Journal of Biosciences

, Volume 32, Issue 3, pp 559–568 | Cite as

The Kdp-ATPase system and its regulation

Article

Abstract

K+, the dominant intracellular cation, is required for various physiological processes like turgor homeostasis, pH regulation etc. Bacterial cells have evolved many diverse K+ transporters to maintain the desired concentration of internal K+. In E. coli, the KdpATPase (comprising of the KdpFABC complex), encoded by the kdpFABC operon, is an inducible high-affinity K+ transporter that is synthesised under conditions of severe K+ limitation or osmotic upshift. The E. coli kdp expression is transcriptionally regulated by the KdpD and KdpE proteins, which together constitute a typical bacterial two-component signal transduction system. The Kdp system is widely dispersed among the different classes of bacteria including the cyanobacteria. The ordering of the kdpA, kdpB and kdpC is relatively fixed but the kdpD/E genes show different arrangements in distantly related bacteria. Our studies have shown that the cyanobacterium Anabaena sp. strain L-31 possesses two kdp operons, kdp1 and kdp2, of which, the later is expressed under K+ deficiency and desiccation. Among the regulatory genes, the kdpD ORF of Anabaena L-31 is truncated when compared to the kdpD of other bacteria, while a kdpE-like gene is absent. The extremely radio-resistant bacterium, Deinococcus radiodurans strain R1, also shows the presence of a naturally short kdpD ORF similar to Anabaena in its kdp operon. The review elaborates the expression of bacterial kdp operons in response to various environmental stress conditions, with special emphasis on Anabaena. The possible mechanism(s) of regulation of the unique kdp operons from Anabaena and Deinococcus are also discussed.

Keywords

Anabaena Escherichia coli, Kdp ATPase potassium limitation signal transduction two component system 

