Abstract
Recent findings are summarized in support of the view that mitochondria (including hydrogenosomes) and plastids (including complex ones) descend from symbiotic associations of once free-living organisms. The reasoning behind endosymbiotic hypotheses stems from a comparison of biochemistry and physiology in organelles with that in free-living cells; their strength is shown to lie in the specific testable predictions they generate about expected similarity patterns among genes. Although disdained for many decades, endosymbiotic hypotheses have gradually become very popular. In the wake of that popularity, endosymbiotic hypotheses have been formulated to explain the origins of eukaryotic cell compartments and structures that have no biochemical similarity to free-living cells. In particular, it has become fashionable in recent years to entertain the century-old notion that the nucleus might also descend from an endosymbiotic bacterium. A critique of that hypothesis is formulated and a simple alternative to it is outlined, which derives the nuclear compartment in a mitochondrion-bearing cell.
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- Akhmanova A., Voncken F., van Alen T., van Hoek A., Boxma B., Vogels G., Veenhuis M., Hackstein J. H. A hydrogenosome with a genome. Nature. 1998 Dec 10;396(6711):527–528. doi: 10.1038/25023. [DOI] [PubMed] [Google Scholar]
- Andersson S. G., Zomorodipour A., Andersson J. O., Sicheritz-Pontén T., Alsmark U. C., Podowski R. M., Näslund A. K., Eriksson A. S., Winkler H. H., Kurland C. G. The genome sequence of Rickettsia prowazekii and the origin of mitochondria. Nature. 1998 Nov 12;396(6707):133–140. doi: 10.1038/24094. [DOI] [PubMed] [Google Scholar]
- Bakker B. M., Michels P. A., Opperdoes F. R., Westerhoff H. V. Glycolysis in bloodstream form Trypanosoma brucei can be understood in terms of the kinetics of the glycolytic enzymes. J Biol Chem. 1997 Feb 7;272(6):3207–3215. doi: 10.1074/jbc.272.6.3207. [DOI] [PubMed] [Google Scholar]
- Benchimol M., Durand R., Almeida J. C. A double membrane surrounds the hydrogenosomes of the anaerobic fungus Neocallimastix frontalis. FEMS Microbiol Lett. 1997 Sep 15;154(2):277–282. doi: 10.1111/j.1574-6968.1997.tb12656.x. [DOI] [PubMed] [Google Scholar]
- Blattner J., Helfert S., Michels P., Clayton C. Compartmentation of phosphoglycerate kinase in Trypanosoma brucei plays a critical role in parasite energy metabolism. Proc Natl Acad Sci U S A. 1998 Sep 29;95(20):11596–11600. doi: 10.1073/pnas.95.20.11596. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bogorad L. Evolution of organelles and eukaryotic genomes. Science. 1975 May 30;188(4191):891–898. doi: 10.1126/science.1138359. [DOI] [PubMed] [Google Scholar]
- Bui E. T., Bradley P. J., Johnson P. J. A common evolutionary origin for mitochondria and hydrogenosomes. Proc Natl Acad Sci U S A. 1996 Sep 3;93(18):9651–9656. doi: 10.1073/pnas.93.18.9651. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Cavalier-Smith T. Cell and genome coevolution: facultative anaerobiosis, glycosomes and kinetoplastan RNA editing. Trends Genet. 1997 Jan;13(1):6–9. doi: 10.1016/s0168-9525(96)30116-9. [DOI] [PubMed] [Google Scholar]
- Cavalier-Smith T., Chao E. E. Molecular phylogeny of the free-living archezoan Trepomonas agilis and the nature of the first eukaryote. J Mol Evol. 1996 Dec;43(6):551–562. doi: 10.1007/BF02202103. [DOI] [PubMed] [Google Scholar]
