Previous Article | Next Article 
Journal of Bacteriology, February 2004, p. 683-691, Vol. 186, No. 3
0021-9193/04/$08.00+0 DOI: 10.1128/JB.186.3.683-691.2004
Copyright © 2004, American Society for Microbiology. All Rights Reserved.
ATP/ADP Translocases: a Common Feature of Obligate Intracellular Amoebal Symbionts Related to Chlamydiae and Rickettsiae
Stephan Schmitz-Esser,1 Nicole Linka,2 Astrid Collingro,1 Cora L. Beier,3 H. Ekkehard Neuhaus,2 Michael Wagner,1 and Matthias Horn1*
Abteilung Mikrobielle Ökologie, Universität Wien, A-1090 Vienna, Austria,1
Abteilung Planzenphysiologie, Universität Kaiserslautern, D-67653 Kaiserslautern,2
Institut für Humangenetik, Technische Universität München, D-81675 Munich, Germany3
Received 14 September 2003/
Accepted 8 October 2003
ATP/ADP translocases catalyze the highly specific transport of ATP across a membrane in an exchange mode with ADP. Such unique transport proteins are employed by plant plastids and have among the prokaryotes so far only been identified in few obligate intracellular bacteria belonging to the Chlamydiales and the Rickettsiales. In this study, 12 phylogenetically diverse bacterial endosymbionts of free-living amoebae and paramecia were screened for the presence of genes encoding ATP/ADP transport proteins. The occurrence of ATP/ADP translocase genes was found to be restricted to endosymbionts related to rickettsiae and chlamydiae. We showed that the ATP/ADP transport protein of the Parachlamydia-related endosymbiont of Acanthamoeba sp. strain UWE25, a recently identified relative of the important human pathogens Chlamydia trachomatis and Chlamydophila pneumoniae, is functional when expressed in the heterologous host Escherichia coli and demonstrated the presence of transcripts during the chlamydial developmental cycle. These findings indicate that the interaction between Parachlamydia-related endosymbionts and their amoeba hosts concerns energy parasitism similar to the interaction between pathogenic chlamydiae and their human host cells. Phylogenetic analysis of all known ATP/ADP translocases indicated that the genes encoding ATP/ADP translocases originated from a chlamydial ancestor and were, after an ancient gene duplication, transferred horizontally to rickettsiae and plants.
* Corresponding author. Mailing address: Abteilung Mikrobielle Ökologie, Institut für Ökologie und Naturschutz, Universität Wien, Althanstr. 14, A-1090 Vienna, Austria. Phone: 43 1 4277 54393. Fax: 43 1 4277 54389. E-mail:
horn{at}microbial-ecology.net.
Journal of Bacteriology, February 2004, p. 683-691, Vol. 186, No. 3
0021-9193/04/$08.00+0 DOI: 10.1128/JB.186.3.683-691.2004
Copyright © 2004, American Society for Microbiology. All Rights Reserved.
This article has been cited by other articles:
-
Fournier, G. P., Huang, J., Gogarten, J. P.
(2009). Horizontal gene transfer from extinct and extant lineages: biological innovation and the coral of life.. Phil Trans R Soc B
364: 2229-2239
[Abstract]
[Full Text]
-
Mukhopadhyay, S., Akmal, A., Stewart, A. C., Hsia, R.-c., Read, T. D.
(2009). Identification of Bacillus anthracis Spore Component Antigens Conserved across Diverse Bacillus cereus sensu lato Strains. Mol. Cell. Proteomics
8: 1174-1191
[Abstract]
[Full Text]
-
Ast, M., Gruber, A., Schmitz-Esser, S., Neuhaus, H. E., Kroth, P. G., Horn, M., Haferkamp, I.
(2009). Diatom plastids depend on nucleotide import from the cytosol. Proc. Natl. Acad. Sci. USA
106: 3621-3626
[Abstract]
[Full Text]
-
Trentmann, O., Jung, B., Neuhaus, H. E., Haferkamp, I.
(2008). Nonmitochondrial ATP/ADP Transporters Accept Phosphate as Third Substrate. J. Biol. Chem.
283: 36486-36493
[Abstract]
[Full Text]
-
Schmitz-Esser, S., Haferkamp, I., Knab, S., Penz, T., Ast, M., Kohl, C., Wagner, M., Horn, M.
(2008). Lawsonia intracellularis Contains a Gene Encoding a Functional Rickettsia-Like ATP/ADP Translocase for Host Exploitation. J. Bacteriol.
190: 5746-5752
[Abstract]
[Full Text]
-
Wang, G., Burczynski, F., Anderson, J., Zhong, G.
(2007). Effect of host fatty acid-binding protein and fatty acid uptake on growth of Chlamydia trachomatis L2. Microbiology
153: 1935-1939
[Abstract]
[Full Text]
-
Abergel, C., Blanc, G., Monchois, V., Renesto, P., Sigoillot, C., Ogata, H., Raoult, D., Claverie, J.-M.
(2006). Impact of the Excision of an Ancient Repeat Insertion on Rickettsia conorii Guanylate Kinase Activity. Mol Biol Evol
23: 2112-2122
[Abstract]
[Full Text]
-
Audia, J. P., Winkler, H. H.
(2006). Study of the Five Rickettsia prowazekii Proteins Annotated as ATP/ADP Translocases (Tlc): Only Tlc1 Transports ATP/ADP, While Tlc4 and Tlc5 Transport Other Ribonucleotides.. J. Bacteriol.
188: 6261-6268
[Abstract]
[Full Text]
-
Collingro, A., Toenshoff, E. R., Taylor, M. W., Fritsche, T. R., Wagner, M., Horn, M.
(2005). 'Candidatus Protochlamydia amoebophila', an endosymbiont of Acanthamoeba spp.. Int. J. Syst. Evol. Microbiol.
55: 1863-1866
[Abstract]
[Full Text]
-
Molmeret, M., Horn, M., Wagner, M., Santic, M., Abu Kwaik, Y.
(2005). Amoebae as Training Grounds for Intracellular Bacterial Pathogens. Appl. Environ. Microbiol.
71: 20-28
[Full Text]
-
Horn, M., Collingro, A., Schmitz-Esser, S., Beier, C. L., Purkhold, U., Fartmann, B., Brandt, P., Nyakatura, G. J., Droege, M., Frishman, D., Rattei, T., Mewes, H.-W., Wagner, M.
(2004). Illuminating the Evolutionary History of Chlamydiae. Science
304: 728-730
[Abstract]
[Full Text]