Skip to main content
Applied and Environmental Microbiology logoLink to Applied and Environmental Microbiology
. 1997 Mar;63(3):969–972. doi: 10.1128/aem.63.3.969-972.1997

Coregulation of beta-galactoside uptake and hydrolysis by the hyperthermophilic bacterium Thermotoga neapolitana

MY Galperin 1, KM Noll 1, AH Romano 1
PMCID: PMC168389  PMID: 9285771

Abstract

Regulation of the beta-galactoside transport system in response to growth substrates in the extremely thermophilic anaerobic bacterium Thermotoga neapolitana was studied with the nonmetabolizable analog methyl-beta-D-thiogalactopyranoside (TMG) as the transport substrate. T. neapolitana cells grown on galactose or lactose accumulated TMG against a concentration gradient in an intracellular free sugar pool that was exchangeable with external galactose or lactose and showed induced levels of beta-galactosidase. Cells grown on glucose, maltose, or galactose plus glucose showed no capacity to accumulate TMG, though these cells carried out active transport of the nonmetabolizable glucose analog 2-deoxy-D-glucose. Glucose neither inhibited TMG uptake nor caused efflux of preaccumulated TMG; rather, glucose promoted TMG uptake by supplying metabolic energy. These data show that beta-D-galactosides are taken up by T. neapolitana via an active transport system that can be induced by galactose or lactose and repressed by glucose but which is not inhibited by glucose. Thus, the phenomenon of catabolite repression is present in T. neapolitana with respect to systems catalyzing both the transport and hydrolysis of beta-D-galactosides, but inducer exclusion and inducer expulsion, mechanisms that regulate permease activity, are not present. Regulation is manifest at the level of synthesis of the beta-galactoside transport system but not in the activity of the system.

