Identification and Functional Characterization of theLactococcus lactisCodY-Regulated Branched-Chain Amino Acid Permease BcaP (CtrA)
10.1128/jb.188.9.3280-3289.2006
Crossref journal-article
American Society for Microbiology
Journal of Bacteriology (235)
Abstract

ABSTRACTTranscriptome analyses have previously revealed that a gene encoding the putative amino acid transporter CtrA (YhdG) is one of the major targets of the pleiotropic regulator CodY inLactococcus lactisandBacillus subtilis. The role ofctrAinL. lactiswas further investigated with respect to both transport activity as well as CodY-mediated regulation. CtrA is required for optimal growth in media containing free amino acids as the only amino acid source. Amino acid transport studies showed thatctrAencodes a secondary amino acid transport system that is specific for branched-chain amino acids (BCAAs) (isoleucine, leucine, and valine) and methionine, which is in disagreement with its previously proposed function (a cationic amino acid transporter), which was assigned based on homology. We propose to rename CtrA BcaP, for branched-chain amino acid permease. BcaP is a member of a group of conserved transport systems, as homologs are widely distributed among gram-positive bacteria. Deletion ofbcaPresulted in the loss of most of the BCAA uptake activity ofL. lactis, indicating that BcaP is the major BCAA carrier of this organism. Deletion ofbcaPtogether with a second (putative) BCAA permease, encoded bybrnQ, further reduced the viability of the strain. DNA microarray analysis showed that deletion ofbcaPpredominantly affects genes belonging to the regulons of the transcriptional regulator CodY, which is involved in global nitrogen metabolism and needs BCAAs for its activation, and of CmbR, which is involved in sulfur amino acid metabolism.

Bibliography

den Hengst, C. D., Groeneveld, M., Kuipers, O. P., & Kok, J. (2006). Identification and Functional Characterization of theLactococcus lactisCodY-Regulated Branched-Chain Amino Acid Permease BcaP (CtrA). Journal of Bacteriology, 188(9), 3280–3289.

Authors 4
  1. Chris D. den Hengst (first)
  2. Maarten Groeneveld (additional)
  3. Oscar P. Kuipers (additional)
  4. Jan Kok (additional)
References 66 Referenced 55
  1. 10.1016/S0022-2836(05)80360-2
  2. 10.1128/jb.179.17.5448-5457.1997
  3. Bolotin, A., B. Quinquis, P. Renault, A. Sorokin, S. D. Ehrlich, S. Kulakauskas, A. Lapidus, E. Goltsman, M. Mazur, G. D. Pusch, M. Fonstein, R. Overbeek, N. Kyprides, B. Purnelle, D. Prozzi, K. Ngui, D. Masuy, F. Hancy, S. Burteau, M. Boutry, J. Delcour, A. Goffeau, and P. Hols. 2004. Complete sequence and comparative genome analysis of the dairy bacterium Streptococcus thermophilus. Nat. Biotechnol. 22 : 1554-1558. (10.1038/nbt1034) / Nat. Biotechnol. (2004)
  4. Bolotin, A., P. Wincker, S. Mauger, O. Jaillon, K. Malarme, J. Weissenbach, S. D. Ehrlich, and A. Sorokin. 2001. The complete genome sequence of the lactic acid bacterium Lactococcus lactis ssp. lactis IL1403. Genome Res. 11 : 731-753. (10.1101/gr.GR-1697R) / Genome Res. (2001)
  5. 10.1128/JB.187.2.512-521.2005
  6. den Hengst, C. D., S. A. F. T. van Hijum, J. M. Geurts, A. Nauta, J. Kok, and O. P. Kuipers. 2005. The Lactococcus lactis CodY regulon: identification of a conserved cis-regulatory element. J. Biol. Chem. 280 : 34332-34342. (10.1074/jbc.M502349200) / J. Biol. Chem. (2005)
  7. 10.1128/aem.62.10.3662-3667.1996
  8. 10.1128/jb.169.11.5193-5200.1987
