This Article
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrowReprints and Permissions
Right arrow Copyright Information
Right arrow Books from ASM Press
Right arrow MicrobeWorld
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Kappes, R. M.
Right arrow Articles by Bremer, E.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Kappes, R. M.
Right arrow Articles by Bremer, E.

 Previous Article  |  Next Article 

J. Bacteriol., Sep 1996, 5071-5079, Vol 178, No. 17
Copyright © 1996, American Society for Microbiology

Three transport systems for the osmoprotectant glycine betaine operate in Bacillus subtilis: characterization of OpuD

RM Kappes, B Kempf and E Bremer
Max Planck Institute for Terrestrial Microbiology, Marburg, Germany.

The accumulation of the osmoprotectant glycine betaine from exogenous sources provides a high degree of osmotic tolerance to Bacillus subtilis. We have identified, through functional complementation of an Escherichia coli mutant defective in glycine betaine uptake, a new glycine betaine transport system from B. subtilis. The DNA sequence of a 2,310-bp segment of the cloned region revealed a single gene (opuD) whose product (OpuD) was essential for glycine betaine uptake and osmoprotection in E. coli. The opuD gene encodes a hydrophobic 56.13- kDa protein (512 amino acid residues). OpuD shows a significant degree of sequence identity to the choline transporter BetT and the carnitine transporter CaiT from E. coli and a BetT-like protein from Haemophilus influenzae. These membrane proteins form a family of transporters involved in the uptake of trimethylammonium compounds. The OpuD- mediated glycine betaine transport activity in B. subtilis is controlled by the environmental osmolarity. High osmolarity stimulates de novo synthesis of OpuD and activates preexisting OpuD proteins to achieve maximal glycine betaine uptake activity. An opuD mutant was constructed by marker replacement, and the OpuD-mediated glycine betaine uptake activity was compared with that of the previously identified multicomponent OpuA and OpuC (ProU) glycine betaine uptake systems. In addition, a set of mutants was constructed, each of which synthesized only one of the three glycine betaine uptake systems. These mutants were used to determine the kinetic parameters for glycine betaine transport through OpuA, OpuC, and OpuD. Each of these uptake systems shows high substrate affinity, with Km values in the low micromolar range, which should allow B. subtilis to efficiently acquire the osmoprotectant from the environment. The systems differed in their contribution to the overall glycine betaine accumulation and osmoprotection. A triple opuA, opuC, and opuD mutant strain was isolated, and it showed no glycine betaine uptake activity, demonstrating that three transport systems for this osmoprotectant operate in B. subtilis.


This article has been cited by other articles:

  • Santi, I., Grifantini, R., Jiang, S.-M., Brettoni, C., Grandi, G., Wessels, M. R., Soriani, M. (2009). CsrRS Regulates Group B Streptococcus Virulence Gene Expression in Response to Environmental pH: a New Perspective on Vaccine Development. J. Bacteriol. 191: 5387-5397 [Abstract] [Full Text]  