Full Text

The Full Text of this article is available as a PDF (76.5 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Achenbach-Richter L., Gupta R., Stetter K. O., Woese C. R. Were the original eubacteria thermophiles? Syst Appl Microbiol. 1987;9:34–39. doi: 10.1016/s0723-2020(87)80053-x. [DOI] [PubMed] [Google Scholar]
  2. Adams M. W. Biochemical diversity among sulfur-dependent, hyperthermophilic microorganisms. FEMS Microbiol Rev. 1994 Oct;15(2-3):261–277. doi: 10.1111/j.1574-6976.1994.tb00139.x. [DOI] [PubMed] [Google Scholar]
  3. Belkin S., Wirsen C. O., Jannasch H. W. A new sulfur-reducing, extremely thermophilic eubacterium from a submarine thermal vent. Appl Environ Microbiol. 1986 Jun;51(6):1180–1185. doi: 10.1128/aem.51.6.1180-1185.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bradford M. M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 1976 May 7;72:248–254. doi: 10.1016/0003-2697(76)90527-3. [DOI] [PubMed] [Google Scholar]
  5. Childers S. E., Vargas M., Noll K. M. Improved Methods for Cultivation of the Extremely Thermophilic Bacterium Thermotoga neapolitana. Appl Environ Microbiol. 1992 Dec;58(12):3949–3953. doi: 10.1128/aem.58.12.3949-3953.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Deutscher J., Küster E., Bergstedt U., Charrier V., Hillen W. Protein kinase-dependent HPr/CcpA interaction links glycolytic activity to carbon catabolite repression in gram-positive bacteria. Mol Microbiol. 1995 Mar;15(6):1049–1053. doi: 10.1111/j.1365-2958.1995.tb02280.x. [DOI] [PubMed] [Google Scholar]
  7. Galperin MY, Noll KM, Romano AH. The glucose transport system of the hyperthermophilic anaerobic bacterium Thermotoga neapolitana. Appl Environ Microbiol. 1996 Aug;62(8):2915–2918. doi: 10.1128/aem.62.8.2915-2918.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Kashket E. R. Proton motive force in growing Streptococcus lactis and Staphylococcus aureus cells under aerobic and anaerobic conditions. J Bacteriol. 1981 Apr;146(1):369–376. doi: 10.1128/jb.146.1.369-376.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Moore J. B., Markiewicz P., Miller J. H. Identification and sequencing of the Thermotoga maritima lacZ gene, part of a divergently transcribed operon. Gene. 1994 Sep 15;147(1):101–106. doi: 10.1016/0378-1119(94)90046-9. [DOI] [PubMed] [Google Scholar]
  10. Olsen G. J., Woese C. R., Overbeek R. The winds of (evolutionary) change: breathing new life into microbiology. J Bacteriol. 1994 Jan;176(1):1–6. doi: 10.1128/jb.176.1.1-6.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Postma P. W., Lengeler J. W., Jacobson G. R. Phosphoenolpyruvate:carbohydrate phosphotransferase systems of bacteria. Microbiol Rev. 1993 Sep;57(3):543–594. doi: 10.1128/mr.57.3.543-594.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Reizer J., Bergstedt U., Galinier A., Küster E., Saier M. H., Jr, Hillen W., Steinmetz M., Deutscher J. Catabolite repression resistance of gnt operon expression in Bacillus subtilis conferred by mutation of His-15, the site of phosphoenolpyruvate-dependent phosphorylation of the phosphocarrier protein HPr. J Bacteriol. 1996 Sep;178(18):5480–5486. doi: 10.1128/jb.178.18.5480-5486.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Reizer J., Novotny M. J., Panos C., Saier M. H., Jr Mechanism of inducer expulsion in Streptococcus pyogenes: a two-step process activated by ATP. J Bacteriol. 1983 Oct;156(1):354–361. doi: 10.1128/jb.156.1.354-361.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Reizer J., Romano A. H., Deutscher J. The role of phosphorylation of HPr, a phosphocarrier protein of the phosphotransferase system, in the regulation of carbon metabolism in gram-positive bacteria. J Cell Biochem. 1993 Jan;51(1):19–24. doi: 10.1002/jcb.240510105. [DOI] [PubMed] [Google Scholar]
  15. Romano A. H., Brino G., Peterkofsky A., Reizer J. Regulation of beta-galactoside transport and accumulation in heterofermentative lactic acid bacteria. J Bacteriol. 1987 Dec;169(12):5589–5596. doi: 10.1128/jb.169.12.5589-5596.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Saier M. H., Jr Protein phosphorylation and allosteric control of inducer exclusion and catabolite repression by the bacterial phosphoenolpyruvate: sugar phosphotransferase system. Microbiol Rev. 1989 Mar;53(1):109–120. doi: 10.1128/mr.53.1.109-120.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Saier M. H., Jr, Ramseier T. M. The catabolite repressor/activator (Cra) protein of enteric bacteria. J Bacteriol. 1996 Jun;178(12):3411–3417. doi: 10.1128/jb.178.12.3411-3417.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Saier M. H., Jr, Reizer J. Proposed uniform nomenclature for the proteins and protein domains of the bacterial phosphoenolpyruvate: sugar phosphotransferase system. J Bacteriol. 1992 Mar;174(5):1433–1438. doi: 10.1128/jb.174.5.1433-1438.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Vargas M., Noll K. M. Catabolite repression in the hyperthermophilic bacterium Thermotoga neapolitana is independent of cAMP. Microbiology. 1996 Jan;142(Pt 1):139–144. doi: 10.1099/13500872-142-1-139. [DOI] [PubMed] [Google Scholar]
  20. Woese C. R. Bacterial evolution. Microbiol Rev. 1987 Jun;51(2):221–271. doi: 10.1128/mr.51.2.221-271.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Ye J. J., Neal J. W., Cui X., Reizer J., Saier M. H., Jr Regulation of the glucose:H+ symporter by metabolite-activated ATP-dependent phosphorylation of HPr in Lactobacillus brevis. J Bacteriol. 1994 Jun;176(12):3484–3492. doi: 10.1128/jb.176.12.3484-3492.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Applied and Environmental Microbiology are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES