Anaerobik Funguslarda Hidrojenozomlar: Hidrojen Üreten Organeller
Year 2021,
Volume: 12 Issue: 2, 190 - 208, 31.10.2021
Ferit Can Yazdıç
,
Fadime Yazdıç
,
Bülent Kar
,
Prof. Dr. Emin Özköse
,
Mehmet Sait Ekinci
Abstract
Funguslar ökaryotlar içerisinde birçok farklı grubu oluştururlar. Çoğu fungus mitokondri içerir ve oksidatif fosforilasyon yapabilir. Diğer taraftan herbivor memelilerin sindirim sistemindeki Neocallimastigomycota fungusları mitokondri yerine hidrojenozom olarak bilinen bir organel bulundururlar. Anaerobik çevreye uyumun anahtarı olma özelliğine sahip bu organel eşsizdir. Bu derlemede, bu önemli organellerin işlevi, yapısı, biyokimyası, genetik özellikleri ve kalıtımı hakkında bilinenleri kısaca özetlemek istiyoruz.
References
- Akhmanova, A., Voncken, F. G., Hosea, K. M., Harhangi, H., Keltjens, J. T., Op Den Camp, H. J., ... ve Hackstein, J. H. (1999). A hydrogenosome with pyruvate formate‐lyase: Anaerobic chytrid fungi use an alternative route for pyruvate catabolism. Mol. Microbiol., 32(5) 1103-1114.
- Benchimol M. (2007). Structure of the Hydrogenosomes (in this volume). Springer, Heidelberg.
- Benchimol, M., (2000). Ultrastructural characterization of the isolated hydrogenosome in Tritrichomonas foetus. Tissue Cell, 32 1–9.
- Benchimol, M., Almeida, J.C.A., ve de Souza, W. (1996). Further studies on the organization of the hydrogenosome of Tritrichomonas foetus. Tissue Cell, 28 287-299.
- Benchimol, M., Leal, D., Mattos, A., ve Diniz, J.A.P. (1997). Fine structure of Trichomonas gallinae. Biocell, 21 47-58.
- Benchimol, M., ve De Souza, W. (1983). Fine Structure and Cytochemistry of the Hydrogenosome of Tritrichomonas foetus 1. J. Protozool, 30(2) 422-425.
- Boxma, B., de Graaf, R. M., van der Staay, G. W., van Alen, T. A., Ricard, G., Gabaldón, T., ... ve Hackstein, J. H. (2005). An anaerobic mitochondrion that produces hydrogen. Nature, 434(7029) 74-79.
- Boxma, B., Voncken, F., Jannink, S., Van Alen, T., Akhmanova, A., Van Weelden, S. W., ... ve 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(5) 1389-1399.
- Cavalier-Smith, T. (1983). A 6-kingdom classification and a unified phylogeny. Intracellular space as oligogenetic ecosystem, 1027-1034.
- Dacks, J. B., Dyal, P. L., Embley, T. M., ve van der Giezen, M. (2006). Hydrogenosomal succinyl-CoA synthetase from the rumen-dwelling fungus Neocallimastix patriciarum; an energy-producing enzyme of mitochondrial origin. Gene, 373 75-82.
- Durand, R., Fischer, M., Rascle, C., ve Fevre, M. (1995). Neocallimastix frontalis enolase gene, enol: first report of an intron in an anaerobic fungus. Microbiology, 141(6) 1301-1308.
- Dyall, S. D., Koehler, C. M., Delgadillo-Correa, M. G., Bradley, P. J., Plümper, E., Leuenberger, D., ... ve Johnson, P. J. (2000). Presence of a member of the mitochondrial carrier family in hydrogenosomes: conservation of membrane-targeting pathways between hydrogenosomes and mitochondria. Mol. Cell. Biol., 20(7) 2488-2497.
- Dyall, S. D., Yan, W., Delgadillo-Correa, M. G., Lunceford, A., Loo, J. A., Clarke, C. F., ve Johnson, P. J. (2004). Non-mitochondrial complex I proteins in a hydrogenosomal oxidoreductase complex. Nature, 431(7012) 1103-1107.
- Embley, M., der Giezen, M. V., Horner, D. S., Dyal, P. L., ve Foster, P. (2003). Mitochondria and hydrogenosomes are two forms of the same fundamental organelle. Philos. Trans. R. Soc. Lond. B Biol. Sci., 358(1429) 191-203.