  9. Driessen, A. J., K. J. Hellingwerf, and W. N. Konings. 1987. Mechanism of energy coupling to entry and exit of neutral and branched chain amino acids in membrane vesicles of Streptococcus cremoris. J. Biol. Chem. 262 : 12438-12443. (10.1016/S0021-9258(18)45223-4) / J. Biol. Chem. (1987)
  10. 10.1128/jb.169.6.2748-2754.1987
  11. 10.1128/JB.184.1.82-90.2002
  12. 10.1128/jb.177.16.4652-4657.1995
  13. Gasson, M. J. 1983. Plasmid complements of Streptococcus lactis NCDO 712 and other lactic streptococci after protoplast-induced curing. J. Bacteriol. 154 : 1-9. (10.1128/jb.154.1.1-9.1983) / J. Bacteriol. (1983)
  14. Geertsma, E. R., R. H. Duurkens, and B. Poolman. 2005. The activity of the lactose transporter from Streptococcus thermophilus is increased by phosphorylated IIA and the action of beta-galactosidase. Biochemistry 44 : 15889-15897. (10.1021/bi051638w) / Biochemistry (2005)
  15. 10.1128/JB.187.7.2426-2438.2005
  16. Glaser, P., L. Frangeul, C. Buchrieser, C. Rusniok, A. Amend, F. Baquero, P. Berche, H. Bloecker, P. Brandt, T. Chakraborty, A. Charbit, F. Chetouani, E. Couve, A. de Daruvar, P. Dehoux, E. Domann, G. Dominguez-Bernal, E. Duchaud, L. Durant, O. Dussurget, K. D. Entian, H. Fsihi, F. Garcia-del Portillo, P. Garrido, L. Gautier, W. Goebel, N. Gomez-Lopez, T. Hain, J. Hauf, D. Jackson, L. M. Jones, U. Kaerst, J. Kreft, M. Kuhn, F. Kunst, G. Kurapkat, E. Madueno, A. Maitournam, J. M. Vicente, E. Ng, H. Nedjari, G. Nordsiek, S. Novella, B. de Pablos, J. C. Perez-Diaz, R. Purcell, B. Remmel, M. Rose, T. Schlueter, N. Simoes, A. Tierrez, J. A. Vazquez-Boland, H. Voss, J. Wehland, and P. Cossart. 2001. Comparative genomics of Listeria species. Science 294 : 849-852. (10.1126/science.1063447) / Science (2001)
  17. Golic, N., M. Schliekelmann, M. Fernandez, M. Kleerebezem, and R. van Kranenburg. 2005. Molecular characterization of the CmbR activator-binding site in the metC-cysK promoter region in Lactococcus lactis. Microbiology 151 : 439-446. (10.1099/mic.0.27411-0) / Microbiology (2005)
  18. 10.1128/JB.183.12.3614-3622.2001
  19. Guédon, E., P. Serror, S. D. Ehrlich, P. Renault, and C. Delorme. 2001. Pleiotropic transcriptional repressor CodY senses the intracellular pool of branched-chain amino acids in Lactococcus lactis. Mol. Microbiol. 40 : 1227-1239. (10.1046/j.1365-2958.2001.02470.x) / Mol. Microbiol. (2001)
  20. Guédon, E., B. Sperandio, N. Pons, S. D. Ehrlich, and P. Renault. 2005. Overall control of nitrogen metabolism in Lactococcus lactis by CodY, and possible models for CodY regulation in Firmicutes. Microbiology 151 : 3895-3909. (10.1099/mic.0.28186-0) / Microbiology (2005)
  21. Hagting, A., E. R. Kunji, K. J. Leenhouts, B. Poolman, and W. N. Konings. 1994. The di- and tripeptide transport protein of Lactococcus lactis. A new type of bacterial peptide transporter. J. Biol. Chem. 269 : 11391-11399. (10.1016/S0021-9258(19)78137-X) / J. Biol. Chem. (1994)
  22. Hoffmaster, A. R., J. Ravel, D. A. Rasko, G. D. Chapman, M. D. Chute, C. K. Marston, B. K. De, C. T. Sacchi, C. Fitzgerald, L. W. Mayer, M. C. Maiden, F. G. Priest, M. Barker, L. Jiang, R. Z. Cer, J. Rilstone, S. N. Peterson, R. S. Weyant, D. R. Galloway, T. D. Read, T. Popovic, and C. M. Fraser. 2004. Identification of anthrax toxin genes in a Bacillus cereus associated with an illness resembling inhalation anthrax. Proc. Natl. Acad. Sci. USA 101 : 8449-8454. (10.1073/pnas.0402414101) / Proc. Natl. Acad. Sci. USA (2004)
  23. Holo, H., and I. F. Nes. 1995. Transformation of Lactococcus by electroporation. Methods Mol. Biol. 47 : 195-199. / Methods Mol. Biol. (1995)
  24. 10.1128/JB.183.19.5709-5717.2001
  25. Reference deleted.
  26. 10.1128/aem.61.8.3024-3030.1995
  27. 10.1128/aem.63.11.4581-4584.1997
  28. Kleerebezem, M., J. Boekhorst, R. van Kranenburg, D. Molenaar, O. P. Kuipers, R. Leer, R. Tarchini, S. A. Peters, H. M. Sandbrink, M. W. Fiers, W. Stiekema, R. M. Lankhorst, P. A. Bron, S. M. Hoffer, M. N. Groot, R. Kerkhoven, M. de Vries, B. Ursing, W. M. de Vos, and R. J. Siezen. 2003. Complete genome sequence of Lactobacillus plantarum WCFS1. Proc. Natl. Acad. Sci. USA 100 : 1990-1995. (10.1073/pnas.0337704100) / Proc. Natl. Acad. Sci. USA (2003)
  29. Kok, J., and G. Buist. 2003. Genetics of proteolysis in Lactococcus lactis, p. 189-224. In B. J. B. Wood and W. M. de Vos (ed.), Genetics of lactic acid bacteria. Kluwer Academics/Plenum Publishers, New York, N.Y. / Genetics of lactic acid bacteria (2003)
  30. Konings, W. N., B. Poolman, and A. J. Driessen. 1989. Bioenergetics and solute transport in lactococci. Crit. Rev. Microbiol. 16 : 419-476. (10.3109/10408418909104474) / Crit. Rev. Microbiol. (1989)
  31. Kuipers, O. P., M. M. Beerthuyzen, R. J. Siezen, and W. M. de Vos. 1993. Characterization of the nisin gene cluster nisABTCIPR of Lactococcus lactis. Requirement of expression of the nisA and nisI genes for development of immunity. Eur. J. Biochem. 216 : 281-291. (10.1111/j.1432-1033.1993.tb18143.x) / Eur. J. Biochem. (1993)
  32. Kuipers, O. P., P. G. de Ruyter, M. Kleerebezem, and W. M. de Vos. 1998. Quorum sensing controlled gene expression in lactic acid bacteria. Biotechnology 64 : 15-21. / Biotechnology (1998)
  33. Kunji, E. R., A. Hagting, C. J. De Vries, V. Juillard, A. J. Haandrikman, B. Poolman, and W. N. Konings. 1995. Transport of beta-casein-derived peptides by the oligopeptide transport system is a crucial step in the proteolytic pathway of Lactococcus lactis. J. Biol. Chem. 270 : 1569-1574. (10.1074/jbc.270.4.1569) / J. Biol. Chem. (1995)
  34. Kunji, E. R., I. Mierau, A. Hagting, B. Poolman, and W. N. Konings. 1996. The proteolytic systems of lactic acid bacteria. Antonie Leeuwenhoek 70 : 187-221. (10.1007/BF00395933) / Antonie Leeuwenhoek (1996)
  35. 10.1038/36786
  36. Kyte, J., and R. F. Doolittle. 1982. A simple method for displaying the hydropathic character of a protein. J. Mol. Biol. 157 : 105-132. (10.1016/0022-2836(82)90515-0) / J. Mol. Biol. (1982)
  37. 10.1038/227680a0
  38. 10.1128/AEM.69.5.2521-2532.2003