Abbreviations used

CTD

C-terminal domain

K+

potassium

NTD

N-terminal domain

ORF

open reading frame

RR

response regulator

SK

sensor kinase

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References

  1. Abee T, Knoll J, Hellingwerf K J, Bakker E P, Siebers A and Konings W N 1992a A Kdp-like, high affinity, K+-translocating ATPase is expressed during growth of Rhodobacter sphaeroides in low potassium media; Arch. Microbiol. 158 374–380CrossRefGoogle Scholar
  2. Abee T, Seibers A, Altendorf K and Konings W N 1992b Isolation and characterization of high-affinity K+-translocating ATPase from Rhodobacter sphaeroides; J. Bacteriol. 174 6911–6917PubMedGoogle Scholar
  3. Alahari A and Apte S K 1998 Pleiotropic effects of potassium deficiency in heterocystous, nitrogen-fixing cyanobacterium, Anabaena torulosa; Microbiology 144 1557–1563PubMedCrossRefGoogle Scholar
  4. Alahari A, Ballal A and Apte S K 2001 Regulation of the potassium-dependent Kdp-ATPase expression in the nitrogen-fixing cyanobacterium Anabaena torulosa; J. Bacteriol. 183 5578–5581CrossRefGoogle Scholar
  5. Apte S K and Alahari A 1994 Role of alkali cations (K+ and Na+) in cyanobacterial nitrogen fixation and adaptation to salinity and osmotic stress; Indian J. Biochem. Biophys. 31 267–279PubMedGoogle Scholar
  6. Asha H and Gowrishankar J 1993 Regulation of kdp operon expression in Escherichia coli: evidence against turgor as a signal for transcriptional control; J. Bacteriol. 181 4528–4537Google Scholar
  7. Bakker E P, Borchard A, Michels M, Altendorf K and Siebers A 1987 High-affinity potassium uptake system in Bacillus acidocaldarius showing immunological cross-reactivity with the Kdp system from Escherichia coli; J. Bacteriol. 169 4342–4348PubMedGoogle Scholar
  8. Ballal A and Apte S K 2005 Differential expression of the two kdp operons in the nitrogen-fixing cyanobacterium Anabaena sp. strain L-31; Appl. Environ. Microbiol. 71 5297–5303PubMedCrossRefGoogle Scholar
  9. Ballal A, Bramkamp M, Rajaram H, Zimmann P, Apte S K and Altendorf K 2005 An atypical KdpD homologue from the cyanobacterium Anabaena sp. strain L-31: cloning, in vivo expression and interaction with Escherichia coli KdpD-CTD; J. Bacteriol. 187 4921–4927PubMedCrossRefGoogle Scholar
  10. Ballal A, Heermann R, Jung K, Gassel M, Apte S K and Altendorf K 2002 A chimeric Anabaena/Escherichia coli KdpD protein (Anacoli KdpD) functionally interacts with E. coli KdpE and activates kdp expression in E. coli; Arch. Micobiol. 178 141–148CrossRefGoogle Scholar
  11. Behrens M, Schreiber W and Durre P 2001 The high-affinity K+-translocating complex from Clostridium acetobutylicum consists of 6 subunits; Anaerobe 7 159–169CrossRefGoogle Scholar
  12. Berry S, Esper B, Karandashova I, Teuber M, Elanskaya I, Roegner M and Hagemann M 2003 Potassium uptake in the unicellular cyanobacterium Synechocystis sp. strain 6803 mainly depends on a Ktr-like system encoded by slr1509 (ntpJ); FEBS Lett. 548 53–58PubMedCrossRefGoogle Scholar
  13. Booth I R 1985 Regulation of cytoplasmic pH in bacteria; Microbiol. Rev. 49 359–378PubMedGoogle Scholar
  14. Bremer E and Kramer R 2000 Coping with osmotic challenges: Osmoregulation through accumulation and release of compatible solutes in bacteria; in Bacterial stress responses (eds) G Storz and R Hengge-Aronis (Washington, D C: ASM Press) pp 79–97Google Scholar
  15. Bronstead L, Kallipolitis B H, Ingmer H and Knochel S 2003 kdpE and a putative RsbQ homologue contribute to growth of Listeria monocytogenes at high osmolarity and low temperature; FEMS Microbiol. Lett. 219 233–239CrossRefGoogle Scholar
  16. Cairney J, Booth I R and Higgins C F 1985 Salmonella typhimurium proP gene encodes a transport system for the osmoprotectant glycine betaine; J. Bacteriol. 174 1218–1223Google Scholar
  17. Cole S T, Brosch R, Parkhill J, Garnier T, Churcher C, Harris D et al 1998 Deciphering the biology of Mycobacterium tuberculosis from the complete genome sequence; Nature (London) 393 537–544CrossRefGoogle Scholar
  18. Csonka L N and A D Hanson 1991 Prokaryotic osmoregulation: Genetics and physiology; Annu. Rev. Microbiol. 45 569–606PubMedCrossRefGoogle Scholar
  19. Csonka L N and Epstein W 1996 Osmoregulation; in Escherichia coli and Salmonella: cellular and molecular biology (eds) F C Niedhardt et al (Washington, D C: ASM Press) 2nd edition, pp 1210–1223Google Scholar
  20. Dunlap V J and Csonka L N 1985 Osmotic regulation of L-proline transport in Salmonella typhimurium; J. Bacteriol. 163 296–304PubMedGoogle Scholar
  21. Epstein W 1986 Osmoregulation of K+ transport in Escherichia coli; FEMS Microbiol. Rev. 39 73–78CrossRefGoogle Scholar
  22. Epstein W 1992 Kdp, a bacterial P-type ATPase whose expression and activity are regulated by turgor pressure; Acta Physiol. Scand. 146 836–843Google Scholar
  23. Epstein W 2003 The roles and regulation of potassium in bacteria; Prog. Nucleic Acid Res. Mol. Biol. 75 293–320PubMedCrossRefGoogle Scholar
  24. Epstein W and Kim B S 1971 Potassium transport loci in Escherichia coli K-12; J. Bacteriol. 101 836–843Google Scholar
  25. Gassel M, Mollenkamp T, Puppe W and Altendorf K 1999 The KdpF subunit is a part of the K+-translocating Kdp complex of the Escherichia coli and is responsible for stabilization of the complex in vitro; J. Biol. Chem. 274 37901–37907PubMedCrossRefGoogle Scholar
  26. Gowrishankar J 1985 Identification of osmoresponsive genes in E. coli: Evidence for participation of potassium and proline transport systems in osmoregulation; J. Bacteriol. 164 434–445PubMedGoogle Scholar
  27. Gowrishankar J 1987 A model for the regulation of the expression of the potassium-transport operon, kdp, in Escherichia coli; J. Genet. 66 87–92CrossRefGoogle Scholar
  28. Hafer J, Siebers A and Bakker E P 1989 The high-affinity K+ translocating ATPase complex from Bacillus acidocaldarius consists of three subunits; Mol. Microbiol. 3 487–495PubMedCrossRefGoogle Scholar
  29. Heermann R, Altendorf K and Jung K 2003 The N-terminal input domain of the sensor kinase KdpD of Escherichia coli stabilizes the interaction between the cognate response regulator KdpE and the corresponding DNA-binding site; J. Biol. Chem. 278 51277–51284PubMedCrossRefGoogle Scholar
  30. Heermann R, Altendorf K and K Jung 2000 The hydrophilic N-terminal domain complements the membrane-anchored C-terminal domain of the sensor kinase KdpD of Escherichia coli; J. Biol. Chem. 275 17080–17085PubMedCrossRefGoogle Scholar
  31. Hesse J E, Wieczorek L, Altendorf K, Reicin A S, Dorus E and Epstein W 1984 Sequence homology between two membrane transport ATPases, the Kdp-ATPase of Escherichia coli and the Ca2+-ATPase of sarcoplasmic reticulum; Proc. Natl. Acad. Sci. USA 81 4746–4750PubMedCrossRefGoogle Scholar
  32. Jung K and K Altendorf 1998 Truncation of amino acids 12-228 causes deregulation of the phosphatase activity of the sensor kinase KdpD of Escherichia coli; J. Biol. Chem. 273 17406–17410PubMedCrossRefGoogle Scholar
  33. Kaneko T, Nakamura Y, Wolk C P, Kuritz T, Sasamoto S, Watanabe A, et al 2001 Complete genomic sequence of the filamentous nitrogen-fixing cyanobacterium Anabaena sp. strain PCC 7120; DNA Res. 8 205–213PubMedCrossRefGoogle Scholar
  34. Kaneko T, Sato S, Kotani H, Tanaka A, Asamizu E, Nakamura Y, et al 1996 Sequence analysis of the genome of the unicellular cyanobacterium Synechocystis sp. strain PCC 6803. II. Sequence determination of the entire genome and assignment of potential protein-coding regions; DNA Res. 3 109–136PubMedCrossRefGoogle Scholar
  35. Kanesaki Y, Suzuki I, Allakhverdiev S I, Mikami K and N Murata 2002 Salt stress and hyperosmotic stress regulate expression of different set of genes in Synechocystis PCC 6803; Biochem. Biophys. Res. Commun. 290 339–348PubMedCrossRefGoogle Scholar
  36. Katoh H, Asthana R K and Ohmori M 2004 Gene expression in the cyanobacterium Anabaena sp. PCC 7120 under desiccation; Microb. Ecol. 47 164–174PubMedCrossRefGoogle Scholar
  37. Laimins L A, Rhoads D B and Epstein W 1981 Osmotic control of kdp operon expression in Escherichia coli; Proc. Natl. Acad. Sci. USA 78 464–468PubMedCrossRefGoogle Scholar
  38. Malli R and Epstein W 1998 Expression of the Kdp-ATPase is consistent with regulation by turgor pressure; J. Bacteriol. 180 5012–5018Google Scholar
  39. Matsuda N, Kobayashi H, Katoh H, Ogawa T, