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Mitochondrial respiration and genomic analysis provide insight into the influence of the symbiotic bacterium on host trypanosomatid oxygen consumption

  • A. C. AZEVEDO-MARTINS (a1) (a2), A. C. L. MACHADO (a1) (a2), C. C. KLEIN (a3) (a4), L. CIAPINA (a5), L. GONZAGA (a5), A. T. R. VASCONCELOS (a5), M. F. SAGOT (a3) (a4), W. DE SOUZA (a1) (a2) (a6), M. EINICKER-LAMAS (a7), A. GALINA (a8) and M. C. M. MOTTA (a1) (a2)...


Certain trypanosomatids co-evolve with an endosymbiotic bacterium in a mutualistic relationship that is characterized by intense metabolic exchanges. Symbionts were able to respire for up to 4 h after isolation from Angomonas deanei. FCCP (carbonyl cyanide-4-(trifluoromethoxy)phenylhydrazone) similarly increased respiration in wild-type and aposymbiotic protozoa, though a higher maximal O2 consumption capacity was observed in the symbiont-containing cells. Rotenone, a complex I inhibitor, did not affect A. deanei respiration, whereas TTFA (thenoyltrifluoroacetone), a complex II activity inhibitor, completely blocked respiration in both strains. Antimycin A and cyanide, inhibitors of complexes III and IV, respectively, abolished O2 consumption, but the aposymbiotic protozoa were more sensitive to both compounds. Oligomycin did not affect cell respiration, whereas carboxyatractyloside (CAT), an inhibitor of the ADP-ATP translocator, slightly reduced O2 consumption. In the A. deanei genome, sequences encoding most proteins of the respiratory chain are present. The symbiont genome lost part of the electron transport system (ETS), but complex I, a cytochrome d oxidase, and FoF1-ATP synthase remain. In conclusion, this work suggests that the symbiont influences the mitochondrial respiration of the host protozoan.


Corresponding author

* Corresponding authors: M.C.M. Motta: Laboratório de Ultraestrutura Celular Hertha Meyer, Instituto de Biofísica Carlos Chagas Filho, Centro de Ciências da Saúde, Universidade Federal do Rio de Janeiro, UFRJ, Avenida Carlos Chagas Filho, 343, Bloco G, Subsolo, Cidade Universitária, Ilha do Fundão, Rio de Janeiro, CEP 21941-590, Brasil. E-mail:; A. Galina: E-mail:


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Acestor, N., Zíková, A., Dalley, R. A., Anupama, A., Panigrahi, A. K. and Kenneth, D. S. (2011). Trypanosoma brucei mitochondrial respiratome: composition and organization in procyclic form. Molecular Cell Proteomics 10, M110.006908.
Alves, J. M. P., Voegtly, L., Matveyev, A. V., Lara, A. M., Silva, F. M., Serrano, M. G., Buck, G. A., Teixeira, M. M. G. and Camargo, E. P. (2011). Identification and phylogenetic analysis of heme synthesis genes in trypanosomatids and their bacterial endosymbionts. PLOS ONE 6, e23518.
Alves, J. M., Klein, C. C., da Silva, F. M., Costa-Martins, A. G., Serrano, M. G., Buck, G. A., Vasconcelos, A. T., Sagot, M. F., Teixeira, M. M., Motta, M. C. M. and Camargo, E. P. (2013 a). Endosymbiosis in trypanosomatids: the genomic cooperation between bacterium and host in the synthesis of essential amino acids is heavily influenced by multiple horizontal gene transfers. BMC Evolutionary Biology 13, 190. doi: 10.1186/1471-2148-13-190.
Alves, J. M., Serrano, M. G., Maia da Silva, F., Voegtly, L. J., Matveyev, A. V., Teixeira, M. M., Camargo, E. P. and Buck, G. A. (2013 b). Genome evolution and phylogenomic analysis of Candidatus Kinetoplastibacterium, the betaproteobacterial endosymbionts of Strigomonas and Angomonas. PLOS ONE 5, 338350. doi: 10.1093/gbe/evt012.
Aslett, M., Aurrecoechea, C., Berriman, M., Brestelli, J., Brunk, B. P., Carrington, M., Depledge, D. P., Fisher, S., Gajria, B., Gao, X., Gardner, M. J., Gingle, A., Grant, G., Harb, O. S., Heiges, M., Hertz-Fowler, C., Houston, R., Innamorato, F., Iodice, J., Kissinger, J. C., Kraemer, E., Li, W., Logan, F. J., Miller, J. A., Mitra, S., Myler, P. J., Nayak, V., Pennington, C., Phan, I., Pinney, D. F., Ramasamy, G., Rogers, M. B., Roos, D. S., Ross, C., Sivam, D., Smith, D. F., Srinivasamoorthy, G., Stoeckert, C. J., Subramanian, S., Thibodeau, R., Tivey, A., Tratman, C., Velarde, G. and Wang, H. (2010). TriTryDB: a functional genomic resource for the Trypanosomatidae. Nucleic Acids Research 38, D457D463. doi: 10.1093/nar/gkp851.
Azevedo-Martins, A. C., Frossard, M. L., de Souza, W., Einicker-Lamas, M. and Motta, M. C. M. (2007). Phosphatidylcholine synthesis in Crithidia deanei: the influence of the endosymbiont. FEMS Microbiology Letters 275, 229236.
Belevich, I. and Verkhovsky, M. I. (2008). Molecular mechanism of proton translocation by cytochrome c oxidase. Antioxidants and Redox Signaling 10, 129.
Bernard, G., Faustin, B., Passerieux, E., Galinier, A., Rocher, C., Bellance, N., Delage, J. -P., Casteilla, L., Letellier, T. and Rossignol, R. (2006). Physiological diversity of mitochondrial oxidative phosphorylation. American Journal of Physiology Cell Physiology 291, C1172C1182.
Brandt, U. (2006). Energy converting NADH:quinone oxidoreductase (complex I). Annual Review in Biochemistry 75, 6992.
Camargo, E. P. and Freymüller, E. (1977). Endosymbiont as supplier of ornithine carbamoyltransferase in a trypanosomatid. Nature 270, 5253.
Chang, K. P., Chang, C. S. and Sassa, S. (1975). Heme biosynthesis in bacterium-protozoon symbioses: enzymic defects in host hemofagellates and complemental role of their intracellular symbiotes. Proceedings of the National Academy of Sciences USA 72, 29792983.
Dean, S., Gould, M. K., Dewar, C. E. and Schnaufer, A. C. (2013). Single point mutations in ATP synthase compensate for mitochondrial loss in trypanosomatids. Proceedings of the National Academy of Sciences USA 110, 1474114746.
Du, Y., McLaughlin, G. and Chang, K. P. (1994). 16S ribosomal DNA sequence identies of β- proteobacterial endosymbionts in three Crithidia species. Journal of Bacteriology 176, 30813084.
Edwards, C. and Chance, C. (1982). Evidence for the presence of two terminal oxidases in the trypanosomatid Crithidia oncopelti . Journal of General Microbiology 128, 14091414.
Esteves, M. J. G., Andrade, A. F. B., Angluster, J., de Souza, W., Mundim, M. H., Roitman, I. and Pereira, M. E. A. (1982). Cell surface carbohydrates in Crithidia deanei: influence of the endosymbiont. European Journal of Cell Biology 28, 244248.
Fiorini, J. E., Faria e Silva, P. M., Soares, M. J. and Brasil, R. P. (1989). Três novas espécies de tripanosomatídeos de insetos isolados em Alfenas, Minas Gerais, Brasil. Memórias do Instituto Oswaldo Cruz 84, 6974.
Freymuller, J. E. and Camargo, E. P. (1981). Ultrastructural differences between species of trypanosomatids with and without endosymbionts. Journal of Protozoology 28, 175182.
Frossard, M. L., Seabra, S. H., DaMatta, R. A., de Souza, W., de Mello, F. G. and Motta, M. C. M. (2006). An endosymbiont positively modulates ornithine decarboxylase in host trypanosomatids. Biochemical and Biophysical Research Communications 343, 443449.
Galinari, S. and Camargo, E. P. (1978). Trypanosomatid protozoa: survey of acetylornithinase and ornithine acetyltransferase. Experimental Parasitology 46, 277282.
Grigorieff, N. (1999). Structure of the NADH:quinone oxidoreductase (complex I). Current Opinion in Structural Biology 9, 476483.
Guénebaut, V., Schlitt, A., Weiss, H., Leonard, K. and Friedrich, T. (1998). Consistent structure between bacterial and mitochondrial NADH:quinone oxidoreductase (complex I). Journal of Molecular Biology 276, 105112.
Hatch, T. P., Al-Hossainy, E. and Silverman, J. A. (1982). Adenine nucleoside and lysine transport in Chlamydia psittaci . Journal of Bacteriology 150, 662670.
Herby, O. and Persson, L. (1990). Molecular genetics of polyamine synthesis in eukaryotic cells. Trends Biochemistry Sciences 15, 153158.
Klein, C. C., Alves, J. M., Serrano, M. G., Buck, G. A., Vasconcelos, A. T., Sagot, M. F., Teixeira, M. M., Camargo, E. P. and Motta, M. C. M. (2013). Biosynthesis of vitamins and cofactors in bacterium-harbouring trypanosomatids depends on the symbiotic association as revealed by genomic analyses. PLOS ONE 8, e79786. doi: 10.1371/journal.pone.0079786.
Kronick, P. and Hill, G. C. (1974). Evidence for the functioning of cytochrome o in kinetoplastida. Biochimica Biophysica Acta 368, 173180.
Lenaz, G. and Genova, M. L. (2009). Structural and functional organization of the mitochondrial respiratory chain: a dynamic super-assembly. International Journal of Biochemistry and Cell Biology 41, 17501772.
Morales, J., Mogi, T., Mineki, S., Takashima, E., Mineki, R., Hirawake, H., Sakamoto, K., Ōmura, S. and Kita, K. (2009). Novel mitochondrial Complex II isolated from Trypanosoma cruzi is composed of 12 peptides including a heterodimeric Ip subunit. Journal of Biological Chemistry 284, 72557263.
Motta, M. C. M. (2010). Endosymbiosis in trypanosomatids as a model to study cell evolution. Open Parasitology Journal 4, 139147.
Motta, M. C. M., Monteiro-Leal, L. H., de Souza, W., Almeida, D. F. and Ferreira, L. C. S. (1997 a). Detection of penicilin-binding proteins in endosymbiosis of the trypanosomatid Crithidia deanei . Journal of Eukaryotic Microbiology 44, 492496.
Motta, M. C. M., Soares, M. J., Attias, M., Morgado, J., Lemos, A. P., Saad-Nehme, J., Meyer-Fernandes, J. R. and De Souza, W. (1997 b). Ultrastructural and biochemical analysis of the relationship of Crithidia deanei with its endosymbiont. European Journal of Cellular Biology 72, 370377.
Motta, M. C., Martins, A. C., de Souza, S. S., Catta-Preta, C. M., Silva, R., Klein, C. C., de Almeida, L. G., de Lima Cunha, O., Ciapina, L. P., Brocchi, M., Colabardini, A. C., de Araujo Lima, B., Machado, C. R., de Almeida Soares, C. M., Probst, C. M., de Menezes, C. B., Thompson, C. E., Bartholomeu, D. C., Gradia, D. F., Pavoni, D. P., Grisard, E. C., Fantinatti-Garboggini, F., Marchini, F. K., Rodrigues-Luiz, G. F., Wagner, G., Goldman, G. H., Fietto, J. L., Elias, M. C., Goldman, M. H., Sagot, M. F., Pereira, M., Stoco, P. H., de Mendonça-Neto, R. P., Teixeira, S. M., Maciel, T. E., de Oliveira Mendes, T. A., Ürményi, T. P., de Souza, W., Schenkman, S. and de Vasconcelos, A. T. (2013). Predicting the proteins of Angomonas deanei, Strigomonas culicis and their respective endosymbionts reveals new aspects of the trypanosomatidae family. PLOS ONE 8, e60209. doi: 10.1371/journal.pone.0060209.
Mundim, M. H. and Roitman, I. (1977). Extra nutritional requirements of artificially aposymbiotic Crithidia deanei . Journal of Protozoology 24, 329331.
Mundim, M. H., Roitman, I., Hermans, M. A. and Kitajima, E. W. (1974). Simple nutrition of Crithidia deanei, a reduviid trypanosomatid with an endosymbiont. Journal of Protozoology 21, 518521.
Oda, L. M., Alviano, C. S., Costa e Silva Filho, F., Angluster, J., Roitman, I. and De Souza, W. (1984). Surface anionic group in symbiont-bearing and symbiont-free strains of Crithidia deanei . Journal of Protozoology 31, 131134.
Opperdoes, F. R. and Michels, P. A. (2008). Complex I of trypanosomatids: does it exist? Trends in Parasitology 24, 310317.
Palmié-Peixoto, I., Rocha, M. R., Urbina, J., De Souza, W., Einicker-Lamas, M. and Motta, M. C. M. (2006). Effects of sterol-biosynthesis inhibitors on endosymbiont-bearing trypanosomatids. FEMS Microbiology Letters 255, 3342.
Schägger, H. (2001). Respiratory supercomplexes. IUBMB Life 52, 119128.
Speijer, D., Breek, C. K. D., Muijsers, A. O., Groenevelt, P. X., Dekker, H., De Haan, A. and Benne, R. (1996). The sequence of a small subunit of cytochrome c oxidase from Crithidia fasciculata which is homologous to mammalian subunit IV. FEBS Letters 381, 123126.
Strauss, M., Hofhaus, G., Schöder, R. R. and Kühlbrandt, W. (2008). Dimer ribbons of ATP synthase shape the inner mitochondrial membrane. EMBO Journal 27, 11541160.
Teixeira, M. M. G., Borghesan, T. C., Ferreira, R. C., Santos, M. A., Takata, C. S. A., Campaner, M., Nunes, V. L. B., Wilder, R. V., De Souza, W. and Camargo, E. P. (2011). Phylogenetic validation of the genera Angomonas and Strigomonas of trypanosomatids harboring bacterial endosymbionts with the description of new species of trypanosomatids and of proteobacterial symbionts. Protist 162, 503524.
Warren, L. G. (1960). Metabolism of Schizotrypanum cruzi, Chagas. I. Effect of culture age and substrate concentration on respiratory rate. Journal of Parasitology 46, 529539.
Winkler, H. H. (1976). Rickettsial permeability. An ADP-ATP transport system. Journal of Biological Chemistry 251, 389396.
World Health Organization (2007). Update of American trypanosomiasis and leishmania control and research: final report. Pan American Health Organization/World Health Organization, Rio de Janeiro.


Mitochondrial respiration and genomic analysis provide insight into the influence of the symbiotic bacterium on host trypanosomatid oxygen consumption

  • A. C. AZEVEDO-MARTINS (a1) (a2), A. C. L. MACHADO (a1) (a2), C. C. KLEIN (a3) (a4), L. CIAPINA (a5), L. GONZAGA (a5), A. T. R. VASCONCELOS (a5), M. F. SAGOT (a3) (a4), W. DE SOUZA (a1) (a2) (a6), M. EINICKER-LAMAS (a7), A. GALINA (a8) and M. C. M. MOTTA (a1) (a2)...


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