Lawsonia intracellularis contains a gene encoding a functional rickettsia-like ATP/ADP translocase for host exploitation

Journal of Bacteriology

Volumn 190, Issue 17, 2008, Pages 5746-5752

  Schmitz Esser, Stephan ^a   Haferkamp, Ilka ^b   Knab, Silvia ^a   Penz, Thomas ^a   Ast, Michelle ^b   Kohl, Christian ^b   Wagner, Michael ^a   Horn, Matthias ^a  

^a UNIVERSITY OF VIENNA   (Austria)

^b Rheinland Pfälzische Technische Universität Kaiserslautern Landau   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATE; CARRIER PROTEIN; NUCLEOTIDE TRANSPORTER; NUCLEOTIDE TRANSPORTER 1; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ARTICLE; BACTERIAL GENE; CHLAMYDIA; CONTROLLED STUDY; ENERGY; ESCHERICHIA COLI; GENE EXPRESSION; GENE TRANSFER; HOST; ISOTOPE LABELING; LAWSONIA; LAWSONIA INTRACELLULARIS; MOLECULAR CLONING; NONHUMAN; NUCLEOTIDE SEQUENCE; PARASITISM; PRIORITY JOURNAL; PROTEIN TRANSPORT; RICKETTSIA; RICKETTSIALES;

ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATE; BACTERIAL PROTEINS; BIOLOGICAL TRANSPORT; CHROMATOGRAPHY, THIN LAYER; ESCHERICHIA COLI; EUKARYOTIC CELLS; GENE TRANSFER, HORIZONTAL; HOST-PATHOGEN INTERACTIONS; KINETICS; LAWSONIA BACTERIA; MITOCHONDRIAL ADP, ATP TRANSLOCASES; MOLECULAR SEQUENCE DATA; PHYLOGENY; POLYMERASE CHAIN REACTION; RICKETTSIA; SUBSTRATE SPECIFICITY;

BACTERIA (MICROORGANISMS); CHLAMYDIAE; DELTAPROTEOBACTERIA; ESCHERICHIA COLI; LAWSONIA INTRACELLULARIS; RICKETTSIA; RICKETTSIACEAE; RICKETTSIALES; SUIDAE;

EID: 50249140106     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.00391-08     Document Type: Article

References (58)