  39. Leenhouts, K., G. Buist, A. Bolhuis, A. ten Berge, J. Kiel, I. Mierau, M. Dabrowska, G. Venema, and J. Kok. 1996. A general system for generating unlabelled gene replacements in bacterial chromosomes. Mol. Gen. Genet. 253 : 217-224. (10.1007/s004380050315) / Mol. Gen. Genet. (1996)
  40. 10.1128/aem.56.9.2726-2735.1990
  41. 10.1128/jb.174.17.5633-5638.1992
  42. Marchler-Bauer, A., J. B. Anderson, P. F. Cherukuri, C. Weese-Scott, L. Y. Geer, M. Gwadz, S. He, D. I. Hurwitz, J. D. Jackson, Z. Ke, C. J. Lanczycki, C. A. Liebert, C. Liu, F. Lu, G. H. Marchler, M. Mullokandov, B. A. Shoemaker, V. Simonyan, J. S. Song, P. A. Thiessen, R. A. Yamashita, J. J. Yin, D. Zhang, and S. H. Bryant. 2005. CDD: a conserved domain database for protein classification. Nucleic Acids Res. 33 : D192-D196. (10.1093/nar/gni191) / Nucleic Acids Res. (2005)
  43. 10.1128/jb.176.10.2854-2861.1994
  44. Mills, O. E., and T. D. Thomas. 1981. Nitrogen sources for growth of lactic streptococci in milk. N. Z. J. Dairy Sci. Technol. 16 : 43-55. / N. Z. J. Dairy Sci. Technol. (1981)
  45. 10.1128/JB.185.6.1911-1922.2003
  46. 10.1266/jjg.63.343
  47. Ohnishi, K., K. Matsubara, Y. Hattori, H. Sadanari, R. Yamada, and S. Fukuda. 1999. Identification of a cis-acting regulatory sequence responsible for the repression of brnQ in Salmonella typhimurium. Biochim. Biophys. Acta 1445 : 196-206. (10.1016/S0167-4781(99)00043-3) / Biochim. Biophys. Acta (1999)
  48. Paulsen, I. T., L. Banerjei, G. S. Myers, K. E. Nelson, R. Seshadri, T. D. Read, D. E. Fouts, J. A. Eisen, S. R. Gill, J. F. Heidelberg, H. Tettelin, R. J. Dodson, L. Umayam, L. Brinkac, M. Beanan, S. Daugherty, R. T. Deboy, S. Durkin, J. Kolonay, R. Madupu, W. Nelson, J. Vamathevan, B. Tran, J. Upton, T. Hansen, J. Shetty, H. Khouri, T. Utterback, D. Radune, K. A. Ketchum, B. A. Dougherty, and C. M. Fraser. 2003. Role of mobile DNA in the evolution of vancomycin-resistant Enterococcus faecalis. Science 299 : 2071-2074. (10.1126/science.1080613) / Science (2003)
  49. Petranovic, D., E. Guedon, B. Sperandio, C. Delorme, D. Ehrlich, and P. Renault. 2004. Intracellular effectors regulating the activity of the Lactococcus lactis CodY pleiotropic transcription regulator. Mol. Microbiol. 53 : 613-621. (10.1111/j.1365-2958.2004.04136.x) / Mol. Microbiol. (2004)
  50. 10.1128/jb.170.2.700-707.1988
  51. 10.1101/gad.874201
  52. Sambrook J. E. F. Fritsch and T. Maniatis . 1989. Molecular cloning: a laboratory manual 2nd ed. Cold Spring Harbor Laboratory Press Cold Spring Harbor N.Y.