  • den Besten, H. M. W., Mols, M., Moezelaar, R., Zwietering, M. H., Abee, T. (2009). Phenotypic and Transcriptomic Analyses of Mildly and Severely Salt-Stressed Bacillus cereus ATCC 14579 Cells. Appl. Environ. Microbiol. 75: 4111-4119 [Abstract] [Full Text]  
  • Bursy, J., Kuhlmann, A. U., Pittelkow, M., Hartmann, H., Jebbar, M., Pierik, A. J., Bremer, E. (2008). Synthesis and Uptake of the Compatible Solutes Ectoine and 5-Hydroxyectoine by Streptomyces coelicolor A3(2) in Response to Salt and Heat Stresses. Appl. Environ. Microbiol. 74: 7286-7296 [Abstract] [Full Text]  
  • Smits, S. H. J., Hoing, M., Lecher, J., Jebbar, M., Schmitt, L., Bremer, E. (2008). The Compatible-Solute-Binding Protein OpuAC from Bacillus subtilis: Ligand Binding, Site-Directed Mutagenesis, and Crystallographic Studies. J. Bacteriol. 190: 5663-5671 [Abstract] [Full Text]  
  • Price, C. T. D., Bukka, A., Cynamon, M., Graham, J. E. (2008). Glycine Betaine Uptake by the ProXVWZ ABC Transporter Contributes to the Ability of Mycobacterium tuberculosis To Initiate Growth in Human Macrophages. J. Bacteriol. 190: 3955-3961 [Abstract] [Full Text]  
  • Chen, C., Beattie, G. A. (2008). Pseudomonas syringae BetT Is a Low-Affinity Choline Transporter That Is Responsible for Superior Osmoprotection by Choline over Glycine Betaine. J. Bacteriol. 190: 2717-2725 [Abstract] [Full Text]  
  • Hoffmann, T., Boiangiu, C., Moses, S., Bremer, E. (2008). Responses of Bacillus subtilis to Hypotonic Challenges: Physiological Contributions of Mechanosensitive Channels to Cellular Survival. Appl. Environ. Microbiol. 74: 2454-2460 [Abstract] [Full Text]  
  • Jiang, S.-M., Ishmael, N., Hotopp, J. D., Puliti, M., Tissi, L., Kumar, N., Cieslewicz, M. J., Tettelin, H., Wessels, M. R. (2008). Variation in the Group B Streptococcus CsrRS Regulon and Effects on Pathogenicity. J. Bacteriol. 190: 1956-1965 [Abstract] [Full Text]  
  • Chen, C., Beattie, G. A. (2007). Characterization of the Osmoprotectant Transporter OpuC from Pseudomonas syringae and Demonstration that Cystathionine-{beta}-Synthase Domains Are Required for Its Osmoregulatory Function. J. Bacteriol. 189: 6901-6912 [Abstract] [Full Text]  
  • Tondervik, A., Strom, A. R. (2007). Membrane topology and mutational analysis of the osmotically activated BetT choline transporter of Escherichia coli. Microbiology 153: 803-813 [Abstract] [Full Text]  
  • Laloknam, S., Tanaka, K., Buaboocha, T., Waditee, R., Incharoensakdi, A., Hibino, T., Tanaka, Y., Takabe, T. (2006). Halotolerant Cyanobacterium Aphanothece halophytica Contains a Betaine Transporter Active at Alkaline pH and High Salinity. Appl. Environ. Microbiol. 72: 6018-6026 [Abstract] [Full Text]  
  • Diab, F., Bernard, T., Bazire, A., Haras, D., Blanco, C., Jebbar, M. (2006). Succinate-mediated catabolite repression control on the production of glycine betaine catabolic enzymes in Pseudomonas aeruginosa PAO1 under low and elevated salinities.. Microbiology 152: 1395-1406 [Abstract] [Full Text]  
  • Lopez, C. S., Alice, A. F., Heras, H., Rivas, E. A., Sanchez-Rivas, C. (2006). Role of anionic phospholipids in the adaptation of Bacillus subtilis to high salinity.. Microbiology 152: 605-616 [Abstract] [Full Text]  
