Oxygen initiation of respiration and mitochondrial biogenesis in rice. J. Biol. Chem. 282, 15619–15631 (2007).
Schulte, U. et al. A family of mitochondrial proteins involved in bioenergetics and biogenesis. Nature 339, 147–149 (1989).
Glaser, E. & Dessi, P. Integration of the mitochondrial-processing peptidase into the cytochrome bc1 complex in plants. J. Bioenerg. Biomembr. 31, 259–274 (1999).
Deng, K., Shenoy, S. K., Tso, S. C., Yu, L. & Yu, C. A. Reconstitution of mitochondrial processing peptidase from the core proteins (subunits I and II) of bovine heart mitochondrial cytochrome bc1 complex. J. Biol. Chem. 276, 6499–6505 (2001).
Brown, M. T. et al. A functionally divergent hydrogenosomal peptidase with protomitochondrial ancestry. Mol. Microbiol. 64, 1154–1163 (2007).
Frazier, A. E. et al. Pam16 has an essential role in the mitochondrial protein import motor. Nature Struct. Mol. Biol. 11, 226–233 (2004).
Bonnefoy, N., Fiumera, H. L., Dujardin, G. & Fox, T. D. Roles of Oxa1-related inner-membrane translocases in assembly of respiratory chain complexes. Biochim. Biophys. Acta 1793, 60–70 (2009).
Jarvis, P. Targeting of nucleus-encoded proteins to chloroplasts in plants. New Phytol. 179, 257–285 (2008).
Vojta, L., Soll, J. & Bolter, B. Protein transport in chloroplasts — targeting to the intermembrane space. FEBS J. 274, 5043–5054 (2007).
Brink, S. et al. Preproteins of chloroplast envelope inner membrane contain targeting information for receptor-dependent import into fungal mitochondria. J. Biol. Chem. 269, 16478–16485 (1994).
Jackson-Constan, D., Akita, M. & Keegstra, K. Molecular chaperones involved in chloroplast protein import. Biochim. Biophys. Acta 1541, 102–113 (2001).
Brink, S., Fischer, K., Klosgen, R. B. & Flugge, U. I. Sorting of nuclear-encoded chloroplast membrane proteins to the envelope and the thylakoid membrane. J. Biol. Chem. 270, 20808–20815 (1995).
Knight, J. S. & Gray, J. C. The N-terminal hydrophobic region of the mature phosphate translocator is sufficient for targeting to the chloroplast inner envelope membrane. Plant Cell 7, 1421–1432 (1995).
Chiu, C. C. & Li, H. M. Tic40 is important for reinsertion of proteins from the chloroplast stroma into the inner membrane. Plant J. 56, 793–801 (2008).
Balsera, M. et al. Characterization of Tic110, a channel-forming protein at the inner envelope membrane of chloroplasts, unveils a response to Ca2+ and a stromal regulatory disulfide bridge. J. Biol. Chem. 284, 2603–2616 (2009).
Inaba, T. et al. Arabidopsis tic110 is essential for the assembly and function of the protein import machinery of plastids. Plant Cell 17, 1482–1496 (2005).
Vojta, L., Soll, J. & Bolter, B. Requirements for a conservative protein translocation pathway in chloroplasts. FEBS Lett. 581, 2621–2624 (2007).
Blobel, G. Intracellular protein topogenesis. Proc. Natl Acad. Sci. USA 77, 1496–1500 (1980).
Tamames, J. et al. The frontier between cell and organelle: genome analysis of Candidatus Carsonella ruddii. BMC Evol. Biol. 7, 181 (2007).
Yoon, H. S., Reyes-Prieto, A., Melkonian, M. & Bhattacharya, D. Minimal plastid genome evolution in the Paulinella endosymbiont. Curr. Biol. 16, R670–672 (2006).
Yamano, K. et al. Tom20 and Tom22 share the common signal recognition pathway in mitochondrial protein import. J. Biol. Chem. 283, 3799–3807 (2008).
Kutik, S. et al. Dissecting membrane insertion of mitochondrial β-barrel proteins. Cell 132, 1011–1024 (2008).
Zientz, E., Dandekar, T. & Gross, R. Metabolic interdependence of obligate intracellular bacteria and their insect hosts. Microbiol. Mol. Biol. Rev. 68, 745–770 (2004).
Janssen, M. J., Koorengevel, M. C., de Kruijff, B. & de Kroon, A. I. Transbilayer movement of phosphatidylcholine in the mitochondrial outer membrane of Saccharomyces cerevisiae is rapid and bidirectional. Biochim. Biophys. Acta 1421, 64–76 (1999).
de Azevedo-Martins, A. C., Frossard, M. L., de Souza, W., Einicker-Lamas, M. & Motta, M. C. Phosphatidylcholine synthesis in Crithidia deanei: the influence of the endosymbiont. FEMS Microbiol. Lett. 275, 229–236 (2007).
Benning, C. A role for lipid trafficking in chloroplast biogenesis. Prog. Lipid Res. 47, 381–389 (2008).
Lee, D. H., Severin, K., Yokobayashi, Y. & Ghadiri, M. R. Emergence of symbiosis in peptide self-replication through a hypercyclic network. Nature 390, 591–594 (1997).
Chacinska, A. et al. Mitochondrial biogenesis, switching the sorting pathway of the intermembrane space receptor Mia40. J. Biol. Chem. 283, 29723–29729 (2008).
Acknowledgements
D.B. acknowledges support from the National Science Foundation and the National Institutes of Health. The authors also thank W. Lanier (Iowa) for a critical reading of the manuscript.
Author information
Authors and Affiliations
Corresponding author
Supplementary information
Supplementary Table 1
Function and phylogenetic affiliation of molecular components involved in protein sorting in the mitochondrion (Saccharomyces cerevisiae) and plastid (Pisum sativum). (PDF 367 kb)
Related links
Glossary
- β-Barrel proteins
-
A class of membrane proteins composed of antiparallel β-strands that form barrel-type pores. Porins are typical β-barrel pores in the outer membrane of Gram-negative bacteria.
- Chaperones
-
These are molecular components that fold, unfold, stabilize or escort the transit of protein substrates. In addition, chaperones such as the 70 kDa heat shock protein (Hsp70) and Hsp93 hydrolyse ATP to provide the energy for protein import across organelle membranes.
- Endosymbiotic gene transfer
-
The migration and fixation of endosymbiont genes in the nuclear genome of the host.
- Muller's ratchet
-
Describes the progressive irreversible accumulation of deleterious mutations in asexual populations. Muller's ratchet explains the genomic and physiological degeneration that is usually observed among obligatory endosymbionts.
- Membrane anchor signal
-
This is a topogenic signal used to anchor a membrane protein in the lipid bilayer. The core of a membrane anchor signal is usually the first hydrophobic α-helix that is C-terminal to the presequence.
- Presequence
-
This is a transient topogenic signal appended to the N-terminus of a sorted protein that is cleaved from the mature protein.
- Presequence translocase-associated motor
-
(PAM). This is a module of the Tim23 complex associated with Hsp70 that provides the energy for translocation of proteins across the mitochondrial inner membrane. In yeast, PAM is composed of the structural platform Tim44, the co-chaperones Pam14, Pam16 and Pam18, and the nucleotide exchange factor Mge1.
- Single transmembrane domain
-
(STMD). α-Helical STMDs are found in membrane proteins, and fold into a hydrophobic, helical structure spanning the lipid bilayer.
- Sorting and assembly machinery
-
(SAM). The Sam complex inserts and assembles β-barrel proteins in the OM of mitochondria. In yeast, it is comprised of the protein pore Sam50 and the peripheral subunits Sam35 and Sam37.
- Sorting substrate
-
This is a protein that is relocated by the catalytic action of a translocase or an insertase. A sorting substrate is also referred to as a precursor or a preprotein.
- Tic
-
(Translocon at the inner envelope membrane of chloroplasts). In higher plants, the Tic complex is composed of the protein-conducting channel Tic110, the putative protein pores Tic20 and Tic21, the intermembrane space protein Tic22, the chaperone Hsp93 and its co-chaperone Toc40. Tic32, Tic55 and Tic62 are regulatory subunits.
- Tim22 insertase
-
An insertase is a molecular machine usually consisting of a receptor and a protein pore that recognizes specific protein substrates and catalyses their insertion into the lipid bilayer of a membrane. The Tim22 insertase is specialized in the insertion of the mitochondrial carriers into the inner membrane. In yeast, it is comprised of the Tim22 protein pore and the subunits Tim54 and Tim18.
- Tim23
-
(Translocase of the mitochondrial inner membrane). In yeast, the Tim23 and Tim17 subunits constitute the protein-conducting pore of the Tim23 complex that, in combination with Tim50 and Tim21, acts as an insertase for single transmembrane domain proteins. The addition of the PAM module confers a translocase function for the Tim23 complex.
- Toc
-
(Translocon at the outer envelope membrane of chloroplasts). In higher plants, the Toc complex is composed of the protein-conducting pore Toc75, the receptors Toc34 and Toc159, and the accessory subunits Toc12 and Toc64.
- Tom
-
(Translocase of the mitochondrial outer membrane). In yeast, the Tom complex is formed by the Tom40 protein-conducting pore, the receptors Tom22, Tom20 and Tom70, and the structural subunits Tom5, Tom6 and Tom7
- Topogenic signal
-
This is a segment of amino acids in a sorted protein that provides information about its final location and conformation (topology) in a cellular compartment.
- Translocon
-
A molecular machine usually consisting of a receptor and a protein pore that recognizes specific protein substrates and catalyses their movement across a membrane. 'Translocase' is a general term to describe an enzyme that facilitates the movement of a molecule, usually across a membrane.
Rights and permissions
About this article
Cite this article
Gross, J., Bhattacharya, D. Mitochondrial and plastid evolution in eukaryotes: an outsiders' perspective. Nat Rev Genet 10, 495–505 (2009). https://doi.org/10.1038/nrg2610
Issue Date:
DOI: https://doi.org/10.1038/nrg2610
This article is cited by
-
A break in mitochondrial endosymbiosis as a basis for inflammatory diseases
Nature (2024)
-
Characterization of signal and transit peptides based on motif composition and taxon-specific patterns
Scientific Reports (2023)
-
Sestrins: Darkhorse in the regulation of mitochondrial health and metabolism
Molecular Biology Reports (2020)
-
Evolution of mitochondrial TAT translocases illustrates the loss of bacterial protein transport machines in mitochondria
BMC Biology (2018)
-
Identification and Characterization of a Bacterial Homolog of Chloride Intracellular Channel (CLIC) Protein
Scientific Reports (2017)