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

Published online by Cambridge University Press:  27 August 2014

A. C. AZEVEDO-MARTINS ,
A. C. L. MACHADO ,
C. C. KLEIN ,
L. CIAPINA ,
L. GONZAGA ,
A. T. R. VASCONCELOS ,
M. F. SAGOT ,
W. DE SOUZA ,
M. EINICKER-LAMAS  and
A. GALINA
...Show all authors
A. C. AZEVEDO-MARTINS
Affiliation:
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 Instituto Nacional de Ciência e Tecnologia em Biologia Estrutural e Bioimagens, Brasil
A. C. L. MACHADO
Affiliation:
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 Instituto Nacional de Ciência e Tecnologia em Biologia Estrutural e Bioimagens, Brasil
C. C. KLEIN
Affiliation:
BAMBOO Team, INRIA Grenoble-Rhône-Alpes, Villeurbanne, France Laboratoire de Biométrie et Biologie Evolutive, Université de Lyon, Université Lyon 1, CNRS, UMR5558, Villeurbanne, France
L. CIAPINA
Affiliation:
Laboratório Nacional de Computação Científica, Av. Getúlio Vargas, 333, Quitandinha, Petrópolis, RJ, CEP: 25651-075, Brasil
L. GONZAGA
Affiliation:
Laboratório Nacional de Computação Científica, Av. Getúlio Vargas, 333, Quitandinha, Petrópolis, RJ, CEP: 25651-075, Brasil
A. T. R. VASCONCELOS
Affiliation:
Laboratório Nacional de Computação Científica, Av. Getúlio Vargas, 333, Quitandinha, Petrópolis, RJ, CEP: 25651-075, Brasil
M. F. SAGOT
Affiliation:
BAMBOO Team, INRIA Grenoble-Rhône-Alpes, Villeurbanne, France Laboratoire de Biométrie et Biologie Evolutive, Université de Lyon, Université Lyon 1, CNRS, UMR5558, Villeurbanne, France
W. DE SOUZA
Affiliation:
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 Instituto Nacional de Ciência e Tecnologia em Biologia Estrutural e Bioimagens, Brasil Instituto Nacional de Metrologia, Qualidade e Tecnologia – Inmetro, Rio de Janeiro, RJ, Brasil
M. EINICKER-LAMAS
Affiliation:
Laboratório Intermediário de Biomembranas, Instituto de Biofísica Carlos Chagas Filho, Centro de Ciências da Saúde, Universidade Federal do Rio de Janeiro, UFRJ, Avenida Carlos Chagas Filho, 343, Bloco C, Cidade Universitária, Ilha do Fundão, Rio de Janeiro, CEP 21941-590, Brasil
A. GALINA*
Affiliation:
Laboratório de Bioenergética e Fisiologia Mitocondrial, Programa de Biofísica e Bioquímica Celular, Instituto de Bioquímica Médica, Centro de Ciências da Saúde, Universidade Federal do Rio de Janeiro, UFRJ, Avenida Carlos Chagas Filho, 343, Bloco D SS sala 13, Cidade Universitária, Ilha do Fundão, Rio de Janeiro, CEP 21941-590, Brasil
M. C. M. MOTTA*
Affiliation:
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 Instituto Nacional de Ciência e Tecnologia em Biologia Estrutural e Bioimagens, Brasil
*
*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: motta@biof.ufrj.br; A. Galina: E-mail: galina@bioqmed.ufrj.br
*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: motta@biof.ufrj.br; A. Galina: E-mail: galina@bioqmed.ufrj.br
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Summary

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.

Keywords

Symbiosistrypanosomatidsbioenergeticselectron transfer complexevolution
Type
Research Article
Information
Parasitology , Volume 142 , Issue 2 , February 2015 , pp. 352 - 362
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Copyright © Cambridge University Press 2014 

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