1. Alexeyev, M. F., and H. H. Winkler. 1999. Membrane topology of the Rickettsia prowazekii ATP/ADP translocase revealed by novel dual pho-lac reporters. J. Mol. Biol. 285:1503-1513.
2. Altschul, S. F., W. Gish, W. Miller, E. W. Meyers, and D. J. Lipman. 1990. Basic local alignment search tool. J. Mol. Biol. 215:403-410.
3. Amiri, H., O. Karlberg, and S. E. Andersson. 2003. Deep origin of plastid/parasite ATP/ADP translocases. J. Mol. Evol. 56:137-150.
4. Andersson, S. G., A. Zomorodipour, J. O. Andersson, T. Sicheritz-Ponten, U. C. Alsmark, R. M. Podowski, A. K. Naslund, A. S. Eriksson, H. H. Winkler, and C. G. Kurland. 1998. The genome sequence of Rickettsia prowazekii and the origin of mitochondria. Nature 396:133-140.
5. Arai, M., H. Mitsuke, M. Ikeda, J. X. Xia, T. Kikuchi, M. Satake, and T. Shimizu. 2004. ConPred II: a consensus prediction method for obtaining transmembrane topology models with high reliability. Nucleic Acids Res. 32:W390-W393.
6. Audia, J. P., and H. H. Winkler. 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.
7. Battistuzzi, F. U., A. Feijao, and S. B. Hedges. 2004. A genomic timescale of prokaryote evolution: insights into the origin of methanogenesis, phototrophy, and the colonization of land. BMC Evol. Biol. 4:44.
8. Casson, N., R. Michel, R. D. Mueller, and G. Greub. 2008. Protochlamydia naegleriophila as etiologic agent of pneumonia. Emerg. Infect. Dis. 14:168-172.
9. Collingro, A., E. R. Toenshoff, M. W. Taylor, T. R. Fritsche, M. Wagner, and M. Horn. 2005. 'Candidatus Protochiamydia amoebophila', an endosymbiont of Acanthamoeba spp. Int. J. Syst. Evol. Microbiol. 55:1863-1866.
10. Daugherty, R. M., N. Linka, J. P. Audia, C. Urbany, H. E. Neuhaus, and H. H. Winkler. 2004. The nucleotide transporter of Caedibacter caryophilus exhibits an extended substrate spectrum compared to the analogous ATP/ADP translocase of Rickettsia prowazekii. J. Bacteriol. 186:3262-3265.
11. Devereux, R., S. H. He, C. L. Doyle, S. Orkland, D. A. Stahl, J. LeGall, and W. B. Whitman. 1990. Diversity and origin of Desulfovibrio species: phylogenetic definition of a family. J. Bacteriol. 172:3609-3619.
12. Felsenstein, J. 1989. PHYLIP - phylogeny inference package (version 3.2). Cladistics 5:164-166.
13. Feng, D. F., G. Cho, and R. F. Doolittle. 1997. Determining divergence times with a protein clock: update and reevaluation. Proc. Natl. Acad. Sci. USA 94:13028-13033.
14. Fuxelius, H. H., A. Darby, C. K. Min, N. H. Cho, and S. G. Andersson. 2007. The genomic and metabolic diversity of Rickettsia. Res. Microbiol. 158:745-753.
15. Greub, G., and D. Raoult. 2003. History of the ADP/ATP-translocase-encoding gene, a parasitism gene transferred from a Chlamydiales ancestor to plants 1 billion years ago. Appl. Environ. Microbiol. 69:5530-5535.
16. + transporter in an intracellular bacterial symbiont related to Chlamydiae. Nature 432:622-625.
17. Haferkamp, I., S. Schmitz-Esser, M. Wagner, N. Neigel, M. Horn, and H. E. Neuhaus. 2006. Tapping the nucleotide pool of the host: novel nucleotide carrier proteins of Protochlamydia amoebophila. Mol. Microbiol. 60:1534-1545.
18. Horn, M. 12 May 2008, posting date. Chlamydiae as symbionts in eukaryotes. Annu. Rev. Microbiol. doi:10.1146/annurev.micro.62.081307.162818.
19. Horn, M., A. Collingro, S. Schmitz-Esser, C. L. Beier, U. Purkhold, B. Fartmann, P. Brandt, G. J. Nyakatura, M. Droege, D. Frishman, T. Rattei, H. W. Mewes, and M. Wagner. 2004. Illuminating the evolutionary history of chlamydiae. Science 304:728-730.
20. Huang, J., and J. P. Gogarten. 2007. Did an ancient chlamydial endosymbiosis facilitate the establishment of primary plastids? Genome Biol. 8:R99.
21. Iliffe-Lee, E. R., and G. McClarty. 1999. Glucose metabolism in Chlamydia trachomatis: the 'energy parasite' hypothesis revisited. Mol. Microbiol. 33: 177-187.
22. Joseph, B., and W. Goebel. 2007. Life of Listeria monocytogenes in the host cells' cytosol. Microbes Infect. 9:1188-1195.
23. Kanehisa, M., S. Goto, S. Kawashima, Y. Okuno, and M. Hattori. 2004. The KEGG resource for deciphering the genome. Nucleic Acids Res. 32:D277-D280.
24. Katoh, K., K. Kuma, H. Toh, and T. Miyata. 2005. MAFFT version 5: improvement in accuracy of multiple sequence alignment. Nucleic Acids Res. 33:511-518.
25. Klingenberg, M. 1989. Molecular aspects of the adenine nucleotide carrier from mitochondria. Arch. Biochem. Biophys. 270:1-14.
26. Krause, D. C., H. H. Winkler, and D. O. Wood. 1985. Cloning and expression of the Rickettsia prowazekii ADP/ATP translocator in Escherichia coli. Proc. Natl. Acad. Sci. USA 82:3015-3019.
27. Kroll, J. J., M. B. Roof, L. J. Hoffman, J. S. Dickson, and D. L. Harris. 2005. Proliferative enteropathy: a global enteric disease of pigs caused by Lawsonia intracellularis. Anim. Health Res. Rev. 6:173-197.
28. Lawrence, J. G., and H. Ochman. 1997. Amelioration of bacterial genomes: rates of change and exchange. J. Mol. Evol. 44:383-397.
29. Lawson, G. H., and C. J. Gebhart. 2000. Proliferative enteropathy. J. Comp. Pathol. 122:77-100.
30. Linka, N., H. Hurka, B. F. Lang, G. Burger, H. H. Winkler, C. Stamme, C. Urbany, I. Seil, J. Kusch, and H. E. Neuhaus. 2003. Phylogenetic relationships of non-mitochondrial nucleotide transport proteins in bacteria and eukaryotes. Gene 306:27-35.
31. 1. Ludwig, W., O. Strunk, R. Westram, L. Richter, H. Meier, Yadhukumar, A. Buchner, T. Lai, S. Steppi, G. Jobb, W. Forster, I. Brettske, S. Gerber, A. W. Ginhart, O. Gross, S. Grumann, S. Hermann, R. Jost, A. Konig, T. Liss, R. Lussmann, M. May, B. Nonhoff, B. Reichel, R. Strehlow, A. Stamatakis, N. Stuckmann, A. Vilbig, M. Lenke, T. Ludwig, A. Bode, and K. H. Schleifer. 2004. ARB: a Software environment for sequence data. Nucleic Acids Res. 32:1363-1371.
32. Mangold, H. K. 1967. Dünnschicht Chromatographie. Ein Laboratoriumshandbuch. Springer, Heidelberg, Germany.
33. Markowitz, V. M., F. Korzeniewski, K. Palaniappan, E. Szeto, G. Werner, A. Padki, X. Zhao, I. Dubchak, P. Hugenholtz, I. Anderson, A. Lykidis, K. Mavromatis, N. Ivanova, and N. C. Kyrpides. 2006. The integrated microbial genomes (IMG) system. Nucleic Acids Res. 34:D344-D348.
34. Mauch, C.-P., and G. Bilkei. 2005. Reproductive performance of gilts following an outbreak of acute proliferative enteropathy due to Lawsonia intracellularis. Vet. J. 170:128-131.
35. McClarty, G. 1999. Chlamydial metabolism as inferred from the complete genome sequence, p. 69-100. In R. S. Stephens (ed.), Chlamydia. American Society for Microbiology, Washington, DC.
36. McOrist, S. 2005. Defining the full costs of endemic porcine proliferative enteropathy. Vet. J. 170:8-9.
37. McOrist, S., C. J. Gebhart, R. Boid, and S. M. Barns. 1995. Characterization of Lawsonia intracellularis gen. nov., sp. nov., the obligately intracellular bacterium of porcine proliferative enteropathy. Int. J. Syst. Bacteriol. 45: 820-825.
38. Mewes, H. W., S. Dietmann, D. Frishman, R. Gregory, G. Mannhaupt, K. F. Mayer, M. Munsterkotter, A. Ruepp, M. Spannagl, V. Stumpflen, and T. Rattei. 2008. MIPS: analysis and annotation of genome information in 2007. Nucleic Acids Res. 36:D196-D201.
39. Neuhaus, H. E., E. Thom, T. Mohlmann, M. Steup, and K. Kampfenkel. 1997. Characterization of a novel eukaryotic ATP/ADP translocator located in the plastid envelope of Arabidopsis thaliana L. Plant J. 11:73-82.
40. Ochman, H., S. Elwyn, and N. A. Moran. 1999. Calibrating bacterial evolution. Proc. Natl. Acad. Sci. USA 96:12638-12643.
41. Palmieri, L., H. Rottensteiner, W. Girzalsky, P. Scarcia, F. Palmieri, and R. Erdmann. 2001. Identification and functional reconstitution of the yeast peroxisomal adenine nucleotide transporter. EMBO J. 20:5049-5059.
42. Ren, Q., K. H. Kang, and I. T. Paulsen. 2004. TransportDB: a relational database of cellular membrane transport systems. Nucleic Acids Res. 32(Database issue):D284-D288.
43. Saier, M. H., Jr. 2000. A functional-phylogenetic classification system for transmembrane solute transporters. Microbiol. Mol. Biol. Rev. 64:354-411.
44. Saier, M. H., Jr., C. V. Tran, and R. D. Barabote. 2006. TCDB: the transporter classification database for membrane transport protein analyses and information. Nucleic Acids Res. 34:D181-D186.
45. Schmitz-Esser, S., N. Linka, A. Collingro, C. L. Beier, H. E. Neuhaus, M. Wagner, and M. Horn. 2004. ATP/ADP translocases: a common feature of obligate intracellular amoebal symbionts related to chlamydiae and rickettsiae. J. Bacteriol. 186:683-691.
46. Smith, D. G., and G. H. Lawson. 2001. Lawsonia intracellularis: getting inside the pathogenesis of proliferative enteropathy. Vet. Microbiol. 82:331-345.
47. Thomas, V., N. Casson, and G. Greub. 2006. Criblamydia sequanensis, a new intracellular Chlamydiales isolated from Seine river water using amoebal co-culture. Environ. Microbiol. 8:2125-2135.
48. Thomson, N. R., M. T. Holden, C. Carder, N. Lennard, S. J. Lockey, P. Marsh, P. Skipp, C. D. O'Connor, I. Goodhead, H. Norbertzcak, B. Harris, D. Ormond, R. Rance, M. A. Quail, J. Parkhill, R. S. Stephens, and I. N. Clarke. 2008. Chlamydia trachomatis: genome sequence analysis of lymphogranuloma venereum isolates. Genome Res. 18:161-171.
49. Thomson, N. R., C. Yeats, K. Bell, M. T. Holden, S. D. Bentley, M. Livingstone, A. M. Cerdeno-Tarraga, B. Harris, J. Doggett, D. Ormond, K. Mungall, K. Clarke, T. Feltwell, Z. Hance, M. Sanders, M. A. Quail, C. Price, B. G. Barrell, J. Parkhill, and D. Longbottom. 2005. The Chlamydophila abortus genome sequence reveals an array of variable proteins that contribute to interspecies variation. Genome Res. 15:629-640.
50. Tjaden, J., T. Mohlmann, K. Kampfenkel, G. Henrichs, and H. E. Neuhaus. 1998. Altered plastidic ATP/ADP-transporter activity influences potato (Solanum tuberosum L.) tuber morphology, yield and composition of tuber starch. Plant J. 16:531-540.
51. Tjaden, J., H. H. Winkler, C. Schwoppe, M. Van Der Laan, T. Mohlmann, and H. E. Neuhaus. 1999. Two nucleotide transport proteins in Chlamydia trachomatis, one for net nucleoside triphosphate uptake and the other for transport of energy. J. Bacteriol. 181:1196-1202.
52. Trentmann, O., C. Decker, H. H. Winkler, and H. E. Neuhaus. 2000. Charged amino-acid residues in transmembrane domains of the plastidic ATP/ADP transporter from arabidopsis are important for transport efficiency, substrate specificity, and counter exchange properties. Eur. J. Biochem. 267:4098-4105.
53. Trentmann, O., M. Horn, A. C. van Scheltinga, H. E. Neuhaus, and I. Haferkamp. 2007. Enlightening energy parasitism by analysis of an ATP/ADP transporter from chlamydiae. PLoS Biol. 5:e231.
54. Tyra, H. M., M. Linka, A. P. Weber, and D. Bhattacharya. 2007. Host origin of plastid solute transporters in the first photosynthetic eukaryotes. Genome Biol. 8:R212.
55. Vandahl, B. B., S. Birkelund, and G. Christiansen. 2004. Genome and proteome analysis of Chlamydia. Proteomics 4:2831-2842.
56. Wheeler, D. L., T. Barrett, D. A. Benson, S. H. Bryant, K. Canese, V. Chetvernin, D. M. Church, M. DiCuccio, R. Edgar, S. Federhen, M. Feolo, L. Y. Geer, W. Helmberg, Y. Kapustin, O. Khovayko, D. Landsman, D. J. Lipman, T. L. Madden, D. R. Maglott, V. Miller, J. Ostell, K. D. Pruitt, G. D. Schuler, M. Shumway, E. Sequeira, S. T. Sherry, K. Sirotkin, A. Souvorov, G. Starchenko, R. L. Tatusov, T. A. Tatusova, L. Wagner, and E. Yaschenko. 2008. Database resources of the National Center for Biotechnology Information, vol. 36, p.D13-D21.
57. Winkler, H. H., and H. E. Neuhaus. 1999. Non-mitochondrial ATP transport. Trends Biochem. Sci. 24:64-68.
58. Wolf, Y. I., L. Aravind, and E. V. Koonin. 1999. Rickettsiae and chlamydiae: evidence of horizontal gene transfer and gene exchange. Trends Genet. 15:173-175.