Hostname: page-component-586b7cd67f-l7hp2 Total loading time: 0 Render date: 2024-11-22T06:45:01.408Z Has data issue: false hasContentIssue false
  • English
  • Français

Acetate and succinate production in amoebae, helminths, diplomonads, trichomonads and trypanosomatids: common and diverse metabolic strategies used by parasitic lower eukaryotes

Published online by Cambridge University Press:  23 December 2009

F. BRINGAUD ,
C. EBIKEME  and
M. BOSHART
F. BRINGAUD*
Affiliation:
Résonance Magnétique des Systèmes Biologiques, UMR-5536 CNRS, Université Victor Segalen Bordeaux 2, 146 rue Léo Saignat, 33076 Bordeaux cedex, France
C. EBIKEME
Affiliation:
Résonance Magnétique des Systèmes Biologiques, UMR-5536 CNRS, Université Victor Segalen Bordeaux 2, 146 rue Léo Saignat, 33076 Bordeaux cedex, France
M. BOSHART
Affiliation:
Biozentrum, Genetik, Ludwig-Maximilians-Universität München, Grosshadernerstr. 2-4, D-82152 Martinsried, Germany
*
*Corresponding author: Tel: (33) 5 57 57 46 32. Fax: (33) 5 57 57 45 56. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

Parasites that often grow anaerobically in their hosts have adopted a fermentative strategy relying on the production of partially oxidized end products, including lactate, glycerol, ethanol, succinate and acetate. This review focuses on recent progress in understanding acetate production in protist parasites, such as amoebae, diplomonads, trichomonads, trypanosomatids and in the metazoan parasites helminths, as well as the succinate production pathway(s) present in some of them. We also describe the unconventional organisation of the tricarboxylic acid cycle associated with the fermentative strategy adopted by the procyclic trypanosomes, which may resemble the probable structure of the primordial TCA cycle in prokaryotes.

Keywords

acetate and succinate excretionacetate:succinate CoA-transferaseEntamoeba histolyticaFasciola hepaticafumarate reductaseGiardia lambliareductive TCA cycleTrichomonas vaginalisTrypanosoma brucei
Type
Research Article
Information
Parasitology , Volume 137 , Special Issue 9: Insights into the metabolomes of parasites , August 2010 , pp. 1315 - 1331
Copyright
Copyright © Cambridge University Press 2009

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Adam, R. D. (2001). Biology of Giardia lamblia. Clinical Microbiology Reviews 14, 447–475.CrossRefGoogle ScholarPubMed
Anderson, I. J. and Loftus, B. J. (2005). Entamoeba histolytica: observations on metabolism based on the genome sequence. Experimental Parasitology 110, 173–177.CrossRefGoogle ScholarPubMed
Arikawa, Y., Enomoto, K., Muratsubaki, H. and Okazaki, M. (1998). Soluble fumarate reductase isoenzymes from Saccharomyces cerevisiae are required for anaerobic growth. FEMS Microbiology Letters 165, 111–116.CrossRefGoogle ScholarPubMed
Bapteste, E., Moreira, D. and Philippe, H. (2003). Rampant horizontal gene transfer and phospho-donor change in the evolution of the phosphofructokinase. Gene 318, 185–191.CrossRefGoogle ScholarPubMed
Barrett, M. P., Burchmore, R. J., Stich, A., Lazzari, J. O., Frasch, A. C., Cazzulo, J. J. and Krishna, S. (2003). The trypanosomiases. Lancet 362, 1469–1480.CrossRefGoogle ScholarPubMed
Besteiro, S., Barrett, M. P., Riviere, L. and Bringaud, F. (2005). Energy generation in insect stages of Trypanosoma brucei: metabolism in flux. Trends in Parasitology 21, 185–191.CrossRefGoogle ScholarPubMed
Besteiro, S., Biran, M., Biteau, N., Coustou, V., Baltz, T., Canioni, P. and Bringaud, F. (2002). Succinate secreted by Trypanosoma brucei is produced by a novel and unique glycosomal enzyme, NADH-dependent fumarate reductase. Journal of Biological Chemistry 277, 38001–38012.CrossRefGoogle ScholarPubMed
Bochud-Allemann, N. and Schneider, A. (2002). Mitochondrial substrate level phosphorylation is essential for growth of procyclic Trypanosoma brucei. Journal of Biological Chemistry 277, 32849–32854.CrossRefGoogle ScholarPubMed
Bogitsh, B. J., Carter, C. E. and Oeltmann, T. N. (2005). Human Parasitology, third edition, Elsevier Academic Press Inc., USA.Google Scholar
Boxma, B., De Graaf, R. M., Van Der Staay, G. W., Van Alen, T. A., Ricard, G., Gabaldon, T., Van Hoek, A. H., Moon-Van Der Staay, S. Y., Koopman, W. J., Van Hellemond, J. J., Tielens, A. G., Friedrich, T., Veenhuis, M., Huynen, M. A. and Hackstein, J. H. (2005). An anaerobic mitochondrion that produces hydrogen. Nature 434, 74–79.CrossRefGoogle ScholarPubMed
Bringaud, F., Baltz, D. and Baltz, T. (1998). Functional and molecular characterization of a glycosomal PPi-dependent enzyme in trypanosomatids: pyruvate, phosphate dikinase. Proceedings of the National Academy of Sciences, USA 95, 7963–7968.CrossRefGoogle ScholarPubMed
Bringaud, F., Riviere, L. and Coustou, V. (2006). Energy metabolism of trypanosomatids: adaptation to available carbon sources. Molecular and Biochemical Parasitology 149, 1–9.CrossRefGoogle ScholarPubMed
Brown, D. M., Upcroft, J. A., Edwards, M. R. and Upcroft, P. (1998). Anaerobic bacterial metabolism in the ancient eukaryote Giardia duodenalis. International Journal for Parasitology 28, 149–164.CrossRefGoogle ScholarPubMed
Brown, T. D., Jones-Mortimer, M. C. and Kornberg, H. L. (1977). The enzymic interconversion of acetate and acetyl-coenzyme A in Escherichia coli. Journal of General Microbiology 102, 327–336.CrossRefGoogle ScholarPubMed
Bruderer, T., Wehrli, C. and Kohler, P. (1996). Cloning and characterization of the gene encoding pyruvate phosphate dikinase from Giardia duodenalis. Molecular and Biochemical Parasitology 77, 225–233.CrossRefGoogle ScholarPubMed
Casal, M., Cardoso, H. and Leao, C. (1996). Mechanisms regulating the transport of acetic acid in Saccharomyces cerevisiae. Microbiology 142, 1385–1390.CrossRefGoogle ScholarPubMed
Cassio, F., Leao, C. and Van Uden, N. (1987). Transport of lactate and other short-chain monocarboxylates in the yeast Saccharomyces cerevisiae. Applied and Environmental Microbiology 53, 509–513.CrossRefGoogle ScholarPubMed
Cazzulo, J. J. (1992). Aerobic fermentation of glucose by trypanosomatids. FASEB Journal 6, 3153–3161.CrossRefGoogle ScholarPubMed
Chi, A. S., Deng, Z., Albach, R. A. and Kemp, R. G. (2001). The two phosphofructokinase gene products of Entamoeba histolytica. Journal of Biological Chemistry 276, 19974–19981.CrossRefGoogle ScholarPubMed
Chi, A. and Kemp, R. G. (2000). The primordial high energy compound: ATP or inorganic pyrophosphate? Journal of Biological Chemistry 275, 35677–35679.CrossRefGoogle ScholarPubMed
Colasante, C., Ellis, M., Ruppert, T. and Voncken, F. (2006). Comparative proteomics of glycosomes from bloodstream form and procyclic culture form Trypanosoma brucei brucei. Proteomics 6, 3275–3293.CrossRefGoogle ScholarPubMed
Colasante, C., Peña Diaz, P., Clayton, C. and Voncken, F. (2009). Mitochondrial carrier family inventory of Trypanosoma brucei brucei: Identification, expression and subcellular localisation. Molecular and Biochemical Parasitology 167, 104–117.CrossRefGoogle ScholarPubMed
Coombs, G. H. and Müller, M. (1995). Energy metabolism in anaerobic protozoa. In Biochemistry and Molecular Biology of Parasites (ed. Marr, J. J. and Müller, M.), pp. 33–47. Academic Press Ltd, London.CrossRefGoogle Scholar
Cotch, M. F., Pastorek, J. G. 2nd, Nugent, R. P., Hillier, S. L., Gibbs, R. S., Martin, D. H., Eschenbach, D. A., Edelman, R., Carey, J. C., Regan, J. A., Krohn, M. A., Klebanoff, M. A., Rao, A. V. and Rhoads, G. G. (1997). Trichomonas vaginalis associated with low birth weight and preterm delivery. The Vaginal Infections and Prematurity Study Group. Sexually Transmitted Diseases 24, 353–360.CrossRefGoogle ScholarPubMed
Coustou, V., Besteiro, S., Biran, M., Diolez, P., Bouchaud, V., Voisin, P., Michels, P. A., Canioni, P., Baltz, T. and Bringaud, F. (2003). ATP generation in the Trypanosoma brucei procyclic form: Cytosolic substrate level phosphorylation is essential, but not oxidative phosphorylation. Journal of Biological Chemistry 278, 49625–49635.CrossRefGoogle Scholar
Coustou, V., Besteiro, S., Riviere, L., Biran, M., Biteau, N., Franconi, J. M., Boshart, M., Baltz, T. and Bringaud, F. (2005). A mitochondrial NADH-dependent fumarate reductase involved in the production of succinate excreted by procyclic Trypanosoma brucei. Journal of Biological Chemistry 280, 16559–16570.CrossRefGoogle ScholarPubMed
Coustou, V., Biran, M., Besteiro, S., Riviere, L., Baltz, T., Franconi, J. M. and Bringaud, F. (2006). Fumarate is an essential intermediary metabolite produced by the procyclic Trypanosoma brucei. Journal of Biological Chemistry 281, 26832–26846.CrossRefGoogle ScholarPubMed
Coustou, V., Biran, M., Breton, M., Guegan, F., Riviere, L., Plazolles, N., Nolan, D., Barrett, M. P., Franconi, J. M. and Bringaud, F. (2008). Glucosed-induced remodelling of intermediary and energy metabolism in procyclic Trypanosoma brucei. Journal of Biological Chemistry 283, 16342–16354.CrossRefGoogle Scholar
Crabtree, H. G. (1929). Observations on the carbohydrate metabolism of tumours. Biochemical Journal 23, 536–545.CrossRefGoogle ScholarPubMed
Cross, G. A., Klein, R. A. and Linstead, D. J. (1975). Utilization of amino acids by Trypanosoma brucei in culture: L-threonine as a precursor for acetate. Parasitology 71, 311–326.CrossRefGoogle ScholarPubMed
Das, S., Stevens, T., Castillo, C., Villasenor, A., Arredondo, H. and Reddy, K. (2002). Lipid metabolism in mucous-dwelling amitochondriate protozoa. International Journal for Parasitology 32, 655–675.CrossRefGoogle ScholarPubMed
Dolezal, P., Smid, O., Rada, P., Zubacova, Z., Bursac, D., Sutak, R., Nebesarova, J., Lithgow, T. and Tachezy, J. (2005). Giardia mitosomes and trichomonad hydrogenosomes share a common mode of protein targeting. Proceedings of the National Academy of Sciences, USA 102, 10924–10929.CrossRefGoogle Scholar
Durieux, P. O., Schutz, P., Brun, R. and Kohler, P. (1991). Alterations in Krebs cycle enzyme activities and carbohydrate catabolism in two strains of Trypanosoma brucei during in vitro differentiation of their bloodstream to procyclic stages. Molecular and Biochemical Parasitology 45, 19–27.CrossRefGoogle ScholarPubMed
Dyall, S. D. and Johnson, P. J. (2000). Origins of hydrogenosomes and mitochondria: evolution and organelle biogenesis. Current Opinion in Microbiology 3, 404–411.CrossRefGoogle ScholarPubMed
Ebikeme, C. E., Peacock, L., Coustou, V., Riviere, L., Bringaud, F., Gibson, W. C. and Barrett, M. P. (2008). N-acetyl D-glucosamine stimulates growth in procyclic forms of Trypanosoma brucei by inducing a metabolic shift. Parasitology 135, 585–594.CrossRefGoogle ScholarPubMed
Etchegorry, M. G., Helenport, J. P., Pecoul, B., Jannin, J. and Legros, D. (2001). Availability and affordability of treatment for Human African Trypanosomiasis. Tropical Medicine and International Health 6, 957–959.CrossRefGoogle ScholarPubMed
Fleck, C. B. and Brock, M. (2009). Re-characterisation of Saccharomyces cerevisiae Ach1p: fungal CoA-transferases are involved in acetic acid detoxification. Fungal Genetics and Biology 46, 473–485.CrossRefGoogle ScholarPubMed
Furuya, T., Kessler, P., Jardim, A., Schnaufer, A., Crudder, C. and Parsons, M. (2002). Glucose is toxic to glycosome-deficient trypanosomes. Proceedings of the National Academy of Sciences, USA 99, 14177–14182.CrossRefGoogle ScholarPubMed
Gest, H. (1980). The evolution of biological energy-transducing systems. FEMS Microbiology Letters 7, 73–77.CrossRefGoogle Scholar
Gest, H. (1987). Evolutionary roots of the citric acid cycle in prokaryotes. Biochemical Society Symposia 54, 3–16.Google ScholarPubMed
Gimenez, R., Nunez, M. F., Badia, J., Aguilar, J. and Baldoma, L. (2003). The gene yjcG, cotranscribed with the gene acs, encodes an acetate permease in Escherichia coli. Journal of Bacteriology 185, 6448–6455.CrossRefGoogle ScholarPubMed
Glasemacher, J., Bock, A. K., Schmid, R. and Schonheit, P. (1997). Purification and properties of acetyl-CoA synthetase (ADP-forming), an archaeal enzyme of acetate formation and ATP synthesis, from the hyperthermophile Pyrococcus furiosus. European Journal of Biochemistry 244, 561–567.CrossRefGoogle ScholarPubMed
Goldberg, A. V., Molik, S., Tsaousis, A. D., Neumann, K., Kuhnke, G., Delbac, F., Vivares, C. P., Hirt, R. P., Lill, R. and Embley, T. M. (2008). Localization and functionality of microsporidian iron-sulphur cluster assembly proteins. Nature 452, 624–628.CrossRefGoogle ScholarPubMed
Guerra, D. G., Decottignies, A., Bakker, B. M. and Michels, P. A. (2006). The mitochondrial FAD-dependent glycerol-3-phosphate dehydrogenase of Trypanosomatidae and the glycosomal redox balance of insect stages of Trypanosoma brucei and Leishmania spp. Molecular and Biochemical Parasitology 149, 155–169.CrossRefGoogle ScholarPubMed
Hackstein, J. H., Akhmanova, A., Boxma, B., Harhangi, H. R. and Voncken, F. G. (1999). Hydrogenosomes: eukaryotic adaptations to anaerobic environments. Trends in Microbiology 7, 441–447.CrossRefGoogle ScholarPubMed
Heider, J. (2001). A new family of CoA-transferases. FEBS Letters 509, 345–349.CrossRefGoogle ScholarPubMed
Huynen, M. A., Dandekar, T. and Bork, P. (1999). Variation and evolution of the citric-acid cycle: a genomic perspective. Trends in Microbiology 7, 281–291.CrossRefGoogle ScholarPubMed
Jacob, F. (1977). Evolution and tinkering. Science 196, 1161–1166.CrossRefGoogle ScholarPubMed
Johnston, V. J. and Mabey, D. C. (2008). Global epidemiology and control of Trichomonas vaginalis. Current Opinion in Infectious Diseases 21, 56–64.CrossRefGoogle ScholarPubMed
Kastner, C. N., Schneider, K., Dimroth, P. and Pos, K. M. (2002). Characterization of the citrate/acetate antiporter CitW of Klebsiella pneumoniae. Archives of Microbiology 177, 500–506.CrossRefGoogle ScholarPubMed
Keenan, T. W. and Zierdt, C. H. (1994). Lipid biosynthesis by axenic strains of Blastocystis hominis. Comparative Biochemistry and Physiology. Part B, Biochemistry & Molecular Biology 107, 525–531.Google Scholar
Keiser, J. and Utzinger, J. (2009). Food-borne trematodiases. Clinical Microbiology Reviews 22, 466–483.CrossRefGoogle ScholarPubMed
Kihara, M. and Macnab, R. M. (1981). Cytoplasmic pH mediates pH taxis and weak-acid repellent taxis of bacteria. Journal of Bacteriology 145, 1209–1221.CrossRefGoogle ScholarPubMed
Klein, R. A. and Linstead, D. J. (1976). Threonine as a perferred source of 2-carbon units for lipid synthesis in Trypanosoma brucei. Biochemical Society Transactions 4, 48–50.CrossRefGoogle ScholarPubMed
Köhler, P. and Voigt, W. P. (1988). Nutrition and metabolism. In Parasitology in Focus (ed. Mehlhorn, H.), pp. 412–452. Springer-Verlag.CrossRefGoogle Scholar
Laga, M., Manoka, A., Kivuvu, M., Malele, B., Tuliza, M., Nzila, N., Goeman, J., Behets, F., Batter, V. and Alary, M. (1993). Non-ulcerative sexually transmitted diseases as risk factors for HIV-1 transmission in women: results from a cohort study. AIDS 7, 95–102.CrossRefGoogle ScholarPubMed
Lamour, N., Riviere, L., Coustou, V., Coombs, G. H., Barrett, M. P. and Bringaud, F. (2005). Proline metabolism in procyclic Trypanosoma brucei is down-regulated in the presence of glucose. Journal of Biological Chemistry 280, 11902–11910.CrossRefGoogle ScholarPubMed
Lantsman, Y., Tan, K. S., Morada, M. and Yarlett, N. (2008). Biochemical characterization of a mitochondrial-like organelle from Blastocystis sp. subtype 7. Microbiology 154, 2757–2766.CrossRefGoogle ScholarPubMed
Li, Z. and Phillips, N. F. (1997). Involvement and identification of a lysine in the PPi-site of pyrophosphate-dependent phosphofructokinase from Giardia lamblia. Biochimie 79, 221–227.CrossRefGoogle ScholarPubMed
Lindmark, D. G. and Muller, M. (1973). Hydrogenosome, a cytoplasmic organelle of the anaerobic flagellate Tritrichomonas foetus, and its role in pyruvate metabolism. Journal of Biological Chemistry 248, 7724–7728.CrossRefGoogle ScholarPubMed
Loftus, B., Anderson, I., Davies, R., Alsmark, U. C., Samuelson, J., Amedeo, P., Roncaglia, P., Berriman, M., Hirt, R. P., Mann, B. J., Nozaki, T., Suh, B., Pop, M., Duchene, M., Ackers, J., Tannich, E., Leippe, M., Hofer, M., Bruchhaus, I., Willhoeft, U., Bhattacharya, A., Chillingworth, T., Churcher, C., Hance, Z., Harris, B., Harris, D., Jagels, K., Moule, S., Mungall, K., Ormond, D., Squares, R., Whitehead, S., Quail, M. A., Rabbinowitsch, E., Norbertczak, H., Price, C., Wang, Z., Guillen, N., Gilchrist, C., Stroup, S. E., Bhattacharya, S., Lohia, A., Foster, P. G., Sicheritz-Ponten, T., Weber, C., Singh, U., Mukherjee, C., El-Sayed, N. M., Petri, W. A. Jr., Clark, C. G., Embley, T. M., Barrell, B., Fraser, C. M. and Hall, N. (2005). The genome of the protist parasite Entamoeba histolytica. Nature 433, 865–868.CrossRefGoogle ScholarPubMed
Marshall, M. M., Naumovitz, D., Ortega, Y. and Sterling, C. R. (1997). Waterborne protozoan pathogens. Clinical Microbiology Reviews 10, 67–85.CrossRefGoogle ScholarPubMed
Marvin-Sikkema, F. D., Pedro Gomes, T. M., Grivet, J. P., Gottschal, J. C. and Prins, R. A. (1993). Characterization of hydrogenosomes and their role in glucose metabolism of Neocallimastix sp. L2. Archives of Microbiology 160, 388–396.CrossRefGoogle ScholarPubMed
McManus, D. P. and Dalton, J. P. (2006). Vaccines against the zoonotic trematodes Schistosoma japonicum, Fasciola hepatica and Fasciola gigantica. Parasitology 133 (Suppl.), S43–S61.CrossRefGoogle ScholarPubMed
McNae, I. W., Martinez-Oyanedel, J., Keillor, J. W., Michels, P. A., Fothergill-Gilmore, L. A. and Walkinshaw, M. D. (2009). The crystal structure of ATP-bound phosphofructokinase from Trypanosoma brucei reveals conformational transitions different from those of other phosphofructokinases. Journal of Molecular Biology 385, 1519–1533.CrossRefGoogle ScholarPubMed
Melendez-Hevia, E., Waddell, T. G. and Cascante, M. (1996). The puzzle of the Krebs citric acid cycle: assembling the pieces of chemically feasible reactions, and opportunism in the design of metabolic pathways during evolution. Journal of Molecular Biology 43, 293–303.Google ScholarPubMed
Mertens, E. (1993). ATP versus pyrophosphate: glycolysis revisited in parasitic protists. Parasitology Today 9, 122–125.CrossRefGoogle ScholarPubMed
Mertens, E., Ladror, U. S., Lee, J. A., Miretsky, A., Morris, A., Rozario, C., Kemp, R. G. and Muller, M. (1998). The pyrophosphate-dependent phosphofructokinase of the protist, Trichomonas vaginalis, and the evolutionary relationships of protist phosphofructokinases. Journal of Molecular Evolution 47, 739–750.CrossRefGoogle ScholarPubMed
Michels, P. A., Bringaud, F., Herman, M. and Hannaert, V. (2006). Metabolic functions of glycosomes in trypanosomatids. Biochimica et Biophysica Acta 1763, 1463–1477.CrossRefGoogle ScholarPubMed
Michels, P. A. M., Michels, J. P. J., Boonstra, J. and Konings, W. N. (1979). Generation of an electrochemical proton gradient in bacteria by the excretion of metabolic end products. FEMS Microbiology letters 5, 357–364.CrossRefGoogle Scholar
Miura, A., Kameya, M., Arai, H., Ishii, M. and Igarashi, Y. (2008). A soluble NADH-dependent fumarate reductase in the reductive tricarboxylic acid cycle of Hydrogenobacter thermophilus TK-6. Journal of Bacteriology 190, 7170–7177.CrossRefGoogle ScholarPubMed
Mony, B. M., Mehta, M., Jarori, G. K. and Sharma, S. (2009). Plant-like phosphofructokinase from Plasmodium falciparum belongs to a novel class of ATP-dependent enzymes. International Journal for Parasitology 39, 1441–1453.CrossRefGoogle ScholarPubMed
Moreno-Sanchez, R., Saavedra, E., Rodriguez-Enriquez, S. and Olin-Sandoval, V. (2008). Metabolic control analysis: a tool for designing strategies to manipulate metabolic pathways. Journal of Biomedicine and Biotechnology 2008, 597913.CrossRefGoogle ScholarPubMed
Morris, J. C., Wang, Z., Drew, M. E. and Englund, P. T. (2002). Glycolysis modulates trypanosome glycoprotein expression as revealed by an RNAi library. EMBO Journal 21, 4429–4438.CrossRefGoogle ScholarPubMed
Muller, M. (1992). Energy metabolism of ancestral eukaryotes: a hypothesis based on the biochemistry of amitochondriate parasitic protists. Biosystems 28, 33–40.CrossRefGoogle ScholarPubMed
Muller, M. (1993). The hydrogenosome. Journal of General Microbiology 139, 2879–2889.CrossRefGoogle ScholarPubMed
Muratsubaki, H., Enomoto, K., Ichijoh, Y., Tezuka, T. and Katsume, T. (1994). Rapid purification of yeast cytoplasmic fumarate reductase by affinity chromatography on blue sepharose CL-6B. Preparative Biochemistry 24, 289–296.CrossRefGoogle ScholarPubMed
Opperdoes, F. R. and Borst, P. (1977). Localization of nine glycolytic enzymes in a microbody-like organelle in Trypanosoma brucei: the glycosome. FEBS Letters 80, 360–364.CrossRefGoogle Scholar
Orii, K. E., Fukao, T., Song, X. Q., Mitchell, G. A. and Kondo, N. (2008). Liver-specific silencing of the human gene encoding succinyl-CoA: 3-ketoacid CoA transferase. Tohoku Journal of Experimental Medicine 215, 227–236.CrossRefGoogle ScholarPubMed
Paget, T. A., Raynor, M. H., Shipp, D. W. and Lloyd, D. (1990). Giardia lamblia produces alanine anaerobically but not in the presence of oxygen. Molecular and Biochemical Parasitology 42, 63–67.CrossRefGoogle Scholar
Pealing, S. L., Black, A. C., Manson, F. D., Ward, F. B., Chapman, S. K. and Reid, G. A. (1992). Sequence of the gene encoding flavocytochrome c from Shewanella putrefaciens: a tetraheme flavoenzyme that is a soluble fumarate reductase related to the membrane-bound enzymes from other bacteria. Biochemistry 31, 12132–12140.CrossRefGoogle Scholar
Reeves, R. E. (1984). Metabolism of Entamoeba histolytica Schaudinn, 1903. Advances in Parasitology 23, 105–142.CrossRefGoogle ScholarPubMed
Riviere, L., Moreau, P., Allmann, S., Hahn, M., Biran, M., Plazolles, N., Franconi, J. M., Boshart, M. and Bringaud, F. (2009). Acetate produced in the mitochondrion is the essential precursor of lipid biosynthesis in procyclic trypanosomes. Proceedings of the National Academy of Sciences, USA 106, 12694–12699.CrossRefGoogle ScholarPubMed
Riviere, L., Van Weelden, S. W., Glass, P., Vegh, P., Coustou, V., Biran, M., Van Hellemond, J. J., Bringaud, F., Tielens, A. G. and Boshart, M. (2004). Acetyl:succinate CoA-transferase in procyclic Trypanosoma brucei. Gene identification and role in carbohydrate metabolism. Journal of Biological Chemistry 279, 45337–45346.CrossRefGoogle ScholarPubMed
Saas, J., Ziegelbauer, K., Von Haeseler, A., Fast, B. and Boshart, M. (2000). A developmentally regulated aconitase related to iron-regulatory protein-1 is localized in the cytoplasm and in the mitochondrion of Trypanosoma brucei. Journal of Biological Chemistry 275, 2745–2755.CrossRefGoogle ScholarPubMed
Saavedra-Lira, E., Ramirez-Silva, L. and Perez-Montfort, R. (1998). Expression and characterization of recombinant pyruvate phosphate dikinase from Entamoeba histolytica. Biochimica et Biophysica Acta 1382, 47–54.CrossRefGoogle ScholarPubMed
Sanchez, L. B. and Muller, M. (1996). Purification and characterization of the acetate forming enzyme, acetyl-CoA synthetase (ADP-forming) from the amitochondriate protist, Giardia lamblia. FEBS Letters 378, 240–244.CrossRefGoogle ScholarPubMed
Saz, H. J., Debruyn, B. and De Mata, Z. (1996). Acyl-CoA transferase activities in homogenates of Fasciola hepatica adults. Journal of Parasitology 82, 694–696.CrossRefGoogle ScholarPubMed
Schwebke, J. R. and Burgess, D. (2004). Trichomoniasis. Clinical Microbiology Reviews 17, 794–803.CrossRefGoogle ScholarPubMed
Searle, S. M. and Muller, M. (1991). Inorganic pyrophosphatase of Trichomonas vaginalis. Molecular and Biochemical Parasitology 44, 91–96.CrossRefGoogle ScholarPubMed
Slamovits, C. H. and Keeling, P. J. (2006). Pyruvate-phosphate dikinase of oxymonads and parabasalia and the evolution of pyrophosphate-dependent glycolysis in anaerobic eukaryotes. Eukaryotic Cell 5, 148–154.CrossRefGoogle ScholarPubMed
Stechmann, A., Hamblin, K., Perez-Brocal, V., Gaston, D., Richmond, G. S., Van Der Giezen, M., Clark, C. G. and Roger, A. J. (2008). Organelles in Blastocystis that blur the distinction between mitochondria and hydrogenosomes. Current Biology 18, 580–585.CrossRefGoogle ScholarPubMed
Steinbuchel, A. and Muller, M. (1986). Anaerobic pyruvate metabolism of Tritrichomonas foetus and Trichomonas vaginalis hydrogenosomes. Molecular and Biochemical Parasitology 20, 57–65.CrossRefGoogle ScholarPubMed
Stich, A., Barrett, M. P. and Krishna, S. (2003). Waking up to sleeping sickness. Trends in Parasitology 19, 195–197.CrossRefGoogle ScholarPubMed
Stoppani, A. O., Docampo, R., De Boiso, J. F. and Frasch, A. C. (1980). Effect of inhibitors of electron transport and oxidative phosphorylation on Trypanosoma cruzi respiration and growth. Molecular and Biochemical Parasitology 2, 3–21.CrossRefGoogle ScholarPubMed
Suematsu, N., Okamoto, K., Shibata, K., Nakanishi, Y. and Isohashi, F. (2001). Molecular cloning and functional expression of rat liver cytosolic acetyl-CoA hydrolase. European Journal of Biochemistry 268, 2700–2709.CrossRefGoogle ScholarPubMed
Takasaki, K., Shoun, H., Yamaguchi, M., Takeo, K., Nakamura, A., Hoshino, T. and Takaya, N. (2004). Fungal ammonia fermentation, a novel metabolic mechanism that couples the dissimilatory and assimilatory pathways of both nitrate and ethanol. Role of acetyl CoA synthetase in anaerobic ATP synthesis. Journal of Biological Chemistry 279, 12414–12420.CrossRefGoogle ScholarPubMed
Ten Brink, B. and Konings, W. N. (1986). Generation of a protonmotive force in anaerobic bacteria by end-product efflux. Methods in Enzymology 125, 492–510.CrossRefGoogle ScholarPubMed
Tielens, A. G., Van Den Heuvel, J. M. and Van Den Bergh, S. G. (1984). The energy metabolism of Fasciola hepatica during its development in the final host. Molecular and Biochemical Parasitology 13, 301–307.CrossRefGoogle ScholarPubMed
Tielens, A. G. and Van Hellemond, J. J. (1999). Reply. Parasitology Today 15, 347–348.CrossRefGoogle ScholarPubMed
Tovar, J., Fischer, A. and Clark, C. G. (1999). The mitosome, a novel organelle related to mitochondria in the amitochondrial parasite Entamoeba histolytica. Molecular Microbiology 32, 1013–1021.CrossRefGoogle ScholarPubMed
Turrens, J. (1999). More differences in energy metabolism between Trypanosomatidae. Parasitology Today 15, 346–348.CrossRefGoogle ScholarPubMed
Van Grinsven, K. W., Rosnowsky, S., Van Weelden, S. W., Putz, S., Van Der Giezen, M., Martin, W., Van Hellemond, J. J., Tielens, A. G. and Henze, K. (2008). Acetate:succinate CoA-transferase in the hydrogenosomes of Trichomonas vaginalis: identification and characterization. Journal of Biological Chemistry 283, 1411–1418.CrossRefGoogle ScholarPubMed
Van Grinsven, K. W., Van Hellemond, J. J. and Tielens, A. G. (2009). Acetate:succinate CoA-transferase in the anaerobic mitochondria of Fasciola hepatica. Molecular and Biochemical Parasitology 164, 74–79.CrossRefGoogle ScholarPubMed
Van Hellemond, J. J. and Tielens, A. G. (1994). Expression and functional properties of fumarate reductase. Biochemical Journal 304, 321–331.CrossRefGoogle ScholarPubMed
Van Hellemond, J. J. and Tielens, A. G. (1997). Inhibition of the respiratory chain results in a reversible metabolic arrest in Leishmania promastigotes. Molecular and Biochemical Parasitology 85, 135–138.CrossRefGoogle Scholar
Van Hellemond, J. J., Opperdoes, F. R. and Tielens, A. G. (1998). Trypanosomatidae produce acetate via a mitochondrial acetate:succinate CoA transferase. Proceedings of the National Academy of Sciences USA 95, 3036–3041.CrossRefGoogle Scholar
Van Hellemond, J. J., Van Der Klei, A., Van Weelden, S. W. and Tielens, A. G. (2003). Biochemical and evolutionary aspects of anaerobically functioning mitochondria. Philosophical Transactions of the Royal Society B: Biological Sciences 358, 205–213.CrossRefGoogle ScholarPubMed
Van Weelden, S. W., Fast, B., Vogt, A., Van Der Meer, P., Saas, J., Van Hellemond, J. J., Tielens, A. G. and Boshart, M. (2003). Procyclic Trypanosoma brucei do not use Krebs cycle activity for energy generation. Journal of Biological Chemistry 278, 12854–12863.CrossRefGoogle Scholar
Van Weelden, S. W., Van Hellemond, J. J., Opperdoes, F. R. and Tielens, A. G. (2005). New functions for parts of the Krebs cycle in procyclic Trypanosoma brucei, a cycle not operating as a cycle. Journal of Biological Chemistry 280, 12451–12460.CrossRefGoogle Scholar
Vickerman, K. (1985). Developmental cycles and biology of pathogenic trypanosomes. British Medical Bulletin 41, 105–114.CrossRefGoogle ScholarPubMed
Williams, B. A., Hirt, R. P., Lucocq, J. M. and Embley, T. M. (2002). A mitochondrial remnant in the microsporidian Trachipleistophora hominis. Nature 418, 865–869.CrossRefGoogle ScholarPubMed
Williams, K., Lowe, P. N. and Leadlay, P. F. (1987). Purification and characterization of pyruvate: ferredoxin oxidoreductase from the anaerobic protozoon Trichomonas vaginalis. Biochemical Journal 246, 529–536.CrossRefGoogle ScholarPubMed
Wojtczak, L. (1996). The Crabtree effect: a new look at the old problem. Acta Biochimica Polonica 43, 361–368.CrossRefGoogle Scholar
Wolfe, A. J. (2005). The acetate switch. Microbiology and Molecular Biology Reviews 69, 12–50.CrossRefGoogle ScholarPubMed
World Health Organization (1997). Entamoeba taxonomy. Bulletin of the World Health Organization 75, 291–292.Google Scholar
World Health Organization (2006). The global burden of disease: 2004 update. http://www.who.int/healthinfo/global_burden_disease/2004_report_update/en/Google Scholar
Ximenez, C., Moran, P., Rojas, L., Valadez, A. and Gomez, A. (2009). Reassessment of the epidemiology of amebiasis: State of the art. Infection, Genetics and Evolution. In press PMID: 16103593.CrossRefGoogle ScholarPubMed
Zikova, A., Schnaufer, A., Dalley, R. A., Panigrahi, A. K. and Stuart, K. D. (2009). The F(0)F(1)-ATP synthase complex contains novel subunits and is essential for procyclic Trypanosoma brucei. PLoS Pathogens 5, e1000436.CrossRefGoogle Scholar