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Mitochondrial clock: moderating evolution of early eukaryotes in light of the Proterozoic oceans

  • Shamik Dasgupta EMAIL logo
Published/Copyright: September 14, 2016
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Abstract

Evolution of early eukaryotes in the primitive Earth relied heavily on the origin and evolution of mitochondria. Understanding the structure and origin of mitochondria has a germane relation to understanding origin and evolution of eukaryotes. In light of the extreme conditions and the then existing Proterozoic ocean chemistry, eukaryotic cells developed adaptive adjustments for energy management. Apart from mitochondria, more reduced homologues like hydrogenosomes and mitosomes facilitated the metabolic activities of such eukaryotic life. In this short review, I highlight the importance of mitochondria in pushing eukaryotes to the peak of the evolutionary pyramid. Our knowledge has expanded but studying recent eukaryotic extremophiles and mitochondrial genomics in more details will enable us to estimate the position of the mitochondrial clock, understand its role better, and possibly find new eukaryotic lineages.

Acknowledgements

I sincerely thank Dr. Jiasong Fang for his critics and suggestions. My regards go to Prof. Xiaotong Peng for giving me enough chance and time to complete this review. I thank my colleagues and friends in Tongji University and Institute of Deep-Sea Science and Engineering, CAS, for their valuable advice during preparation. I also take this chance to acknowledge the brilliant scientists who have dedicatedly worked in understanding this research field; at the same time my apologies for missing out names of many such scholars in my review.

References

Adl S.M., Simpson A.G., Farmer M.A., Andersen R.A., Anderson O.R., Barta J.R., Bowser S.S., Brugerolle G., Fensome R.A., Fredericq S., James T.Y., Karpov S., Kugrens P., Krug J., Lane C.E., Lewis L.A., Lodge J., Lynn D.H., Mann D.G., McCourt R.M., Mendoza L., Moestrup O., Mozley-Standridge S.E., Nerad T.A., Shearer C.A., Smirnov A.V., Spiegel F.W. & Taylor M.F. 2005. The new higher level classification of eukaryotes with emphasis on the taxonomy of protists. J Eukaryot. Microbiol. 52: 399–451.10.1111/j.1550-7408.2005.00053.xSearch in Google Scholar

Adl S.M., Simpson A.G., Lane C.E., Lukes J., Bass D., Bowser S.S., Brown M.W., Burki F., Dunthorn M., Hampl V., Heiss A., Hoppenrath M., Lara E., Le Gall L., Lynn D.H., Mc-Manus H., Mitchell E.A., Mozley-Stanridge S.E., Parfrey L.W., Pawlowski J., Rueckert S., Shadwick R.S., Schoch C.L., Smirnov A. & Spiegel F.W. 2012. The revised classification of eukaryotes. J. Eukaryot. Microbiol. 59: 429–493.10.1111/j.1550-7408.2012.00644.xSearch in Google Scholar

Andersson S.G.E. & Kurland C.G. 1999. Origins of mitochondria and hydrogenosomes. Curr. Opin. Microbiol. 2: 535–541.10.1016/S1369-5274(99)00013-2Search in Google Scholar

Boxma B., de Graaf R.R., van der Staay G.W.M., van Alen T.A., Ricard G., Gabaldón T., van Hoek A.H.A.M., van der Staay S.Y.M., Koopman W.J.H., Hellemond J.J., Tielens A.G.M., Friedrich T., Veenhuis M., Huynen M.A. & Hackstein J.H.P. 2005. An anaerobic mitochondrion that produces hydrogen. Nature 434: 74–79.10.1038/nature03343Search in Google Scholar PubMed

Boxma B., Voncken F., Jannink S., van Alen T., Akhmanova A., van Weelden S.W., Hellemond J.J., Ricard G., Huynen M., Tielens A.G. & Hackstein J.H. 2004. The anaerobic chytridiomycete fungus Piromyces sp E2 produces ethanol via pyruvate:formate lyase and an alcohol dehydrogenase E. Mol. Microbiol. 51: 1389–1399.10.1046/j.1365-2958.2003.03912.xSearch in Google Scholar PubMed