- Cavalier-Smith T. Eukaryotes with no mitochondria. 1987 Mar 26-Apr 1Nature. 326(6111):332–333. doi: 10.1038/326332a0. [DOI] [PubMed] [Google Scholar]
- Cavalier-Smith T. Origin of the cell nucleus. Bioessays. 1988 Aug-Sep;9(2-3):72–78. doi: 10.1002/bies.950090209. [DOI] [PubMed] [Google Scholar]
- Cavalier-Smith T. The origin of eukaryotic and archaebacterial cells. Ann N Y Acad Sci. 1987;503:17–54. doi: 10.1111/j.1749-6632.1987.tb40596.x. [DOI] [PubMed] [Google Scholar]
- Cavalier-Smith T. The simultaneous symbiotic origin of mitochondria, chloroplasts, and microbodies. Ann N Y Acad Sci. 1987;503:55–71. doi: 10.1111/j.1749-6632.1987.tb40597.x. [DOI] [PubMed] [Google Scholar]
- Cavalier-tsmith T. The origin of nuclei and of eukaryotic cells. Nature. 1975 Aug 7;256(5517):463–468. doi: 10.1038/256463a0. [DOI] [PubMed] [Google Scholar]
- Chistoserdova L., Vorholt J. A., Thauer R. K., Lidstrom M. E. C1 transfer enzymes and coenzymes linking methylotrophic bacteria and methanogenic Archaea. Science. 1998 Jul 3;281(5373):99–102. doi: 10.1126/science.281.5373.99. [DOI] [PubMed] [Google Scholar]
- Clark C. G., Roger A. J. Direct evidence for secondary loss of mitochondria in Entamoeba histolytica. Proc Natl Acad Sci U S A. 1995 Jul 3;92(14):6518–6521. doi: 10.1073/pnas.92.14.6518. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Clayton C. E., Michels P. Metabolic compartmentation in African trypanosomes. Parasitol Today. 1996 Dec;12(12):465–471. doi: 10.1016/s0169-4758(96)10073-9. [DOI] [PubMed] [Google Scholar]
- De Duve C. Evolution of the peroxisome. Ann N Y Acad Sci. 1969 Dec 19;168(2):369–381. doi: 10.1111/j.1749-6632.1969.tb43124.x. [DOI] [PubMed] [Google Scholar]
- Desai A., Mitchison T. J. Tubulin and FtsZ structures: functional and therapeutic implications. Bioessays. 1998 Jul;20(7):523–527. doi: 10.1002/(SICI)1521-1878(199807)20:7<523::AID-BIES1>3.0.CO;2-L. [DOI] [PubMed] [Google Scholar]
- Doolittle R. F. Microbial genomes opened up. Nature. 1998 Mar 26;392(6674):339–342. doi: 10.1038/32789. [DOI] [PubMed] [Google Scholar]
- Doolittle W. F. A paradigm gets shifty. Nature. 1998 Mar 5;392(6671):15–16. doi: 10.1038/32033. [DOI] [PubMed] [Google Scholar]
- Doolittle W. F. Fun with genealogy. Proc Natl Acad Sci U S A. 1997 Nov 25;94(24):12751–12753. doi: 10.1073/pnas.94.24.12751. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Douglas S. E., Murphy C. A., Spencer D. F., Gray M. W. Cryptomonad algae are evolutionary chimaeras of two phylogenetically distinct unicellular eukaryotes. Nature. 1991 Mar 14;350(6314):148–151. doi: 10.1038/350148a0. [DOI] [PubMed] [Google Scholar]
- Douglas S. E. Plastid evolution: origins, diversity, trends. Curr Opin Genet Dev. 1998 Dec;8(6):655–661. doi: 10.1016/s0959-437x(98)80033-6. [DOI] [PubMed] [Google Scholar]
- Embley T. M., Hirt R. P. Early branching eukaryotes? Curr Opin Genet Dev. 1998 Dec;8(6):624–629. doi: 10.1016/s0959-437x(98)80029-4. [DOI] [PubMed] [Google Scholar]
- Embley T. M., Martin W. A hydrogen-producing mitochondrion. Nature. 1998 Dec 10;396(6711):517–519. doi: 10.1038/24994. [DOI] [PubMed] [Google Scholar]
- Germot A., Philippe H., Le Guyader H. Evidence for loss of mitochondria in Microsporidia from a mitochondrial-type HSP70 in Nosema locustae. Mol Biochem Parasitol. 1997 Aug;87(2):159–168. doi: 10.1016/s0166-6851(97)00064-9. [DOI] [PubMed] [Google Scholar]
- Gilson P. R., Maier U. G., McFadden G. I. Size isn't everything: lessons in genetic miniaturisation from nucleomorphs. Curr Opin Genet Dev. 1997 Dec;7(6):800–806. doi: 10.1016/s0959-437x(97)80043-3. [DOI] [PubMed] [Google Scholar]