- Field, J., Rosenthal, B., ve Samuelson, J. (2000). Early lateral transfer of genes encoding malic enzyme, acetyl‐CoA synthetase and alcohol dehydrogenases from anaerobic prokaryotes to Entamoeba histolytica. Mol. Microbiol., 38(3) 446-455.
- Finlay, B.J. ve Fenchel, T. (1989). Hydrogenosomes in some anaerobic protozoa resemble mitochondria. FEMS Microbiol. Lett., 65 311-314.
- Fliegerova, K. O., Podmirseg, S. M., Vinzelj, J., Grilli, D. J., Kvasnová, S., Schierová, D., ... ve Moniello, G. (2021). The Effect of a High-Grain Diet on the Rumen Microbiome of Goats with a Special Focus on Anaerobic Fungi. Microorganisms, 9(1) 157.
- Gelius-Dietrich, G., Ter Braak, M., Henze, K. (2007). Mitochondrial steps of arginine biosynthesis are conserved in the hydrogenosomes of the Chytridiomycete Neocallimastix frontalis. J. Eukaryot. Microbiol., 54 42–4.
- Gelius‐Dietrich, Gabriel., ve Henze, K. (2004). Pyruvate Formate Lyase (PFL) and PFL Activating Enzyme in the Chytrid Fungus Neocallimastix frontalis: A Free‐Radical Enzyme System Conserved Across Divergent Eukaryotic Lineages 1. Journal of Eukaryotic Microbiology, 51(4), 456-463.
- Gleason, F.H. ve Gordon, G.L.R. (2004). The ultrastructure of hydrogenosomes in thin sections and in freeze fracture replicas from the anaerobic chytrid fungus caecomyces sp. Australasian Mycologist, 22 (3) 92-98.
- Hackstein, J. H., Akhmanova, A., Boxma, B., Harhangi, H. R., ve Voncken, F. G. (1999). Hydrogenosomes: eukaryotic adaptations to anaerobic environments. Trends in microbiology, 7(11) 441-447.
- Hashimoto, T., Sánchez, L. B., Shirakura, T., Müller, M., & Hasegawa, M. (1998). Secondary absence of mitochondria in Giardia lamblia and Trichomonas vaginalis revealed by valyl-tRNA synthetase phylogeny. Proc. Natl. Acad. Sci., 95(12) 6860-6865.
- Heath, I. B., Bauchop, T., ve Skipp, R. A. (1983). Assignment of the rumen anaerobe Neocallimastix frontalis to the Spizellomycetales (Chytridiomycetes) on the basis of its polyflagellate zoospore ultrastructure. Can. J. Bot., 61(1) 295-307.
- Henze, K. (2007). The proteome of T. vaginalis hydrogenosomes. In Hydrogenosomes and mitosomes: mitochondria of anaerobic eukaryotes (pp. 163-178). Springer, Berlin, Heidelberg.
- Julliand, V., Riondet, C., de Vaux, A., Alcaraz, G., ve Fonty, G. (1998). Comparison of metabolic activities between Piromyces citronii, an equine fungal species, and Piromyces communis, a ruminal species. Anim. Feed Sci. Technol., 70(1-2), 161-168.
- Koonin, E. V. (2015). Origin of eukaryotes from within archaea, archaeal eukaryome and bursts of gene gain: eukaryogenesis just made easier?. Philos. Trans. R. Soc. B: Biological Sciences, 370(1678) 20140333.
- Li, J., Heath, I. B., ve Bauchop, T. (1990). Piromyces mae and Piromyces dumbonica, two new species of uniflagellate anaerobic chytridiomycete fungi from the hindgut of the horse and elephant. Can. J. Bot., 68(5) 1021-1033.
- Li, J., Heath, I. B., ve Cheng, K. J. (1991). The development and zoospore ultrastructure of a polycentric chytridiomycete gut fungus, Orpinomyces joyonii comb. nov. Can. J. Bot., 69(3) 580-589.
- Lindmark, D. G., ve Müller, M. (1973). Hydrogenosome, a cytoplasmic organelle of the anaerobic flagellate Tritrichomonas foetus, and its role in pyruvate metabolism. J. Biol. Chem., 248(22) 7724-7728.