  • Schwan, W. R., Lehmann, L., McCormick, J. (2006). Transcriptional Activation of the Staphylococcus aureus putP Gene by Low-Proline-High Osmotic Conditions and during Infection of Murine and Human Tissues. Infect. Immun. 74: 399-409 [Abstract] [Full Text]  
  • Martin-Galiano, A. J., Overweg, K., Ferrandiz, M. J., Reuter, M., Wells, J. M., de la Campa, A. G. (2005). Transcriptional analysis of the acid tolerance response in Streptococcus pneumoniae. Microbiology 151: 3935-3946 [Abstract] [Full Text]  
  • Choquet, G., Jehan, N., Pissavin, C., Blanco, C., Jebbar, M. (2005). OusB, a Broad-Specificity ABC-Type Transporter from Erwinia chrysanthemi, Mediates Uptake of Glycine Betaine and Choline with a High Affinity. Appl. Environ. Microbiol. 71: 3389-3398 [Abstract] [Full Text]  
  • Kapfhammer, D., Karatan, E., Pflughoeft, K. J., Watnick, P. I. (2005). Role for Glycine Betaine Transport in Vibrio cholerae Osmoadaptation and Biofilm Formation within Microbial Communities. Appl. Environ. Microbiol. 71: 3840-3847 [Abstract] [Full Text]  
  • Jebbar, M., Sohn-Bosser, L., Bremer, E., Bernard, T., Blanco, C. (2005). Ectoine-Induced Proteins in Sinorhizobium meliloti Include an Ectoine ABC-Type Transporter Involved in Osmoprotection and Ectoine Catabolism. J. Bacteriol. 187: 1293-1304 [Abstract] [Full Text]  
  • Dupont, L., Garcia, I., Poggi, M.-C., Alloing, G., Mandon, K., Le Rudulier, D. (2004). The Sinorhizobium meliloti ABC Transporter Cho Is Highly Specific for Choline and Expressed in Bacteroids from Medicago sativa Nodules. J. Bacteriol. 186: 5988-5996 [Abstract] [Full Text]  
  • Craig, S. A. (2004). Betaine in human nutrition. Am. J. Clin. Nutr. 80: 539-549 [Abstract] [Full Text]  
  • Holtmann, G., Bremer, E. (2004). Thermoprotection of Bacillus subtilis by Exogenously Provided Glycine Betaine and Structurally Related Compatible Solutes: Involvement of Opu Transporters. J. Bacteriol. 186: 1683-1693 [Abstract] [Full Text]  
  • Ly, A., Henderson, J., Lu, A., Culham, D. E., Wood, J. M. (2004). Osmoregulatory Systems of Escherichia coli: Identification of Betaine-Carnitine-Choline Transporter Family Member BetU and Distributions of betU and trkG among Pathogenic and Nonpathogenic Isolates. J. Bacteriol. 186: 296-306 [Abstract] [Full Text]  
  • Steil, L., Hoffmann, T., Budde, I., Volker, U., Bremer, E. (2003). Genome-Wide Transcriptional Profiling Analysis of Adaptation of Bacillus subtilis to High Salinity. J. Bacteriol. 185: 6358-6370 [Abstract] [Full Text]  
  • Pflughoeft, K. J., Kierek, K., Watnick, P. I. (2003). Role of Ectoine in Vibrio cholerae Osmoadaptation. Appl. Environ. Microbiol. 69: 5919-5927 [Abstract] [Full Text]  
  • Kazmierczak, M. J., Mithoe, S. C., Boor, K. J., Wiedmann, M. (2003). Listeria monocytogenes {sigma}B Regulates Stress Response and Virulence Functions. J. Bacteriol. 185: 5722-5734 [Abstract] [Full Text]  
  • Brigulla, M., Hoffmann, T., Krisp, A., Volker, A., Bremer, E., Volker, U. (2003). Chill Induction of the SigB-Dependent General Stress Response in Bacillus subtilis and Its Contribution to Low-Temperature Adaptation. J. Bacteriol. 185: 4305-4314 [Abstract] [Full Text]  
  • Gadda, G., McAllister-Wilkins, E. E. (2003). Cloning, Expression, and Purification of Choline Dehydrogenase from the Moderate Halophile Halomonas elongata. Appl. Environ. Microbiol. 69: 2126-2132 [Abstract] [Full Text]  