- Gray M. W., Burger G., Lang B. F. Mitochondrial evolution. Science. 1999 Mar 5;283(5407):1476–1481. doi: 10.1126/science.283.5407.1476. [DOI] [PubMed] [Google Scholar]
- Gray M. W., Doolittle W. F. Has the endosymbiont hypothesis been proven? Microbiol Rev. 1982 Mar;46(1):1–42. doi: 10.1128/mr.46.1.1-42.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gray M. W., Lang B. F., Cedergren R., Golding G. B., Lemieux C., Sankoff D., Turmel M., Brossard N., Delage E., Littlejohn T. G. Genome structure and gene content in protist mitochondrial DNAs. Nucleic Acids Res. 1998 Feb 15;26(4):865–878. doi: 10.1093/nar/26.4.865. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gupta R. S., Aitken K., Falah M., Singh B. Cloning of Giardia lamblia heat shock protein HSP70 homologs: implications regarding origin of eukaryotic cells and of endoplasmic reticulum. Proc Natl Acad Sci U S A. 1994 Apr 12;91(8):2895–2899. doi: 10.1073/pnas.91.8.2895. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gupta R. S., Golding G. B. The origin of the eukaryotic cell. Trends Biochem Sci. 1996 May;21(5):166–171. [PubMed] [Google Scholar]
- Gupta R. S. Protein phylogenies and signature sequences: A reappraisal of evolutionary relationships among archaebacteria, eubacteria, and eukaryotes. Microbiol Mol Biol Rev. 1998 Dec;62(4):1435–1491. doi: 10.1128/mmbr.62.4.1435-1491.1998. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hall J. L., Ramanis Z., Luck D. J. Basal body/centriolar DNA: molecular genetic studies in Chlamydomonas. Cell. 1989 Oct 6;59(1):121–132. doi: 10.1016/0092-8674(89)90875-1. [DOI] [PubMed] [Google Scholar]
- Hashimoto T., Sánchez L. B., Shirakura T., Müller M., Hasegawa M. Secondary absence of mitochondria in Giardia lamblia and Trichomonas vaginalis revealed by valyl-tRNA synthetase phylogeny. Proc Natl Acad Sci U S A. 1998 Jun 9;95(12):6860–6865. doi: 10.1073/pnas.95.12.6860. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Heins L., Soll J. Chloroplast biogenesis: mixing the prokaryotic and the eukaryotic? Curr Biol. 1998 Mar 12;8(6):R215–R217. doi: 10.1016/s0960-9822(98)70129-0. [DOI] [PubMed] [Google Scholar]
- Henze K., Badr A., Wettern M., Cerff R., Martin W. A nuclear gene of eubacterial origin in Euglena gracilis reflects cryptic endosymbioses during protist evolution. Proc Natl Acad Sci U S A. 1995 Sep 26;92(20):9122–9126. doi: 10.1073/pnas.92.20.9122. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Horner D. S., Hirt R. P., Kilvington S., Lloyd D., Embley T. M. Molecular data suggest an early acquisition of the mitochondrion endosymbiont. Proc Biol Sci. 1996 Aug 22;263(1373):1053–1059. doi: 10.1098/rspb.1996.0155. [DOI] [PubMed] [Google Scholar]
- John P., Whatley F. R. Paracoccus denitrificans and the evolutionary origin of the mitochondrion. Nature. 1975 Apr 10;254(5500):495–498. doi: 10.1038/254495a0. [DOI] [PubMed] [Google Scholar]
- Johnson D. E., Dutcher S. K. Molecular studies of linkage group XIX of Chlamydomonas reinhardtii: evidence against a basal body location. J Cell Biol. 1991 Apr;113(2):339–346. doi: 10.1083/jcb.113.2.339. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Knoll A. H. Proterozoic and early Cambrian protists: evidence for accelerating evolutionary tempo. Proc Natl Acad Sci U S A. 1994 Jul 19;91(15):6743–6750. doi: 10.1073/pnas.91.15.6743. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Knoll A. H. The early evolution of eukaryotes: a geological perspective. Science. 1992 May 1;256(5057):622–627. doi: 10.1126/science.1585174. [DOI] [PubMed] [Google Scholar]
- Kobayashi M., Shoun H. The copper-containing dissimilatory nitrite reductase involved in the denitrifying system of the fungus Fusarium oxysporum. J Biol Chem. 1995 Feb 24;270(8):4146–4151. doi: 10.1074/jbc.270.8.4146. [DOI] [PubMed] [Google Scholar]
- Koga Y., Kyuragi T., Nishihara M., Sone N. Did archaeal and bacterial cells arise independently from noncellular precursors? A hypothesis stating that the advent of membrane phospholipid with enantiomeric glycerophosphate backbones caused the separation of the two lines of descent. J Mol Evol. 1998 Jan;46(1):54–63. doi: 10.1007/pl00006283. [DOI] [PubMed] [Google Scholar]
- Kunau W. H., Erdmann R. Peroxisome biogenesis: back to the endoplasmic reticulum? Curr Biol. 1998 Apr 23;8(9):R299–R302. doi: 10.1016/s0960-9822(98)70191-5. [DOI] [PubMed] [Google Scholar]
- Köhler S., Delwiche C. F., Denny P. W., Tilney L. G., Webster P., Wilson R. J., Palmer J. D., Roos D. S. A plastid of probable green algal origin in Apicomplexan parasites. Science. 1997 Mar 7;275(5305):1485–1489. doi: 10.1126/science.275.5305.1485. [DOI] [PubMed] [Google Scholar]
- Lake J. A., Rivera M. C. Was the nucleus the first endosymbiont? Proc Natl Acad Sci U S A. 1994 Apr 12;91(8):2880–2881. doi: 10.1073/pnas.91.8.2880. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lang B. F., Burger G., O'Kelly C. J., Cedergren R., Golding G. B., Lemieux C., Sankoff D., Turmel M., Gray M. W. An ancestral mitochondrial DNA resembling a eubacterial genome in miniature. Nature. 1997 May 29;387(6632):493–497. doi: 10.1038/387493a0. [DOI] [PubMed] [Google Scholar]
- Lindmark D. G., Müller M. Hydrogenosome, a cytoplasmic organelle of the anaerobic flagellate Tritrichomonas foetus, and its role in pyruvate metabolism. J Biol Chem. 1973 Nov 25;248(22):7724–7728. [PubMed] [Google Scholar]
- López-Garćia P., Moreira D. Metabolic symbiosis at the origin of eukaryotes. Trends Biochem Sci. 1999 Mar;24(3):88–93. doi: 10.1016/s0968-0004(98)01342-5. [DOI] [PubMed] [Google Scholar]
- Löwe J., Amos L. A. Crystal structure of the bacterial cell-division protein FtsZ. Nature. 1998 Jan 8;391(6663):203–206. doi: 10.1038/34472. [DOI] [PubMed] [Google Scholar]
- Maier U. G. The four genomes of the alga Pyrenomonas salina (Cryptophyta). Biosystems. 1992;28(1-3):69–73. doi: 10.1016/0303-2647(92)90009-n. [DOI] [PubMed] [Google Scholar]
- Margulis L. Archaeal-eubacterial mergers in the origin of Eukarya: phylogenetic classification of life. Proc Natl Acad Sci U S A. 1996 Feb 6;93(3):1071–1076. doi: 10.1073/pnas.93.3.1071. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Martin W., Müller M. The hydrogen hypothesis for the first eukaryote. Nature. 1998 Mar 5;392(6671):37–41. doi: 10.1038/32096. [DOI] [PubMed] [Google Scholar]
- Martin W., Stoebe B., Goremykin V., Hapsmann S., Hasegawa M., Kowallik K. V. Gene transfer to the nucleus and the evolution of chloroplasts. Nature. 1998 May 14;393(6681):162–165. doi: 10.1038/30234. [DOI] [PubMed] [Google Scholar]
- Martin W, Herrmann RG. Gene transfer from organelles to the nucleus: how much, what happens, and Why? . Plant Physiol. 1998 Sep;118(1):9–17. doi: 10.1104/pp.118.1.9. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Mayr E. Two empires or three? Proc Natl Acad Sci U S A. 1998 Aug 18;95(17):9720–9723. doi: 10.1073/pnas.95.17.9720. [DOI] [PMC free article] [PubMed] [Google Scholar]