- Martin, W. (2005). The missing link between hydrogenosomes and mitochondria. Trends in microbiology, 13(10) 457-459.
- Martin, W. ve Russell, M.J. (2003). On the origins of cells: a hypothesis for the evolutionary transitions from abiotic geochemistry to chemoautotrophic prokaryotes, and from prokaryotes to nucleated cells. Philos. Trans. R. Soc. Lond. B Biol. Sci., 358 59-83.
- Martin, W., ve Müller, M. (1998). The hydrogen hypothesis for the first eukaryote. Nature, 392(6671) 37-41.
- Marvin-Sikkema, F.D., Lahpor, G.A., Kraak, M.N., Gottschal, J.C., ve Prins, R.A. (1992). Characterization of an anaerobic fungus from llama faeces. J. General Microbiol., 138 2235-2241.
- Marvin-Sikkema, F.D., Pedro Gomes, T.M., Grivet, J.P., Gottschal, J.C., ve Prins, R.A. (1993). Characterization of hydrogenosomes and their role in glucose metabolism of Neocallimastix sp. L2. Arch. Microbiol., 160 388-396.
- Marvin-Sikkema, F.D., Richardson, A.J., Stewart, C.S., Gottschal, J.C., ve Prins, R.A. (1990). Influence of hydrogenconsuming bacteria on cellulose degradation by anaerobic fungi. Appl. Environ. Microbiol., 56 3793-3797.
- Müller, M. (1973). Biochemical cytology of trichomonad flagellates: I. Subcellular localization of hydrolases, dehydrogenases, and catalase in Tritrichomonas foetus. The Journal of cell biology, 57(2) 453-474.
- Müller, M. (1993). The hydrogenosome. J. Gen. Microbiol., 139(12) 2879-2889.
- Müller, M. (1998). Enzymes and compartmentation of core energy metabolism of anaerobic protists-a special case in eukaryotic evolution?. Evolutionary relationships among protozoa., 109-132.
- Müller, M., Mentel, M., van Hellemond, J. J., Henze, K., Woehle, C., Gould, S. B., ... ve Martin, W. F. (2012). Biochemistry and evolution of anaerobic energy metabolism in eukaryotes. Microbiol. Mol. Biol. R., 76(2) 444-495.
- O'Fallon, J. V., Wright Jr, R. W., ve Calza, R. E. (1991). Glucose metabolic pathways in the anaerobic rumen fungus Neocallimastix frontalis EB188. Biochem. J., 274(2) 595-599.
- Paul, R.G., Williams, A.G., ve Butler, R.D. (1990). Hydrogenosomes in the rumen entodiniomorphid ciliate Polyplastron multivesiculatum. J. Gen. Microbiol., 136 1981-1989.
- Roger, A.J., (1999). Reconstructing early events in eukaryotic evolution. Am. Nat., 154 S146–S163.
- Rosenthal, B., Mai, Z., Caplivski, D., Ghosh, S., de la Vega, H., Graf, T., ve Samuelson, J. (1997). Evidence for the bacterial origin of genes encoding fermentation enzymes of the amitochondriate protozoan parasite Entamoeba histolytica. J. Bacteriol., 179(11) 3736-3745.
- Shiflett, A. M. ve Johnson, P. J. (2010). Mitochondrion-related organelles in eukaryotic protists. Annu. Rev. Microbiol., 64 409–429.
- Tielens, A. G., Rotte, C., van Hellemond, J. J., ve Martin, W. (2002). Mitochondria as we don't know them. Trends Biochem. Sci., 27(11) 564-572.
- Timmis, J.N., Ayliffe, M.A., Huang, C.Y., ve Martin, W. (2004). Endosymbiotic gene transfer: organelle genomes forge eukaryotic chromosomes. Nat. Rev. Genet., 5 123-135.
- Tovar, J., Leon-Avila, G., Sanchez, L.B., Sutak, R., Tachezy, J., van der Giezen, M., Hernandez, M., Müller, M., and Lucocq, J.M. (2003).
Mitochondrial remnant organelles of Giardia function in iron-sulphur protein maturation. Nature, 426 172-176.
- Trinci, A.P., Davies, D.R., Gull, K., Lawrence, M.I., Bonde Nielsen, B., Rickers, A., ve Theodorou, M.K. (1994). Anaerobic fungi in herbivorous animals. Mycol. Res., 98 129-152.