  53. Sanz, Y., F. C. Lanfermeijer, P. Renault, A. Bolotin, W. N. Konings, and B. Poolman. 2001. Genetic and functional characterization of dpp genes encoding a dipeptide transport system in Lactococcus lactis. Arch. Microbiol. 175 : 334-343. (10.1007/s002030100270) / Arch. Microbiol. (2001)
  54. Sanz, Y., F. Toldra, P. Renault, and B. Poolman. 2003. Specificity of the second binding protein of the peptide ABC-transporter (Dpp) of Lactococcus lactis IL1403. FEMS Microbiol. Lett. 227 : 33-38. (10.1016/S0378-1097(03)00662-1) / FEMS Microbiol. Lett. (2003)
  55. Shivers, R. P., and A. L. Sonenshein. 2004. Activation of the Bacillus subtilis global regulator CodY by direct interaction with branched-chain amino acids. Mol. Microbiol. 53 : 599-611. (10.1111/j.1365-2958.2004.04135.x) / Mol. Microbiol. (2004)
  56. Slack, F. J., P. Serror, E. Joyce, and A. L. Sonenshein. 1995. A gene required for nutritional repression of the Bacillus subtilis dipeptide permease operon. Mol. Microbiol. 15 : 689-702. (10.1111/j.1365-2958.1995.tb02378.x) / Mol. Microbiol. (1995)
  57. Sonenshein, A. L. 2005. CodY, a global regulator of stationary phase and virulence in Gram-positive bacteria. Curr. Opin. Microbiol. 8 : 203-207. (10.1016/j.mib.2005.01.001) / Curr. Opin. Microbiol. (2005)
  58. 10.1128/JB.187.11.3762-3778.2005
  59. 10.1128/jb.174.10.3242-3249.1992
  60. Stucky, K., A. Hagting, J. R. Klein, H. Matern, B. Henrich, W. N. Konings, and R. Plapp. 1995. Cloning and characterization of brnQ, a gene encoding a low-affinity, branched-chain amino acid carrier in Lactobacillus delbruckii subsp. lactis DSM7290. Mol. Gen. Genet. 249 : 682-690. (10.1007/BF00418038) / Mol. Gen. Genet. (1995)
  61. Tauch, A., T. Hermann, A. Burkovski, R. Kramer, A. Puhler, and J. Kalinowski. 1998. Isoleucine uptake in Corynebacterium glutamicum ATCC 13032 is directed by the brnQ gene product. Arch. Microbiol. 169 : 303-312. (10.1007/s002030050576) / Arch. Microbiol. (1998)
  62. 10.1128/am.29.6.807-813.1975
  63. van Hijum, S. A., J. A. De, R. J. Baerends, H. A. Karsens, N. E. Kramer, R. Larsen, C. D. den Hengst, C. J. Albers, J. Kok, and O. P. Kuipers. 2005. A generally applicable validation scheme for the assessment of factors involved in reproducibility and quality of DNA-microarray data. BMC Genomics 6 : 77. (10.1186/1471-2164-6-77) / BMC Genomics (2005)
  64. Veenhoff, L. M., and B. Poolman. 1999. Substrate recognition at the cytoplasmic and extracellular binding site of the lactose transport protein of Streptococcus thermophilus. J. Biol. Chem. 274 : 33244-33250. (10.1074/jbc.274.47.33244) / J. Biol. Chem. (1999)
  65. Walshaw, D. L., and P. S. Poole. 1996. The general L-amino acid permease of Rhizobium leguminosarum is an ABC uptake system that also influences efflux of solutes. Mol. Microbiol. 21 : 1239-1252. (10.1046/j.1365-2958.1996.00078.x) / Mol. Microbiol. (1996)
  66. 10.1128/AEM.70.11.6738-6747.2004
Dates
Type When
Created 19 years, 4 months ago (April 18, 2006, 1:20 a.m.)
Deposited 1 year, 7 months ago (Feb. 3, 2024, 2:48 p.m.)
Indexed 1 year, 1 month ago (July 24, 2024, 4 a.m.)
Issued 19 years, 4 months ago (May 1, 2006)
Published 19 years, 4 months ago (May 1, 2006)
Published Print 19 years, 4 months ago (May 1, 2006)
Funders 0

None

@article{den_Hengst_2006, title={Identification and Functional Characterization of theLactococcus lactisCodY-Regulated Branched-Chain Amino Acid Permease BcaP (CtrA)}, volume={188}, ISSN={1098-5530}, url={http://dx.doi.org/10.1128/jb.188.9.3280-3289.2006}, DOI={10.1128/jb.188.9.3280-3289.2006}, number={9}, journal={Journal of Bacteriology}, publisher={American Society for Microbiology}, author={den Hengst, Chris D. and Groeneveld, Maarten and Kuipers, Oscar P. and Kok, Jan}, year={2006}, month=may, pages={3280–3289} }