- McFadden G. I., Gilson P. R., Douglas S. E., Cavalier-Smith T., Hofmann C. J., Maier U. G. Bonsai genomics: sequencing the smallest eukaryotic genomes. Trends Genet. 1997 Feb;13(2):46–49. doi: 10.1016/s0168-9525(97)01010-x. [DOI] [PubMed] [Google Scholar]
- McFadden G. I., Reith M. E., Munholland J., Lang-Unnasch N. Plastid in human parasites. Nature. 1996 Jun 6;381(6582):482–482. doi: 10.1038/381482a0. [DOI] [PubMed] [Google Scholar]
- McFadden G. I., Waller R. F. Plastids in parasites of humans. Bioessays. 1997 Nov;19(11):1033–1040. doi: 10.1002/bies.950191114. [DOI] [PubMed] [Google Scholar]
- Moreira D, Lopez-Garcia P. Symbiosis between methanogenic archaea and delta-proteobacteria as the origin of eukaryotes: the syntrophic hypothesis . J Mol Evol. 1998 Nov;47(5):517–530. doi: 10.1007/pl00006408. [DOI] [PubMed] [Google Scholar]
- Müller M. Energy metabolism of protozoa without mitochondria. Annu Rev Microbiol. 1988;42:465–488. doi: 10.1146/annurev.mi.42.100188.002341. [DOI] [PubMed] [Google Scholar]
- Müller M., Martin W. The genome of Rickettsia prowazekii and some thoughts on the origin of mitochondria and hydrogenosomes. Bioessays. 1999 May;21(5):377–381. doi: 10.1002/(SICI)1521-1878(199905)21:5<377::AID-BIES4>3.0.CO;2-W. [DOI] [PubMed] [Google Scholar]
- Müller M. The hydrogenosome. J Gen Microbiol. 1993 Dec;139(12):2879–2889. doi: 10.1099/00221287-139-12-2879. [DOI] [PubMed] [Google Scholar]
- Olsen L. J. The surprising complexity of peroxisome biogenesis. Plant Mol Biol. 1998 Sep;38(1-2):163–189. [PubMed] [Google Scholar]
- Raff R. A., Mahler H. R. The non symbiotic origin of mitochondria. Science. 1972 Aug 18;177(4049):575–582. doi: 10.1126/science.177.4049.575. [DOI] [PubMed] [Google Scholar]
- Raven P. H. A multiple origin for plastids and mitochondria. Science. 1970 Aug 14;169(3946):641–646. doi: 10.1126/science.169.3946.641. [DOI] [PubMed] [Google Scholar]
- Roger A. J., Svärd S. G., Tovar J., Clark C. G., Smith M. W., Gillin F. D., Sogin M. L. A mitochondrial-like chaperonin 60 gene in Giardia lamblia: evidence that diplomonads once harbored an endosymbiont related to the progenitor of mitochondria. Proc Natl Acad Sci U S A. 1998 Jan 6;95(1):229–234. doi: 10.1073/pnas.95.1.229. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sagan L. On the origin of mitosing cells. J Theor Biol. 1967 Mar;14(3):255–274. doi: 10.1016/0022-5193(67)90079-3. [DOI] [PubMed] [Google Scholar]
- Sandman K., Pereira S. L., Reeve J. N. Diversity of prokaryotic chromosomal proteins and the origin of the nucleosome. Cell Mol Life Sci. 1998 Dec;54(12):1350–1364. doi: 10.1007/s000180050259. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sandman K., Reeve J. N. Origin of the eukaryotic nucleus. Science. 1998 Apr 24;280(5363):501–503. doi: 10.1126/science.280.5363.499d. [DOI] [PubMed] [Google Scholar]
- Schatz G., Dobberstein B. Common principles of protein translocation across membranes. Science. 1996 Mar 15;271(5255):1519–1526. doi: 10.1126/science.271.5255.1519. [DOI] [PubMed] [Google Scholar]
- Schubert I. Eukaryotic nuclei of endosymbiontic origin? Naturwissenschaften. 1988 Feb;75(2):89–91. doi: 10.1007/BF00368411. [DOI] [PubMed] [Google Scholar]
- Sogin M. L., Gunderson J. H., Elwood H. J., Alonso R. A., Peattie D. A. Phylogenetic meaning of the kingdom concept: an unusual ribosomal RNA from Giardia lamblia. Science. 1989 Jan 6;243(4887):75–77. doi: 10.1126/science.2911720. [DOI] [PubMed] [Google Scholar]
- Tielens A. G., Van Hellemond J. J. The electron transport chain in anaerobically functioning eukaryotes. Biochim Biophys Acta. 1998 Jun 10;1365(1-2):71–78. doi: 10.1016/s0005-2728(98)00045-0. [DOI] [PubMed] [Google Scholar]
- Titorenko V. I., Rachubinski R. A. The endoplasmic reticulum plays an essential role in peroxisome biogenesis. Trends Biochem Sci. 1998 Jul;23(7):231–233. doi: 10.1016/s0968-0004(98)01226-2. [DOI] [PubMed] [Google Scholar]
- Unseld M., Marienfeld J. R., Brandt P., Brennicke A. The mitochondrial genome of Arabidopsis thaliana contains 57 genes in 366,924 nucleotides. Nat Genet. 1997 Jan;15(1):57–61. doi: 10.1038/ng0197-57. [DOI] [PubMed] [Google Scholar]
- Uzzell T., Spolsky C. Mitochondria and plastids as endosymbionts: a revival of special creation? Am Sci. 1974 May-Jun;62(3):334–343. [PubMed] [Google Scholar]
- Van Hellemond J. J., Opperdoes F. R., Tielens A. G. Trypanosomatidae produce acetate via a mitochondrial acetate:succinate CoA transferase. Proc Natl Acad Sci U S A. 1998 Mar 17;95(6):3036–3041. doi: 10.1073/pnas.95.6.3036. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Vellai T., Takács K., Vida G. A new aspect to the origin and evolution of eukaryotes. J Mol Evol. 1998 May;46(5):499–507. doi: 10.1007/pl00006331. [DOI] [PubMed] [Google Scholar]
- Vicente M., Errington J. Structure, function and controls in microbial division. Mol Microbiol. 1996 Apr;20(1):1–7. doi: 10.1111/j.1365-2958.1996.tb02482.x. [DOI] [PubMed] [Google Scholar]
- Vinella D., D'Ari R. Overview of controls in the Escherichia coli cell cycle. Bioessays. 1995 Jun;17(6):527–536. doi: 10.1002/bies.950170609. [DOI] [PubMed] [Google Scholar]
- Vossbrinck C. R., Maddox J. V., Friedman S., Debrunner-Vossbrinck B. A., Woese C. R. Ribosomal RNA sequence suggests microsporidia are extremely ancient eukaryotes. 1987 Mar 26-Apr 1Nature. 326(6111):411–414. doi: 10.1038/326411a0. [DOI] [PubMed] [Google Scholar]
- Waller R. F., Keeling P. J., Donald R. G., Striepen B., Handman E., Lang-Unnasch N., Cowman A. F., Besra G. S., Roos D. S., McFadden G. I. Nuclear-encoded proteins target to the plastid in Toxoplasma gondii and Plasmodium falciparum. Proc Natl Acad Sci U S A. 1998 Oct 13;95(21):12352–12357. doi: 10.1073/pnas.95.21.12352. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Weeden N. F. Genetic and biochemical implications of the endosymbiotic origin of the chloroplast. J Mol Evol. 1981;17(3):133–139. doi: 10.1007/BF01733906. [DOI] [PubMed] [Google Scholar]
- Whatley J. M., John P., Whatley F. R. From extracellular to intracellular: the establishment of mitochondria and chloroplasts. Proc R Soc Lond B Biol Sci. 1979 Apr 11;204(1155):165–187. doi: 10.1098/rspb.1979.0020. [DOI] [PubMed] [Google Scholar]
- Yeliseev A. A., Krueger K. E., Kaplan S. A mammalian mitochondrial drug receptor functions as a bacterial "oxygen" sensor. Proc Natl Acad Sci U S A. 1997 May 13;94(10):5101–5106. doi: 10.1073/pnas.94.10.5101. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Zellner G., Stackebrandt E., Messner P., Tindall B. J., Conway de Macario E., Kneifel H., Sleytr U. B., Winter J. Methanocorpusculaceae fam. nov., represented by Methanocorpusculum parvum, Methanocorpusculum sinense spec. nov. and Methanocorpusculum bavaricum spec. nov. Arch Microbiol. 1989;151(5):381–390. doi: 10.1007/BF00416595. [DOI] [PubMed] [Google Scholar]