Buetow D.E. 1989. The mitochondrion, pp. 247–314. In: Buetow D.E. (ed.), The Biology of Euglena. Subcellular Biochemistry and Molecular Biology, 4, Academic Press, San Diego.10.1016/B978-0-12-139904-7.50009-9Search in Google Scholar

Bui E.T.N., Bradley P.J. & Johnson P.J. 1996. A common evolutionary origin for mitochondria and hydrogenosomes. Proc. Natl. Acad. Sci. USA 93: 9651–9656.10.1073/pnas.93.18.9651Search in Google Scholar PubMed PubMed Central

Canfield D.E. 2005. The early history of atmospheric oxygen: homage to Robert M. Garrels. Annu. Rev. Earth Planet. Sci. 33: 1–36.10.1146/annurev.earth.33.092203.122711Search in Google Scholar

Canfield D.E., Poulton S.W. & Narbonne G.M. 2007. Late Neoproterozoic deep-ocean oxygenation and the rise of animal life. Science 315: 92–95.10.1126/science.1135013Search in Google Scholar PubMed

Dasgupta S., Fang J., Brake S.S., Hasiotis S.T. & Zhang L. 2012. Biosynthesis of sterols and wax esters by Euglena of acid mine drainage biofilms: implications for eukaryotic evolution and the early Earth. Chem. Geol. 306-307: 139–145.10.1016/j.chemgeo.2012.03.003Search in Google Scholar

Dietrich L.E.P., Tice M.M. & Newman D.K. 2006. The coevolution of life and Earth. Curr. Biol. 16: 395–400.10.1016/j.cub.2006.05.017Search in Google Scholar

Dubilier N., Windoffer R., Grieshaber M.K. & Giere O. 1997. Ultrastructure and anaerobic metabolism of mitochondria in the marine oligochaete Tubificoides benedii: effects of hypoxia and sulfide. Mar. Biol. 127: 637–645.10.1007/s002270050054Search in Google Scholar

Embley T.M. & Hirt R.P. 1998. Early branching eukaryotes? Curr. Opin. Genet. Dev. 8: 655–661.10.1016/S0959-437X(98)80029-4Search in Google Scholar

Embley T.M., van der Giezen M., Horner D.S., Dyal P.L., Bell S. & Foster P.G. 2003. Hydrogenosomes, mitochondria and early eukaryotic evolution. IUBMB Life 55: 387–395.10.1080/15216540310001592834Search in Google Scholar PubMed

Fenchel T. & Finlay B.J. 1995. Ecology and Evolution in Anoxic Worlds. Oxford University Press, Oxford, United Kingdom, 288 pp.Search in Google Scholar

Gabaldón T. & Pittis A.A. 2015. Origin and evolution of metabolic sub-cellular compartmentalization in eukaryotes. Biochimie 119: 262–268.10.1016/j.biochi.2015.03.021Search in Google Scholar PubMed PubMed Central

Goldberg A.V., Molik S., Tsaousis A.D., Neumann K., Kuhnke G., Delbac F., Vivares C.P., Hirt R.P., Lill R. & Embley T. M. 2008. Localization and functionality of microsporidian iron-sulphur cluster assembly proteins. Nature 452: 624–628.10.1038/nature06606Search in Google Scholar PubMed

Goosen N.K., Wagener S. & Stumm C.K. 1990. A comparison of two strains of the anaerobic ciliate Trimyema compressum. Arch. Microbiol. 153: 187–192.10.1007/BF00247819Search in Google Scholar

Gray M.W. 2012. Mitochondrial evolution. Cold Spring Harb. Perspect. Biol. 4: :a011403.10.1007/978-94-011-0163-9_20Search in Google Scholar

Gray M.W., Burger G. & Lang B.F. 2001. The origin and early evolution of mitochondria. Genome Biol. 2: 1018.1–1018.5.10.1186/gb-2001-2-6-reviews1018Search in Google Scholar PubMed PubMed Central

