Structure and function of the universal stress protein TeaD and its role in regulating the ectoine transporter TeaABC of halomonas elongata DSM 2581

Biochemistry

Volumn 49, Issue 10, 2010, Pages 2194-2204

  Schweikhard, Eva S ^a   Kuhlmann, Sonja I ^a   Kunte, Hans Jörg ^b,c   Grammann, Katrin ^c   Ziegler, Christine M ^a  

^a MAX PLANCK INSTITUTE OF BIOPHYSICS   (Germany)

^b BAM FEDERAL INSTITUTE FOR MATERIALS RESEARCH AND TESTING   (Germany)

^c UNIVERSITY OF BONN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVITY REGULATION; ATP BINDING; COMPATIBLE SOLUTES; DIMER COMPLEXES; DNA BINDING; ECTOINE; ENHANCED UPTAKE; GENES ENCODING; HALOMONAS ELONGATA; HALOPHILIC BACTERIA; MOLECULAR REPLACEMENTS; REGULATORY MECHANISM; ROSSMANN; STRESS PROTEIN; TRANSCRIPTIONAL REGULATION;

ENCODING (SYMBOLS); GENES; LAWS AND LEGISLATION; OLIGOMERIZATION; PROTEINS;

CRYSTAL STRUCTURE;

ABC TRANSPORTER; CARRIER PROTEIN; DIMER; ECTOINE; HEAT SHOCK PROTEIN; PROTEIN SUBUNIT; TEAABC; UNCLASSIFIED DRUG; UNIVERSAL STRESS PROTEIN TEAD;

ARTICLE; BACTERIAL STRAIN; CRYSTAL STRUCTURE; DIMERIZATION; DNA BINDING; GENE DELETION; GENE LOCUS; HALOMONAS; HALOMONAS ELONGATA; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; NONHUMAN; OLIGOMERIZATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN STRUCTURE; PROTEIN TRANSPORT; REGULATORY MECHANISM; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TRANSCRIPTION REGULATION;

ADENOSINE TRIPHOSPHATE; AMINO ACID SEQUENCE; AMINO ACID TRANSPORT SYSTEMS; AMINO ACIDS, DIAMINO; BACTERIAL PROTEINS; CRYSTALLOGRAPHY, X-RAY; GENOME, BACTERIAL; HALOMONAS; HEAT-SHOCK PROTEINS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; OSMOTIC PRESSURE; PROTEIN MULTIMERIZATION; PROTEIN STABILITY; PROTEIN STRUCTURE, QUATERNARY; SUBSTRATE SPECIFICITY; TRANSCRIPTION, GENETIC;

BACTERIA (MICROORGANISMS); HALOMONAS ELONGATA;

EID: 77949388201     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi9017522     Document Type: Article

References (38)

1. Goller, K., Ofer, A., and Galinski, E. A. (1998) Construction and characterization of an NaCl-sensitive mutant of Halomonas elongata impaired in. ectoine biosynthesis. FEMS Microbiol. Lett. 161, 293-300.
2. Brown, A. D. (1976) Microbial water stress. Bacteriol, Rev. 40, 803-846.
3. Galinski, E. A., and Truper, H. G. (1982) Betaine, a compatible solute in. the extremely halophilic phototropic bacterium Ectothiorhodospira halochloris. FEMS Microbiol. Lett. 13, 357-360.
4. Mackay, M. A., Norton, R. S., and Borowitzka, L. J. (1984) Organic osmoregulatory solutes in Cyanobacteria. J. Gen. Microbiol. 130, 2177-2191.
5. Wohlfarth, A., Severin, J., and Galinski, E. A. (1990) The spectrum of compatible solutes in heterotrophic halophilic Euhacteria of the family Halomonadaceae. J. Gen. Microbiol. 136, 705-712.
6. Grammann, K., Volke, A., and. Kunte, H. J. (2002) New type of osmoregulated solute transporter identified in halophilic members of the bacteria domain: TRAP transporter TeaABC mediates uptake of ectoine and hydroxyectoine in Halomonas elongata DSM 2581(T). LMMSlM- 184, 3078-3085.
7. Mulligan, C., Kelly, D. J., and Thomas, G. H. (2007) Tripartite ATP-independent periplasmic transporters: application of a relational database for genome-wide analysis of transporter gene frequency and organization. J. Mol. Microbiol. Biotechnol. 12, 218-226.
8. Barabote, R. D., Tamang, D. G., Abeywardena, S. N., Fallah, N. S., Fu, J. Y., Lio, J. K., Mirhosseini, P., Pezeshk, R., Podell, S., Salampessy, M. L., Thever, M. D., and Saier, M. H., Jr. (2006) Extra domains in secondary transport carriers and channel proteins. Biochim. Biophys. Acta 1758, 1557-1579.
9. Drumm, J. E., Mi, K., Bilder, P., Sun, M., Lim, J., Bielefeldt-Ohmann, H., Basaraba, R., So, M., Zhu, G., Tufariello, J. M., Izzo, A. A., Orme, I. M., Almo, S. C., Leyh, T. S., and Chan, J. (2009) Mycobacterium tuberculosis universal stress protein Rv2623 regulates bacillary growth by ATP-binding: requirement for establishing chronic persistent infection. PLoS Pathog. 5, e1000460.
10. Kvint, K., Nachin, L., Diez, A., and Nystrom, T. (2003) The bacterial universal stress protein: function and regulation. Curr. Opin. Microbiol. 6, 140-145.
11. Sousa, M. C., and McKay, D. B. (2001) Structure of the universal stress protein of Haemophilus influenzae. Structure 9, 1135-1141.
12. O'Toole, R., and Williams, H. D. (2003) Universal stress proteins and Mycobacterium tuberculosis. Res. Microbiol. 154, 387-392.
13. Kelly, D. J., and Thomas, G. H. (2001) The tripartite ATP-independent periplasmic (TRAP) transporters of bacteria and archaea.FEMS Microbiol. Rev. 25, 405-424.
14. Galinski, E. A., and Herzog, R. M. (1990) The role of trehalose as a substitute for nitrogen-containing compatible solutes (Ectothiorhodospira halochloris). Arch.Microbiol. 153, 607-613.
15. Kunte, H. J., and Galinski, E. A. (1995) Transposon mutagenesis in halophilic eubacteria: conjugal transfer and insertion of transposon Tn5 and Tn1732 in Halomonas elongata. FEMS Microbiol. Lett. 128, 293-299.
16. Studier, F. W. (2005) Protein production by auto-induction in high density shaking cultures. Protein Expression Purif. 41, 207-234.
17. Kabsch, W. (1993) Automatic processing of rotation diffraction data from crystals of initially unknown symmetry and cell constants. J. Appl. Crystallogr. 26, 795-800.
18. McCoy, A. J. (2007) Solving structures of protein complexes by molecular replacement with Phaser. Acta Crystallogr., Sect. D: Biol. Crystallogr. 63, 32-41.
19. CCP4 (1994) The CCP4 suite: programs for protein crystallography. Acta Crystallogr., Sect. D: Biol. Crystallogr. 50, 760-763.
20. Cohen, S. X., Morris, R. J., Fernandez, F. J., Ben Jelloul, M., Kakaris, M., Parthasarathy, V., Lamzin, V. S., Kleywegt, G. J., and Perrakis, A. (2004) Towards complete validated models in the next generation of ARP/wARP. Acta Crystallogr., Sect. D: Biol. Crystallogr. 60, 2222-2229.
21. Murshudov, G. N., Vagin, A. A., and Dodson, E. J. (1997) Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr., Sect. D: Biol. Crystallogr. 53, 240-255.
22. Painter, J., and Merritt, E. A. (2005) A molecular viewer for the analysis of TLS rigid-body motion in macromolecules. Acta Crystallogr., Sect. D: Biol. Crystallogr. 61, 465-471.
23. DeLano, W. L. The PyMOL Molecular Graphics System, Delano Scientific LLC, San Carlos, CA (http://www/pymol.org).
24. Holm, L. S. (1997) Dali/FSSP classification of three-dimensional protein folds. Nucleic Acids Res. 25, 231-234.
25. Notredame, C., Higgins, D. G., and Heringa, J. (2000) T-Coffee: a novel method for fast and accurate multiple sequence alignment. J. Mol. Biol. 302, 205-217.
26. Altschul, S. F., Gish, W., Miller, W., Myers, E. W., and Lipman, D. J. (1990) Basic local alignment search tool. J. Mol. Biol. 215, 403-410.
27. Thompson, J. D., Higgins, D. G., and Gibson, T. J. (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignments through sequence weighting, position specific gap penalties and weight matrix choice. Nucleic Acids Res. 22, 4673-4680.
28. Hall, T. A. (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acid Symp. Ser. 41, 95-98.
29. Gouet, P., Robert, X., and Courcelle, E. (2003) ESPript/ENDscript: extracting and rendering sequence and 3D information from atomic structures of proteins. Nucleic Acids Res. 31, 3320-3323.
30. Mushegian, A. R., and Koonin, E. V. (1996) Sequence analysis of eukaryotic developmental proteins: ancient and novel domains. Genetics 144, 817-828.
31. Zarembinski, T. I., Hung, L. W., Mueller-Dieckmann, H. J., Kim, K. K., Yokota, H., Kim, R., and Kim, S. H. (1998) Structure-based assignment of the biochemical function of a hypothetical protein: a test case of structural genomics. Proc. Natl. Acad. Sci. U.S.A. 95, 15189-15193.
32. Ogura, T., Whiteheart, S. W., and Wilkinson, A. J. (2004) Conserved arginine residues implicated in ATP hydrolysis, nucleotide-sensing, and inter-subunit interactions in AAA and AAA+ ATPases. J. Struct, Biol. 146, 106-112.
33. Scheffzek, K., Ahmadian, M. R., Kabsch, W., Wiesmuller, L., Lautwein, A., Schmitz, F., and Wittinghofer, A. (1997) The RasRasGAP complex: structural basis for GTPase activation and its loss in oncogenic Ras mutants. Science 277, 333-338.
34. Gauthier, M. J., Lafay, B., Christen, R., Fernandez, L., Acquaviva, M., Bonin, P., and Bertrand, J. C. (1992) Marinohacter hydrocarbonoclasticus gen. nov., sp. nov., a new, extremely halotolerant, hydrocarbon-degrading marine bacterium. Int. J. Svst. Bacteriol. 42, 568-576.
35. Kuhlmann, S. I., Terwisscha van Scheltinga, A. C., Bienert, R., Kunte, H. J., and Ziegler, C. (2008) 1.55 Å structure of the ectoine binding protein TeaA of the osmoregulated TRAP-transporter TeaABC from Halomonas elongata. Biochemistry 47, 9475-9485.
36. Lecher, J., Pittelkow, M., Zobel, S., Bursy, J., Bonig, T., Smits, S. H. J., Schmitt, L., and Bremer, E. (2009) The crystal structure of UehA in complex with ectoine-a comparison with other TRAP-T binding proteins. J. Mol. Biol. 389, 58-73.
37. Saum, S. H., Sydow, J. F., Palm, P., Pfeiffer, F., Oesterhelt, D., and Muller, V. (2006) Biochemical and molecular characterization of the biosynthesis of glutamine and glutamate, two major compatible solutes in the moderately halophilic bacterium Halohacillus halophilus. J. Bacteriol. 188, 6808-6815.
38. Diederichs, K., and Karplus, P. A. (1997) Improved R-factors for diffraction data analysis in macromolecular crystallography. Nat, Struct. Biol. 4, 269-275.