Halotolerant cyanobacterium Aphanothece halophytica contains NapA-type Na+/H+ antiporters with novel ion specificity that are involved in salt tolerance at alkaline pH

Applied and Environmental Microbiology

Volumn 71, Issue 8, 2005, Pages 4176-4184

  Wutipraditkul, Nuchanat ^a   Waditee, Rungaroon ^b   Incharoensakdi, Aran ^c   Hibino, Takashi ^b   Tanaka, Yoshito ^b   Nakamura, Tatsunosuke ^d   Shikata, Masamitsu ^e   Takabe, Tetsuko ^a   Takabe, Teruhiro ^b  

^a NAGOYA UNIVERSITY   (Japan)

^b MEIJO UNIVERSITY   (Japan)

^c CHULALONGKORN UNIVERSITY   (Thailand)

^d NIIGATA UNIVERSITY OF PHARMACY AND APPLIED LIFE SCIENCES   (Japan)

^e SHIMADZU CORPORATION   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ALKALINITY; BIOLOGICAL MEMBRANES; GENES; PH EFFECTS; POLYPEPTIDES; SALTS;

ANTIPORTERS; APHANOTHECE HALOPHYTICA; FUNCTIONAL PROPERTIES;

BACTERIA;

ASPARTIC ACID; FRESH WATER; GLUTAMIC ACID; LITHIUM ION; POLYPEPTIDE; POTASSIUM ION; PROTEIN AP NAPA1 1; PROTEIN AP NAPA1 2; SODIUM CHLORIDE; SODIUM PROTON EXCHANGE PROTEIN; UNCLASSIFIED DRUG;

MICROBIOLOGY;

ALKALINITY; AMINO ACID SEQUENCE; APHANOTHECE HALOPHYTICA; ARTICLE; CONTROLLED STUDY; CYANOBACTERIUM; ENTEROCOCCUS HIRAE; ESCHERICHIA COLI; GENE ISOLATION; GENE OVEREXPRESSION; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; POTASSIUM TRANSPORT; PROTEIN ISOLATION; PSEUDOMONAS AERUGINOSA; SALT TOLERANCE; SITE DIRECTED MUTAGENESIS; SYNECHOCYSTIS;

AMINO ACID SEQUENCE; BACTERIAL PROTEINS; CULTURE MEDIA; CYANOBACTERIA; ESCHERICHIA COLI; GENE EXPRESSION REGULATION, BACTERIAL; HYDROGEN-ION CONCENTRATION; LITHIUM CHLORIDE; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; POTASSIUM; SODIUM CHLORIDE; SODIUM-HYDROGEN ANTIPORTER;

APHANOTHECE HALOPHYTICA; ENTEROCOCCUS HIRAE; ESCHERICHIA COLI; PSEUDOMONAS AERUGINOSA; SYNECHOCOCCUS SP.; SYNECHOCOCCUS SP. PCC 6301; SYNECHOCYSTIS; SYNECHOCYSTIS SP.;

EID: 23744466972     PISSN: 00992240     EISSN: None     Source Type: Journal    
DOI: 10.1128/AEM.71.8.4176-4184.2005     Document Type: Article

References (35)

1. Apse, M. P., and E. Blumwald. 2002. Engineering salt tolerance in plants. Curr. Opin. Biotechnol. 13:146-150.
2. + antiport activity in sugar beet tonoplast by analogs of amipride. Plant Physiol. 85:30-33.
3. + antiporter encoding genes of the cyanobacterium Synechocystis PCC 6803. Biochemistry (Moscow) 67:432-440.
4. + antiporter from Synechocystis species PCC 6803, homologous to SOS1, contains an aspartic residue and long C-terminal tail important for the carrier activity. Plant Physiol. 125:437-446.
5. Hibino, T., N. Kaku, H. Yoshikawa, T. Takabe, and T. Takabe. 1999. Molecular characterization of DnaK from the halotolerant cyanobacterium Aphanothece halophytica for ATPase, protein folding, and copper binding under various salinity conditions. Plant Mol. Biol. 40:409-418.
6. Hofmann, K., and W. Stoffel. 1992. PROFILEGRAPH: an interactive graphical tool for protein sequence analysis. Comput. Appl. Biosci. 8:331-337.
7. +)/H antiporters of Synechocystis. J. Bacteriol. 183:1376-1384.
8. Incharoensakdi, A., T. Takabe, and T. Akazawa. 1986. Role of the small subunit of ribulose-1,5-bisphosphate carboxylase/oxygenase in the activation process. Arch. Biochem. Biophys. 248:62-70.
9. Kaneko, T., S. Sato, H. Kotani, A. Tanaka, E. Asamizu, Y. Nakamura, N. Miyajima, M. Hirosawa, M. Sugiura, S. Sasamoto, T. Kimura, T. Hosouchi, A. Matsuno, A. Muraki, N. Nakazaki, K. Naruo, S. Okumura, S. Shimpo, C. Takeuchi, T. Wada, A. Watanabe, M. Yainada, M. Yasuda, and S. Tabata. 1996. Sequence analysis of the genome of the unicellular cyanobacterium Synechocystis sp. strain PCC6803. 1I. Sequence determination of the entire genome and assignment of potential protein-coding regions. DNA Res. 30:109-136.
10. Kempf, B., and E. Bremer. 1998. Uptake and synthesis of compatible solutes as microbial stress responses to high-osmolality environments. Arch. Microbiol. 170:319-330.
11. Kyte, J., and R. F. Doolittle. 1982. A simple method for displaying the hydropathic character of a protein. J. Mol. Biol. 157:105-132.
12. Lee, B. H., T. Hibino, J. Jo, A. M. Viale, and T. Takabe. 1997. Isolation and characterization of a dnaK genomic locus in a halotolerant cyanobacterium, Aphanothece halophytica. Plant Mol. Biol. 35:763-775.
13. Maser, P., S. Thomine, J. I. Schroeder, J. M. Ward, K. Hirschi, H. Sze, I. N. Talke, A. Amtmann, F. J. Maathuis, D. Sanders, J. F. Harper, J. Tchieu, M. Gribskov, M. W. Persans, D. E. Salt, S. A. Kim, and M. L. Guerinot. 2001. Phylogenetic relationships within cation transporter families of Arabidopsis. Plant Physiol. 126:1646-1667.
14. Munro, A. W., G. Y. Ritchie, A. J. Lamb, R. M. Douglas, and I. R. Booth. 1991. The cloning and DNA sequence of the gene for the glutathione-regulated potassium-efflux system KefC of Escherichia coli. Mol. Microbiol. 5:607-616.
15. Nakamura, C., J. G. Burgess, K. Sode, and T. Matsunaga. 1995. An iron-regulated gene, magA, encoding an iron transport protein of Magnetospirillum sp. strain AMB-1. J. Biol. Chem. 270:28392-28396.
16. +-uptake system of Vibrio alginolyticus. Microbiology 144:2281-2289.
17. + antiporter from Vibrio alginolyticus play a role in the activity of the carrier. Biochim. Biophys. Acta 1230:170-176.
18. Ohyania, T., K. Igarashi, and H. Kobayashi. 1995. Physiological role of the chaA gene in sodium and calcium circulations at a high pH in Escherichia coli. J. Bacteriol. 176:4311-4315.
19. + exchangers of mammalian cells. J. Biol. Chem. 272:22373-22376.
20. + antiporter of Escherichia coli as determined by site-directed thiol cross-linking. Biochemistry 41:14897-14905.
21. Rontein, D., G. Basset, and A. D. Hanson. 2002. Metabolic engineering of osmoprotectant accumulation in plants. Metab. Eng. 4:49-56.
22. Saier, M. H., Jr., B. H. Eng, S. Fard, J. Garg, D. A. Haggerty, W. J. Hutchinson, D. L. Jack, E. C. Lai, H. J. Liu, D. P. Nusinew, A. M. Omar, S. S. Pao, I. T. Paulsen, J. A. Quan, M. Sliwinski, T. T. Tseng, S. Wachi, and G. B. Young. 1999. Phylogenetic characterization of novel transport protein families revealed by genome analyses. Biochim. Biophys. Acta 1422:1-56.
23. + antiporter. J. Bacteriol. 183:5896-5903.
24. + homeostasis in pollen development. Plant Physiol. 136: 2532-2547.
25. + antiporter coded by nhaA (ant) from Escherichia coli. J. Biol. Chem. 266:11289-11294.
26. Tani, K., T. Watanabe, H. Matsuda, M. Nasu, and M. Kondo. 1996. Cloning and sequencing of the spore germination gene of Bacillus megaterium ATCC 12872: similarities to the NaH-antiporter gene of Enterococcus hirae. Microbiol. Immunol. 40:99-105.
27. Thackray, P. D., J. Behravan, T. W. Southworth, and A. Moir. 2001. GerN, an antiporter homologue important in germination of Bacillus cereus endospores. J. Bacteriol. 183:476-482.
28. + antiporter (NhaA) protein from Helicobacter pylori required for ion transport and pH sensing. J. Biol. Chem. 278:21467-21473.
29. + antiporter gene from Pseudomonas aeruginosa Biochm. Biophys. Acta 1398:330-334.
30. + antiporter confers salt tolerance on a freshwater cyanobacterium, making it capable of growth in sea water. Proc. Natl. Acad. Sci. USA 99:4109-4114.
31. Waditee, R., T. Hibino, Y. Tanaka, T. Nakamura, A. Incharoensakdi, S. Hayakawa Y. Futsuhara, Y. Kawamitsu, T. Takabe, and T. Takabe. 2002. Functional characterization of betaine/proline transporters in betaine-accumulating mangrove. J. Biol. Chem. 277:18373-18382.
32. + antiporter, homologous to eukaryotic ones, with novel ion specificity affected by C-terminal tail. J. Biol. Chem. 276:36931-36938.
33. + and pH homeostasis of Synechocystis sp. PCC 6803. Mol. Microbiol. 44:1493-1506.
34. Waser, M., D. Hess-Bienz, K. Davies, and M. Solioz. 1992 Cloning and disruption of a putative NaH-antiporter gene of Enterococcus hirae. J. Biol. Chem. 267:5396-5400.
35. Zhu, J. K. 2003. Regulation of ion homeostasis under salt stress. Curr. Opin. Plant Biol. 6:441-445.