Summary
In Escherichia coli K12, eight substrate-specific, membrane-bound enzymes II of the PEP-dependent carbohydrate: phosphotransferase system (PTS), specific for hexoses, hexosamines and hexitols, have been characterised in a series of isogenic and constitutive strains. In such mutants, lacking all but one enzyme II, the transport and vectorial phosphorylation activities as well as the chemotactical response in capillary tube assays have been compared. According to the data obtained, all enzymes II not only are directly involved in the transport and vectorial phosphorylation of their substrates, but they have also a primary role as the chemoreceptors for these substrates: (1) Metabolism of the attractant beyond the phosphorylation step is not a pre-requisite to eliciting positive chemotaxis. (2) Mutants, having only one enzyme II react in the capillary tube assay only to substrates of this enzyme II, but not to substrates of the missing enzymes II. This holds for enzymes II consisting of one membrane-bound protein as well as for systems containing a soluble factor III (FIII). (3) The substrate specificities or affinities, whether tested by transport and chemotaxis assays in vivo or by phosphorylation tests in vitro, are in correpondence. (4) The activities of enzymes II, regulated in a complex way at the level of enzyme synthesis and activity and tested as above, are also in agreement. (5) Mutants lacking the soluble proteins enzyme I or HPr of the PTS no longer respond chemotactically to any substrate taken up and phosphorylated by enzymes II. It is concluded that in PTS enzymes II some functions required for transport and chemotaxis are identical. It is suggested furthermore, that the alternation of intrinsic membrane-bound proteins between a phosphorylated and a dephosphorylated state, rather than binding of the substrate to the enzyme II, is the decisive stimulus in the chemotaxis toward carbohydrates taken up by these transport systems.
Similar content being viewed by others
References
Adler J (1969) Chemoreceptors in bacteria. Science 166:1588–1597
Adler J (1973) A method for measuring chemotaxis and use of the method to determine optimum conditions for chemotaxis by Escherichia coli. J Gen Microbiol 74:77–91
Adler J (1975) Chemotaxis in bacteria. Annu Rev Biochem 44:341–356
Adler J, Hazelbauer GL, Dahl MM (1973) Chemotaxis toward sugars in Escherichia coli. J Bacteriol 115:824–847
Adler J, Epstein W (1974) Phosphotransferase system enzymes as chemoreceptors for certain sugars in Escherichia coli chemotaxis. Proc Natl Acad Sci USA 71:2895–2899
Bachmann BJ, Low KB (1980) Linkage map of Escherichia coli K12, ed 6. Microbiol Rev 44:1–56
Clarke S, Koshland DE Jr: (1979) Membrane receptors for aspartate and serine in bacterial chemotaxis. J Biol Chem 254:9695–9702
Csonka LN, Clark AJ (1979) Deletions generated by the transposon Tn10 in the srl recA region of the Escherichia coli K12 chromosome. Genetics 93:321–343
Dills SS, Apperson A, Schmidt MR, Saier MH Jr (1980) Carbohydrate transport in bacteria. Microbiol Rev 44:385–418
Hazelbauer GL, Parkinson JS (1977) Bacterial chemotaxis. In: Reissig J (ed) Microbial interactions. Chapman and Hall, London, pp 61–98
Hazelbauer GL, Engström P, Harayama S (1981) Methyl-accepting chemotaxis protein III and transducer gene trg. J Bacteriol 145:43–49
Hedblom ML, Adler J (1980) Genetic and biochemical properties of Escherichia coli mutants with defects in serine chemotaxis. J Bacteriol 144:1048–1060
Jacobson GR, Lee CA, Saier MH Jr (1979) Purification of the mannitol-specific enzyme II of the Escherichia coli phosphoenolpyruvate: sugar phosphotransferase system. J Biol Chem 254:249–252
Lengeler J (1975a) Mutations affecting transport of the hexitols d-mannitol, d-glucitol, and galactitol in Escherichia coli K12: isolation and mapping. J Bacteriol 124:26–38
Lengeler J (1975b) Nature and properties of hexitol transport systems in Escherichia coli K12. J Bacteriol 124:39–47
Lengeler J (1980a) Characterization of mutants of Escherichia coli K12, selected by resistance to streptozotocin. Mol Gen Genet 179:49–54
Lengeler J (1980b) Die biologischen Funktionen bakterieller Transportsysteme. Forum Mikrobiol 3:359–365
Lengeler J, Steinberger H (1978a) Analysis of regulatory mechanisms controlling the synthesis of the hexitol transport systems in Escherichia coli K12. Mol Gen Genet 164:163–169
Lengeler J, Steinberger H (1978b) Analysis of regulatory mechanisms controlling the activity of the hexitol transport systems in Escherichia coli K12. Mol Gen Genet 167:75–82
Lin ECC (1970) The genetics of bacterial transport systems. Annu Rev Genet 4:225–262
Macnab RM (1978) Bacterial motility and chemotaxis: the molecular biology of a behavioral system. CRC Critical Rev Biochem 5:291–341
Macnab RM, Koshland DE Jr (1972) The gradient-sensing mechanism in bacterial chemotaxis. Proc Natl Acad Sci USA 69:2509–2512
Melton T, Hartman PE, Stratis JP, Lee TL, Davis AT (1978) Chemotaxis of Salmonella typhimurium to amino acids and some sugars. J Bacteriol 133:708–716
Ordal GW, Villani DP, Nicholas RA, Hamel FG (1978) Independence of proline chemotaxis and transport in Bacillus subtilis. J Biol Chem 253:4916–4919
Postma PW, Roseman S (1976) The bacterial phosphoenolpyruvate sugar phosphotransferase system. Biochim Biophys Acta 457:213–257
Ron EZ (1975) Growth rate of Enterobacteriaceae at elevated temperatures: limitation by methionine. J Bacteriol 124:243–246
Saier MH Jr (1977) Bacterial phosphoenolpyruvate: sugar phosphotransferase systems: structural, functional, and evolutionary interrelationships. Bacteriol Rev 41:856–871
Solomon E, Miyai K, Lin ECC (1973) Membrane translocation of mannitol in Escherichia coli without phosphorylation. J Bacteriol 114:723–728
Author information
Authors and Affiliations
Additional information
Communicated by H. Saedler
Rights and permissions
About this article
Cite this article
Lengeler, J., Auburger, A.M., Mayer, R. et al. The phosphoenolpyruvate-dependent carbohydrate: Phosphotransferase system enzymes II as chemoreceptors in chemotaxis of Escherichia coli K12. Molec. Gen. Genet. 183, 163–170 (1981). https://doi.org/10.1007/BF00270156
Received:
Issue Date:
DOI: https://doi.org/10.1007/BF00270156