- van der Giezen, M., Birdsey, G. M., Horner, D. S., Lucocq, J., Dyal, P. L., Benchimol, M., ... ve Embley, T. M. (2003). Fungal hydrogenosomes contain mitochondrial heat-shock proteins. Mol. Biol. Evol., 20(7), 1051-1061.
- van der Giezen, M., Rechinger, K. B. R., Svendsen, I., Durand, R., Hirt, R. P., Fevre, M., ... ve Prins, R. A. (1997a). A mitochondrial‐like targeting signal on the hydrogenosomal malic enzyme from the anaerobic fungus Neocallimastix frontalis: support for the hypothesis that hydrogenosomes are modified mitochondria. Mol. Microbiol., 23(1) 11-21.
- van der Giezen, M., Sjollema, K. A., Artz, R. R., Alkema, W., ve Prins, R. A. (1997b). Hydrogenosomes in the anaerobic fungus Neocallimastix frontalis have a double membrane but lack an associated organelle genome. FEBS letters, 408(2) 147-150.
- van der Giezen, M., Slotboom, D. J., Horner, D. S., Dyal, P. L., Harding, M., Xue, G. P., ... ve Kunji, E. R. (2002). Conserved properties of hydrogenosomal and mitochondrial ADP/ATP carriers: a common origin for both organelles. The EMBO journal, 21(4) 572-579.
- Vanacova, S., Liston, D. R., Tachezy, J., ve Johnson, P. J. (2003). Molecular biology of the amitochondriate parasites, Giardia intestinalis, Entamoeba histolytica and Trichomonas vaginalis. Int. J. Parasitol., 33(3) 235-255.
- Yarlett, N., Coleman, G.S., Williams, A.G., Lloyd, D., (1984). Hydrogenosomes in known species of rumen entodiniomorphid protozoa. FEMS Microbiol. Lett., 21 15–19.
- Yarlett, N., Orpin, C. G., Munn, E. A., Yarlett, N. C., ve Greenwood, C. A. (1986). Hydrogenosomes in the rumen fungus Neocallimastix patriciarum. Biochem. J., 236(3) 729-739.
Hydrogenosomes in the Anaerobic Fungi: Hydrogen-Producing Organelles
Year 2021,
Volume: 12 Issue: 2, 190 - 208, 31.10.2021
Ferit Can Yazdıç
,
Fadime Yazdıç
,
Bülent Kar
,
Prof. Dr. Emin Özköse
,
Mehmet Sait Ekinci
Abstract
Fungi form a very diverse group in eukaryotes. Most of the fungi contain mitochondria and capable of oxidative phosphorylation. On the other hand, anaerobic Neocallimastigomycota fungi are in the gastrointestinal tract of many herbivorous mammals, they contain an organelle known as hydrogenosome instead of mitochondria. These organelles capable of being the key to adaptation to an anaerobic environment that is is unique. In this review, we wish to briefly summarize what is known about function, structure, biochemistry, genetics properties and inheritance of these important organelles.
References
- Akhmanova, A., Voncken, F. G., Hosea, K. M., Harhangi, H., Keltjens, J. T., Op Den Camp, H. J., ... ve Hackstein, J. H. (1999). A hydrogenosome with pyruvate formate‐lyase: Anaerobic chytrid fungi use an alternative route for pyruvate catabolism. Mol. Microbiol., 32(5) 1103-1114.
- Benchimol M. (2007). Structure of the Hydrogenosomes (in this volume). Springer, Heidelberg.
- Benchimol, M., (2000). Ultrastructural characterization of the isolated hydrogenosome in Tritrichomonas foetus. Tissue Cell, 32 1–9.
- Benchimol, M., Almeida, J.C.A., ve de Souza, W. (1996). Further studies on the organization of the hydrogenosome of Tritrichomonas foetus. Tissue Cell, 28 287-299.
- Benchimol, M., Leal, D., Mattos, A., ve Diniz, J.A.P. (1997). Fine structure of Trichomonas gallinae. Biocell, 21 47-58.
- Benchimol, M., ve De Souza, W. (1983). Fine Structure and Cytochemistry of the Hydrogenosome of Tritrichomonas foetus 1. J. Protozool, 30(2) 422-425.