Hampl V., Silberman J.D., Stechmann A., Diaz-Trivino S., Johnson P.J. & Roger A.J. 2008. Genetic evidence for a mitochondriate ancestry in the ‘amitochondriate’ flagellate Trimastix pyriformis. PLoS One 3: e1383.10.1371/journal.pone.0001383Search in Google Scholar PubMed PubMed Central

Han T.M. & Runnegar B. 1992. Megascopic eukaryotic algae from the 2.1-billion-year-old Negaunee iron-formation, Michigan. Science 257: 232–235.10.1126/science.1631544Search in Google Scholar

He D., Fiz-Palacios O., Fu C.J., Fehling J., Tsai C.C. & Baldauf S.L. 2014. An alternative root for the eukaryotic tree of life. Curr. Biol. 24: 465–470.10.1016/j.cub.2014.01.036Search in Google Scholar

Hellemond J.J., Hoek A., Schreur P.W., Chupin V., Özdirekcan S., Geysen D., van Grinsven K.W.A., Koets A.P., Van den Bossche P., Geerts S. & Tielens A.G.M. 2007. Energy metabolism of bloodstream form Trypanosoma theileri. Eukaryot. Cell 6: 1693–1696.10.1128/EC.00130-07Search in Google Scholar

Hellemond J.J., Luijten M., Flesch F.M., Gaasenbeek C.P.H. & Tielens A.G.M. 1996. Rhodoquinone is synthesized de novo by Fasciola hepatica. Mol. Biochem. Parasitol. 82: 217–226.10.1016/0166-6851(96)02738-7Search in Google Scholar

Hellemond J.J. & Tielens A.G.M. 1997. Inhibition of the respiratory chain results in a reversible metabolic arrest in Leishmania promastigotes. Mol. Biochem. Parasitol. 85: 135–138.10.1016/S0166-6851(97)02828-4Search in Google Scholar

Hildebrandt T.M. & Grieshaber M.K. 2008. Redox regulation of mitochondrial sulfide oxidation in the lugworm, Arenicola marina. J. Exp. Biol. 211: 2617–2623.10.1242/jeb.019729Search in Google Scholar

Hoffmeister M., Piotrowski M., Nowitzki U. & Martin W. 2004. Mitochondrial trans-2-enoyl-CoA reductase of wax ester fermentation from Euglena gracilis defines a new family of enzymes involved in lipid synthesis. J. Biol. Chem. 280: 4329–4338.10.1074/jbc.M411010200Search in Google Scholar

Hrdy I. & Müller M. 1995a. Primary structure and eubacterial relationships of the pyruvate:ferredoxin oxidoreductase of the amitochondriate eukaryote, Trichomonas vaginalis. J. Mol. Evol. 41: 388–396.10.1007/BF00186551Search in Google Scholar

Hrdy I. & Müller M. 1995b. Primary structure of the hydrogenosomal malic enzyme of Trichomonas vaginalis and its relationship to homologous enzymes. J. Eukaryot. Microbiol. 42: 593–603.10.1111/j.1550-7408.1995.tb05913.xSearch in Google Scholar

Inui H., Miyatake K., Nakano Y. & Kitaoka S. 1982. Wax ester fermentation in Euglena gracilis. FEBS Lett. 150: 89–93.10.1016/0014-5793(82)81310-0Search in Google Scholar

Inui H., Miyatake K., Nakano Y. & Kitaoka S. 1983. Production and composition of wax ester by fermentation of Euglena gracilis. Agric. Biol. Chem. 47: 2669–2671.10.1271/bbb1961.47.2669Search in Google Scholar

Javaux E.J., Knoll A.H. & Walter M.R. 2004. TEM evidence for eukaryotic diversity in mid-Proterozoic oceans. Geobiology 2: 121–132.10.1111/j.1472-4677.2004.00027.xSearch in Google Scholar

Klein B., Grossi V., Bouriat P., Goulas P. & Grimaud R. 2008. Cytoplasmic wax ester accumulation during biofilm-driven substrate assimilation at the alkane-water interface by Marinobacter hydrocarbonoclasticus SP17. Res. Microbiol. 159: 137–144.10.1016/j.resmic.2007.11.013Search in Google Scholar