  • Holtmann, G., Bakker, E. P., Uozumi, N., Bremer, E. (2003). KtrAB and KtrCD: Two K+ Uptake Systems in Bacillus subtilis and Their Role in Adaptation to Hypertonicity. J. Bacteriol. 185: 1289-1298 [Abstract] [Full Text]  
  • Jung, H., Buchholz, M., Clausen, J., Nietschke, M., Revermann, A., Schmid, R., Jung, K. (2002). CaiT of Escherichia coli, a New Transporter Catalyzing L-Carnitine/gamma -Butyrobetaine Exchange. J. Biol. Chem. 277: 39251-39258 [Abstract] [Full Text]  
  • Wemekamp-Kamphuis, H. H., Wouters, J. A., Sleator, R. D., Gahan, C. G. M., Hill, C., Abee, T. (2002). Multiple Deletions of the Osmolyte Transporters BetL, Gbu, and OpuC of Listeria monocytogenes Affect Virulence and Growth at High Osmolarity. Appl. Environ. Microbiol. 68: 4710-4716 [Abstract] [Full Text]  
  • Grammann, K., Volke, A., 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 2581T. J. Bacteriol. 184: 3078-3085 [Abstract] [Full Text]  
  • Waditee, R., Hibino, T., Tanaka, Y., Nakamura, T., Incharoensakdi, A., Hayakawa, S., Suzuki, S., Futsuhara, Y., Kawamitsu, Y., Takabe, T., Takabe, T. (2002). Functional Characterization of Betaine/Proline Transporters in Betaine-accumulating Mangrove. J. Biol. Chem. 277: 18373-18382 [Abstract] [Full Text]  
  • Boscari, A., Mandon, K., Dupont, L., Poggi, M.-C., Le Rudulier, D. (2002). BetS Is a Major Glycine Betaine/Proline Betaine Transporter Required for Early Osmotic Adjustment in Sinorhizobium meliloti. J. Bacteriol. 184: 2654-2663 [Abstract] [Full Text]  
  • Hoffmann, T., Schutz, A., Brosius, M., Volker, A., Volker, U., Bremer, E. (2002). High-Salinity-Induced Iron Limitation in Bacillus subtilis. J. Bacteriol. 184: 718-727 [Abstract] [Full Text]  
  • Sleator, R. D., Wouters, J., Gahan, C. G. M., Abee, T., Hill, C. (2001). Analysis of the Role of OpuC, an Osmolyte Transport System, in Salt Tolerance and Virulence Potential of Listeria monocytogenes. Appl. Environ. Microbiol. 67: 2692-2698 [Abstract] [Full Text]  
  • Jansen, M., Hansen, T. A. (2001). Non-Growth-Associated Demethylation of Dimethylsulfoniopropionate by (Homo)acetogenic Bacteria. Appl. Environ. Microbiol. 67: 300-306 [Abstract] [Full Text]  
  • Fraser, K. R., Harvie, D., Coote, P. J., O'Byrne, C. P. (2000). Identification and Characterization of an ATP Binding Cassette L-Carnitine Transporter in Listeria monocytogenes. Appl. Environ. Microbiol. 66: 4696-4704 [Abstract] [Full Text]  
  • Lai, M.-C., Hong, T.-Y., Gunsalus, R. P. (2000). Glycine Betaine Transport in the Obligate Halophilic Archaeon Methanohalophilus portucalensis. J. Bacteriol. 182: 5020-5024 [Abstract] [Full Text]  
  • Saier, M. H. Jr (2000). Families of transmembrane transporters selective for amino acids and their derivatives. Microbiology 146: 1775-1795 [Full Text]  
  • Boncompagni, E., Dupont, L., Mignot, T., Østeräs, M., Lambert, A., Poggi, M.-C., Le Rudulier, D. (2000). Characterization of a Sinorhizobium meliloti ATP-Binding Cassette Histidine Transporter Also Involved in Betaine and Proline Uptake. J. Bacteriol. 182: 3717-3725 [Abstract] [Full Text]  
  • Gerhardt, P. N. M., Tombras Smith, L., Smith, G. M. (2000). Osmotic and Chill Activation of Glycine Betaine Porter II in Listeria monocytogenes Membrane Vesicles. J. Bacteriol. 182: 2544-2550 [Abstract] [Full Text]  
  • Obis, D., Guillot, A., Gripon, J.-C., Renault, P., Bolotin, A., Mistou, M.-Y. (1999). Genetic and Biochemical Characterization of a High-Affinity Betaine Uptake System (BusA) in Lactococcus lactis Reveals a New Functional Organization within Bacterial ABC Transporters. J. Bacteriol. 181: 6238-6246 [Abstract] [Full Text]  
  • Ko, R., Smith, L. T. (1999). Identification of an ATP-Driven, Osmoregulated Glycine Betaine Transport System in Listeria monocytogenes. Appl. Environ. Microbiol. 65: 4040-4048 [Abstract] [Full Text]  
  • Cosquer, A., Pichereau, V., Pocard, J.-A., Minet, J., Cormier, M., Bernard, T. (1999). Nanomolar Levels of Dimethylsulfoniopropionate, Dimethylsulfonioacetate, and Glycine Betaine Are Sufficient To Confer Osmoprotection to Escherichia coli. Appl. Environ. Microbiol. 65: 3304-3311 [Abstract] [Full Text]  
  • Sleator, R. D., Gahan, C. G. M., Abee, T., Hill, C. (1999). Identification and Disruption of BetL, a Secondary Glycine Betaine Transport System Linked to the Salt Tolerance of Listeria monocytogenes LO28. Appl. Environ. Microbiol. 65: 2078-2083 [Abstract] [Full Text]  
  • Rosenstein, R., Futter-Bryniok, D., Götz, F. (1999). The Choline-Converting Pathway in Staphylococcus xylosus C2A: Genetic and Physiological Characterization. J. Bacteriol. 181: 2273-2278 [Abstract] [Full Text]  
  • Wood, J. M. (1999). Osmosensing by Bacteria: Signals and Membrane-Based Sensors. Microbiol. Mol. Biol. Rev. 63: 230-262 [Abstract] [Full Text]  
  • Nau-Wagner, G., Boch, J., Le Good, J. A., Bremer, E. (1999). High-Affinity Transport of Choline-O-Sulfate and Its Use as a Compatible Solute in Bacillus subtilis. Appl. Environ. Microbiol. 65: 560-568 [Abstract] [Full Text]  
  • Lai, M.-C., Yang, D.-R., Chuang, M.-J. (1999). Regulatory Factors Associated with Synthesis of the Osmolyte Glycine Betaine in the Halophilic Methanoarchaeon Methanohalophilus portucalensis. Appl. Environ. Microbiol. 65: 828-833 [Abstract] [Full Text]  
  • Peter, H., Weil, B., Burkovski, A., Krämer, R., Morbach, S. (1998). Corynebacterium glutamicum Is Equipped with Four Secondary Carriers for Compatible Solutes: Identification, Sequencing, and Characterization of the Proline/Ectoine Uptake System, ProP, and the Ectoine/Proline/Glycine Betaine Carrier, EctP. J. Bacteriol. 180: 6005-6012 [Abstract] [Full Text]  
  • Glaasker, E., Heuberger, E. H. M. L., Konings, W. N., Poolman, B. (1998). Mechanism of Osmotic Activation of the Quaternary Ammonium Compound Transporter (QacT) of Lactobacillus plantarum. J. Bacteriol. 180: 5540-5546 [Abstract] [Full Text]  
  • Becker, L. A., Çetin, M. S., Hutkins, R. W., Benson, A. K. (1998). Identification of the Gene Encoding the Alternative Sigma Factor sigma B from Listeria monocytogenes and Its Role in Osmotolerance. J. Bacteriol. 180: 4547-4554 [Abstract] [Full Text]  
  • Peter, H., Burkovski, A., Kramer, R. (1998). Osmo-sensing by N- and C-terminal Extensions of the Glycine Betaine Uptake System BetP of Corynebacterium glutamicum. J. Biol. Chem. 273: 2567-2574 [Abstract] [Full Text]  


Copyright © 2009 by the American Society for Microbiology.   For an alternate route to Journals.ASM.org, visit: http://intl-journals.asm.org | More Info»