- Boxma, B., de Graaf, R. M., van der Staay, G. W., van Alen, T. A., Ricard, G., Gabaldón, T., ... ve Hackstein, J. H. (2005). An anaerobic mitochondrion that produces hydrogen. Nature, 434(7029) 74-79.
- Boxma, B., Voncken, F., Jannink, S., Van Alen, T., Akhmanova, A., Van Weelden, S. W., ... ve 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(5) 1389-1399.
- Cavalier-Smith, T. (1983). A 6-kingdom classification and a unified phylogeny. Intracellular space as oligogenetic ecosystem, 1027-1034.
- Dacks, J. B., Dyal, P. L., Embley, T. M., ve van der Giezen, M. (2006). Hydrogenosomal succinyl-CoA synthetase from the rumen-dwelling fungus Neocallimastix patriciarum; an energy-producing enzyme of mitochondrial origin. Gene, 373 75-82.
- Durand, R., Fischer, M., Rascle, C., ve Fevre, M. (1995). Neocallimastix frontalis enolase gene, enol: first report of an intron in an anaerobic fungus. Microbiology, 141(6) 1301-1308.
- Dyall, S. D., Koehler, C. M., Delgadillo-Correa, M. G., Bradley, P. J., Plümper, E., Leuenberger, D., ... ve Johnson, P. J. (2000). Presence of a member of the mitochondrial carrier family in hydrogenosomes: conservation of membrane-targeting pathways between hydrogenosomes and mitochondria. Mol. Cell. Biol., 20(7) 2488-2497.
- Dyall, S. D., Yan, W., Delgadillo-Correa, M. G., Lunceford, A., Loo, J. A., Clarke, C. F., ve Johnson, P. J. (2004). Non-mitochondrial complex I proteins in a hydrogenosomal oxidoreductase complex. Nature, 431(7012) 1103-1107.
- Embley, M., der Giezen, M. V., Horner, D. S., Dyal, P. L., ve Foster, P. (2003). Mitochondria and hydrogenosomes are two forms of the same fundamental organelle. Philos. Trans. R. Soc. Lond. B Biol. Sci., 358(1429) 191-203.
- Field, J., Rosenthal, B., ve Samuelson, J. (2000). Early lateral transfer of genes encoding malic enzyme, acetyl‐CoA synthetase and alcohol dehydrogenases from anaerobic prokaryotes to Entamoeba histolytica. Mol. Microbiol., 38(3) 446-455.
- Finlay, B.J. ve Fenchel, T. (1989). Hydrogenosomes in some anaerobic protozoa resemble mitochondria. FEMS Microbiol. Lett., 65 311-314.
- Fliegerova, K. O., Podmirseg, S. M., Vinzelj, J., Grilli, D. J., Kvasnová, S., Schierová, D., ... ve Moniello, G. (2021). The Effect of a High-Grain Diet on the Rumen Microbiome of Goats with a Special Focus on Anaerobic Fungi. Microorganisms, 9(1) 157.
- Gelius-Dietrich, G., Ter Braak, M., Henze, K. (2007). Mitochondrial steps of arginine biosynthesis are conserved in the hydrogenosomes of the Chytridiomycete Neocallimastix frontalis. J. Eukaryot. Microbiol., 54 42–4.
- Gelius‐Dietrich, Gabriel., ve Henze, K. (2004). Pyruvate Formate Lyase (PFL) and PFL Activating Enzyme in the Chytrid Fungus Neocallimastix frontalis: A Free‐Radical Enzyme System Conserved Across Divergent Eukaryotic Lineages 1. Journal of Eukaryotic Microbiology, 51(4), 456-463.
- Gleason, F.H. ve Gordon, G.L.R. (2004). The ultrastructure of hydrogenosomes in thin sections and in freeze fracture replicas from the anaerobic chytrid fungus caecomyces sp. Australasian Mycologist, 22 (3) 92-98.
- Hackstein, J. H., Akhmanova, A., Boxma, B., Harhangi, H. R., ve Voncken, F. G. (1999). Hydrogenosomes: eukaryotic adaptations to anaerobic environments. Trends in microbiology, 7(11) 441-447.
- Hashimoto, T., Sánchez, L. B., Shirakura, T., Müller, M., & Hasegawa, M. (1998). Secondary absence of mitochondria in Giardia lamblia and Trichomonas vaginalis revealed by valyl-tRNA synthetase phylogeny. Proc. Natl. Acad. Sci., 95(12) 6860-6865.
- Heath, I. B., Bauchop, T., ve Skipp, R. A. (1983). Assignment of the rumen anaerobe Neocallimastix frontalis to the Spizellomycetales (Chytridiomycetes) on the basis of its polyflagellate zoospore ultrastructure. Can. J. Bot., 61(1) 295-307.
- Henze, K. (2007). The proteome of T. vaginalis hydrogenosomes. In Hydrogenosomes and mitosomes: mitochondria of anaerobic eukaryotes (pp. 163-178). Springer, Berlin, Heidelberg.
- Julliand, V., Riondet, C., de Vaux, A., Alcaraz, G., ve Fonty, G. (1998). Comparison of metabolic activities between Piromyces citronii, an equine fungal species, and Piromyces communis, a ruminal species. Anim. Feed Sci. Technol., 70(1-2), 161-168.
- Koonin, E. V. (2015). Origin of eukaryotes from within archaea, archaeal eukaryome and bursts of gene gain: eukaryogenesis just made easier?. Philos. Trans. R. Soc. B: Biological Sciences, 370(1678) 20140333.
- Li, J., Heath, I. B., ve Bauchop, T. (1990). Piromyces mae and Piromyces dumbonica, two new species of uniflagellate anaerobic chytridiomycete fungi from the hindgut of the horse and elephant. Can. J. Bot., 68(5) 1021-1033.
- Li, J., Heath, I. B., ve Cheng, K. J. (1991). The development and zoospore ultrastructure of a polycentric chytridiomycete gut fungus, Orpinomyces joyonii comb. nov. Can. J. Bot., 69(3) 580-589.
- Lindmark, D. G., ve Müller, M. (1973). Hydrogenosome, a cytoplasmic organelle of the anaerobic flagellate Tritrichomonas foetus, and its role in pyruvate metabolism. J. Biol. Chem., 248(22) 7724-7728.
- Martin, W. (2005). The missing link between hydrogenosomes and mitochondria. Trends in microbiology, 13(10) 457-459.
- Martin, W. ve Russell, M.J. (2003). On the origins of cells: a hypothesis for the evolutionary transitions from abiotic geochemistry to chemoautotrophic prokaryotes, and from prokaryotes to nucleated cells. Philos. Trans. R. Soc. Lond. B Biol. Sci., 358 59-83.
- Martin, W., ve Müller, M. (1998). The hydrogen hypothesis for the first eukaryote. Nature, 392(6671) 37-41.
- Marvin-Sikkema, F.D., Lahpor, G.A., Kraak, M.N., Gottschal, J.C., ve Prins, R.A. (1992). Characterization of an anaerobic fungus from llama faeces. J. General Microbiol., 138 2235-2241.
- Marvin-Sikkema, F.D., Pedro Gomes, T.M., Grivet, J.P., Gottschal, J.C., ve Prins, R.A. (1993). Characterization of hydrogenosomes and their role in glucose metabolism of Neocallimastix sp. L2. Arch. Microbiol., 160 388-396.
- Marvin-Sikkema, F.D., Richardson, A.J., Stewart, C.S., Gottschal, J.C., ve Prins, R.A. (1990). Influence of hydrogenconsuming bacteria on cellulose degradation by anaerobic fungi. Appl. Environ. Microbiol., 56 3793-3797.
- Müller, M. (1973). Biochemical cytology of trichomonad flagellates: I. Subcellular localization of hydrolases, dehydrogenases, and catalase in Tritrichomonas foetus. The Journal of cell biology, 57(2) 453-474.
- Müller, M. (1993). The hydrogenosome. J. Gen. Microbiol., 139(12) 2879-2889.
- Müller, M. (1998). Enzymes and compartmentation of core energy metabolism of anaerobic protists-a special case in eukaryotic evolution?. Evolutionary relationships among protozoa., 109-132.
- Müller, M., Mentel, M., van Hellemond, J. J., Henze, K., Woehle, C., Gould, S. B., ... ve Martin, W. F. (2012). Biochemistry and evolution of anaerobic energy metabolism in eukaryotes. Microbiol. Mol. Biol. R., 76(2) 444-495.
- O'Fallon, J. V., Wright Jr, R. W., ve Calza, R. E. (1991). Glucose metabolic pathways in the anaerobic rumen fungus Neocallimastix frontalis EB188. Biochem. J., 274(2) 595-599.
- Paul, R.G., Williams, A.G., ve Butler, R.D. (1990). Hydrogenosomes in the rumen entodiniomorphid ciliate Polyplastron multivesiculatum. J. Gen. Microbiol., 136 1981-1989.
- Roger, A.J., (1999). Reconstructing early events in eukaryotic evolution. Am. Nat., 154 S146–S163.
- Rosenthal, B., Mai, Z., Caplivski, D., Ghosh, S., de la Vega, H., Graf, T., ve Samuelson, J. (1997). Evidence for the bacterial origin of genes encoding fermentation enzymes of the amitochondriate protozoan parasite Entamoeba histolytica. J. Bacteriol., 179(11) 3736-3745.
- Shiflett, A. M. ve Johnson, P. J. (2010). Mitochondrion-related organelles in eukaryotic protists. Annu. Rev. Microbiol., 64 409–429.
- Tielens, A. G., Rotte, C., van Hellemond, J. J., ve Martin, W. (2002). Mitochondria as we don't know them. Trends Biochem. Sci., 27(11) 564-572.
- Timmis, J.N., Ayliffe, M.A., Huang, C.Y., ve Martin, W. (2004). Endosymbiotic gene transfer: organelle genomes forge eukaryotic chromosomes. Nat. Rev. Genet., 5 123-135.
- Tovar, J., Leon-Avila, G., Sanchez, L.B., Sutak, R., Tachezy, J., van der Giezen, M., Hernandez, M., Müller, M., and Lucocq, J.M. (2003).
Mitochondrial remnant organelles of Giardia function in iron-sulphur protein maturation. Nature, 426 172-176.
- Trinci, A.P., Davies, D.R., Gull, K., Lawrence, M.I., Bonde Nielsen, B., Rickers, A., ve Theodorou, M.K. (1994). Anaerobic fungi in herbivorous animals. Mycol. Res., 98 129-152.
- van der Giezen, M., Birdsey, G. M., Horner, D. S., Lucocq, J., Dyal, P. L., Benchimol, M., ... ve Embley, T. M. (2003). Fungal hydrogenosomes contain mitochondrial heat-shock proteins. Mol. Biol. Evol., 20(7), 1051-1061.
- van der Giezen, M., Rechinger, K. B. R., Svendsen, I., Durand, R., Hirt, R. P., Fevre, M., ... ve Prins, R. A. (1997a). A mitochondrial‐like targeting signal on the hydrogenosomal malic enzyme from the anaerobic fungus Neocallimastix frontalis: support for the hypothesis that hydrogenosomes are modified mitochondria. Mol. Microbiol., 23(1) 11-21.
- van der Giezen, M., Sjollema, K. A., Artz, R. R., Alkema, W., ve Prins, R. A. (1997b). Hydrogenosomes in the anaerobic fungus Neocallimastix frontalis have a double membrane but lack an associated organelle genome. FEBS letters, 408(2) 147-150.
- van der Giezen, M., Slotboom, D. J., Horner, D. S., Dyal, P. L., Harding, M., Xue, G. P., ... ve Kunji, E. R. (2002). Conserved properties of hydrogenosomal and mitochondrial ADP/ATP carriers: a common origin for both organelles. The EMBO journal, 21(4) 572-579.
- Vanacova, S., Liston, D. R., Tachezy, J., ve Johnson, P. J. (2003). Molecular biology of the amitochondriate parasites, Giardia intestinalis, Entamoeba histolytica and Trichomonas vaginalis. Int. J. Parasitol., 33(3) 235-255.
- Yarlett, N., Coleman, G.S., Williams, A.G., Lloyd, D., (1984). Hydrogenosomes in known species of rumen entodiniomorphid protozoa. FEMS Microbiol. Lett., 21 15–19.
- Yarlett, N., Orpin, C. G., Munn, E. A., Yarlett, N. C., ve Greenwood, C. A. (1986). Hydrogenosomes in the rumen fungus Neocallimastix patriciarum. Biochem. J., 236(3) 729-739.