Koonin E.V. 2010. The origin and early evolution of eukaryotes in the light of phylogenomics. Genome Biol. 11: 209.10.1186/gb-2010-11-5-209Search in Google Scholar

Krauss S. 2001. Mitochondria: Structure and Role in Respiration. Nature Encyclopedia of Life Sciences, Nature Publishing Group.10.1038/npg.els.0001380Search in Google Scholar

Lane N. & Martin W. 2010. The energetic of genome complexity. Nature 467: 594–601.10.1038/nature09486Search in Google Scholar

Lill R., Hoffmann B., Molik S., Pierik A.J., Rietzschel N., Stehling O., Uzarska M.A., Webert H., Wilbrecht C. & Mühlenhoff U. 2012. The role of mitochondria in cellular ironsulfur protein biogenesis and iron metabolism. Biochim. Biophys. Acta 1823: 1491–1508.10.1016/j.bbamcr.2012.05.009Search in Google Scholar

Lill R. & Mühlenhoff U. 2008. Maturation of iron-sulfur proteins in eukaryotes: mechanisms, connected processes, and diseases. Annu. Rev. Biochem 77: 669–700.10.1146/annurev.biochem.76.052705.162653Search in Google Scholar

Lindmark D.G. & Müller M. 1973. Hydrogenosome, a cytoplasmic organelle of the anaerobic flagellate, Tritrichomonas foetus and its role in pyruvate metabolism. J. Biol. Chem. 248: 7724–7728.10.1016/S0021-9258(19)43249-3Search in Google Scholar

Lopez-Garcia P. & Moreira D. 1999. Metabolic symbiosis at the origin of eukaryotes. Trends Biochem. Sci. 24: 88–93.10.1016/S0968-0004(98)01342-5Search in Google Scholar

Maguire F. & Richards T.A. 2014. Organelle evolution: a mosaic of ‘mitochondrial’ functions. Curr. Biol. Dispatches 24: R518–R520.10.1016/j.cub.2014.03.075Search in Google Scholar

Mai Z.M., Ghosh S., Frisardi M., Rosenthal B., Rogers R. & Samuelson J. 1999. Hsp60 is targeted to a cryptic mitochondrion derived organelle (“crypton”) in the microaerophilic protozoan parasite Entamoeba histolytica. Mol. Cell Biol. 19: 2198–2205.10.1128/MCB.19.3.2198Search in Google Scholar

Martin W. & Mentel M. 2010. The Origin of Mitochondria. Nature Education 3: 58.Search in Google Scholar

Martin W. & Müller M. 1998. The hydrogen hypothesis for the first eukaryote. Nature 392: 37–41.10.1038/32096Search in Google Scholar

Martin W. & Müuller M. 2007. Origin of Mitochondria and Hydrogenosomes. Springer-Verlag, Berlin, Germany, 306 pp.10.1007/978-3-540-38502-8Search in Google Scholar

Mentel M. & Martin W. 2008. Energy metabolism among eukaryotic anaerobes in light of Proterozoic ocean chemistry. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 363: 2717–2729.10.1098/rstb.2008.0031Search in Google Scholar

Mountfort D.O. & Orpin C.G. 1994. Anaerobic Fungi: Biology, Ecology and Function. Marcel Dekker Inc, New York, U.S.A., 304 pp.Search in Google Scholar

Müller M. 1993. The hydrogenosome. J. Gen. Microbiol. 139: 2879–2889.10.1099/00221287-139-12-2879Search in Google Scholar

Müller M. 2003. Energy metabolism. Part I. Anaerobic protozoa, pp. 125–139. In: Marr J.J., Nilsen T.W. & Komuniecki R.W. (eds), Molecular Medical Parasitology. Academic Press, London, United Kingdom,Search in Google Scholar

Müller M., Mentel M., Hellemond J.J., Henze K., Woehle C., Gould S.B., Yu R.Y., van der Giezen M., Tielens A.G.M. & Martin W.F. 2012. Biochemistry and evolution of anaerobic energy metabolism in eukaryotes. Microbiol. Mol. Biol. Rew. 76: 444–495.10.1128/MMBR.05024-11Search in Google Scholar

Nagai J., Otha T. & Saito E. 1971. Incorporation of propionate into wax esters by etiolated Euglena. Biochem. Biophys. Res. Commun. 42: 523–529.10.1016/0006-291X(71)90402-5Search in Google Scholar

Nakazawa M., Takenaka S., Ueda M., Inui H., Nakano Y. & Miyatake K. 2003. Pyruvate:NADP+ oxidoreductase is stabilized by its cofactor, thiamin pyrophosphate, in mitochondria of Euglena gracilis. Arch. Biochem. Biophys. 411: 183–188.10.1016/S0003-9861(02)00749-XSearch in Google Scholar

Perez E., Lapaille M., Degand H., Cilibrasi L., Villavicencio-Queijeiro A., Morsomme P., González-Halphene D., Field M.C., Remacle C., Baurain D. & Cardol P. 2014. The mitochondrial respiratory chain of the secondary green alga Euglena gracilis shares many additional subunits with parasitic Trypanosomatidae. Mitochondrion 19: 338–349.10.1016/j.mito.2014.02.001Search in Google Scholar PubMed

Reeves R.E. 1984. Metabolism of Entamoeba histolytica Schaudinn, 1903. Adv. Parasitol. 23: 105–142.10.1016/S0065-308X(08)60286-9Search in Google Scholar

Reeves R.E., Warren L.G., Susskind B. & Lo H.S. 1977. An energy-conserving pyruvate-to-acetate pathway in Entamoeba histolytica. Pyruvate synthase and a new acetate thiokinase. J. Biol. Chem. 252: 726–731.10.1016/S0021-9258(17)32778-3Search in Google Scholar

Roger A.J., Clark C.G. & Doolittle W.F. 1996. A possible mitochondrial gene in the early-branching amitochondriate protist Trichomonas vaginalis. Proc. Natl. Acad. Sci. USA 93: 14618–14622.10.1073/pnas.93.25.14618Search in Google Scholar

Samuelsson J. & Butterfield N. 2001. Neoproterozoic fossils from the Franklin Mountains, northwestern Canada: stratigraphic and palaeobiological implications. Precambrian Res. 107: 235–251.10.1016/S0301-9268(00)00142-XSearch in Google Scholar

Schatz G. 2013. Getting mitochondria to the center stage. Biochem. Biophys. Res. Commun. 434: 407–410.10.1016/j.bbrc.2013.03.081Search in Google Scholar

Schneider R.E., Brown M.T., Shiflett A.M., Dyall S.D., Hayes R.D., Xie Y., Loo J.A. & Johnson P.J. 2011. The Trichomonas vaginalis hydrogenosome proteome is highly reduced relative to mitochondria, yet complex compared with mitosomes. Int. J. Parasitol. 41: 1421–1434.10.1016/j.ijpara.2011.10.001Search in Google Scholar

Shiflett A.M. & Johnson P.J. 2010. Mitochondrion-related organelles in eukaryotic protists. Annu. Rev. Microbiol. 64: 409–429.10.1146/annurev.micro.62.081307.162826Search in Google Scholar

Sousa F.L., Neukirchen S., Allen J.F., Lane N. & Martin W.F. 2016. Lokiarchaeon is hydrogen dependent. Nat. Microbiol. 34: 1–3.10.1038/nmicrobiol.2016.34Search in Google Scholar

Spang A., Saw J.H., Jřrgensen S.L., Zaremba-Niedzwiedzka K., Martjin J., Lind A.E., van Eijk R., Schleper C., Guy L. & Ettema T.J.G. 2015. Complex archaea that bridge the gap between prokaryotes and eukaryotes. Nature 521: 173–179.10.1038/nature14447Search in Google Scholar

Steinbüchel A. & Müller M. 1986. Anaerobic pyruvate metabolism of Tritrichomonas foetus and Trichomonas vaginalis hydrogenosomes. Mol. Biochem. Parasitol. 20: 57–65.10.1016/0166-6851(86)90142-8Search in Google Scholar

Tachezy J. 2008. Hydrogenosomes and Mitosomes: Mitochondria of Anaerobic Eukaryotes. Springer-Verlag, Heidelberg, Germany, 287 pp.10.1007/978-3-540-76733-6Search in Google Scholar

Theissen U., Hoffmeister M., Grieshaber M. & Martin W. 2003. Single eubacterial origin of eukaryotic sulfide:quinone oxidoreductase, a mitochondrial enzyme conserved from the early evolution of eukaryotes during anoxic and sulfidic times. Mol. Biol. Evol. 20: 1564–1574.10.1093/molbev/msg174Search in Google Scholar PubMed

Tielens A.G.M. & Hellemond J.J. 2009. Surprising variety in energy metabolism within Trypanosomatidae. Trends Parasitol. 25: 482–490.10.1016/j.pt.2009.07.007Search in Google Scholar PubMed

Timmis J.N., Ayliffe M.A., Huang C.Y. & Martin W. 2004. Endosymbiotic gene transfer: organelle genomes forge eukaryotic chromosomes. Nat. Rev. Genet. 5: 123–135.10.1038/nrg1271Search in Google Scholar PubMed

Tovar J. 2007. Mitosomes of parasitic protozoa: biology and evolutionary significance, pp. 277–280. In: Martin W.F. & Müller M. (eds), Origin of Mitochondria and Hydrogenosomes. Springer Berlin Heidelberg, Germany.10.1007/978-3-540-38502-8_11Search in Google Scholar

Tovar J., Fischer A. & Clark C.G. 1999. The mitosome, a novel organelle related to mitochondria in the amitochondrial parasite Entamoeba histolytica. Mol. Microbiol. 32: 1013–1021.10.1046/j.1365-2958.1999.01414.xSearch in Google Scholar PubMed

Tovar J., León-Avila G., Sánchez L.B., Sutak R., Tachezy J., van der Giezen M., Hernández M., Müller M. & Lucocq J.M. 2003. Mitochondrial remnant organelles of Giardia function in iron-sulphur protein maturation. Nature 426: 172–176.10.1038/nature01945Search in Google Scholar PubMed

Tucci S., Proksch P. & Martin W. 2006. Fatty acid biosynthesis in mitochondria of Euglena gracilis, pp. 133–136. In: Benning C. & Ohlrogge J. (eds), Advances in Plant Lipid Research: Proceedings of the 17th International Symposium on Plant Lipids. East Lansing, Michigan, Michigan State University Press.Search in Google Scholar

van Grinsven K.W.A., Hellemond J.J. & Tielens A.G.M. 2009. Acetate:succinate CoA-transferase in the anaerobic mitochondria of Fasciola hepatica. Mol. Biochem. Parasitol. 164: 74–79.10.1016/j.molbiopara.2008.11.008Search in Google Scholar PubMed

Walker G., Dorrell R.G., Schlacht A. & Dacks J.B. 2011. Eukaryotic systematics: a user’s guide for cell biologists and parasitologists. J. Parasitol. 138: 1638–1663.10.1017/S0031182010001708Search in Google Scholar PubMed

Whatley J.M., John P. & Whatley F.R. 1979. From extracellular to intracellular: the establishment of mitochondria and chloroplasts. Proc. R. Soc. Lond. B 204: 165–187.10.1098/rspb.1979.0020Search in Google Scholar PubMed

Williams B.A., Hirt R.P., Lucocq J.M. & Embley T.M. 2002. A mitochondrial remnant in the microsporidian Trachipleistophora hominis. Nature 418: 865–869.10.1038/nature00949Search in Google Scholar PubMed

Williams T.A. 2014. Evolution: rooting the eukaryotic tree of life. Curr. Biol. Dispatches 24: R151–R152.10.1016/j.cub.2014.01.026Search in Google Scholar PubMed

Received: 2016-3-25
Accepted: 2016-8-15
Published Online: 2016-9-14
Published in Print: 2016-8-1

©2016 Institute of Molecular Biology, Slovak Academy of Sciences

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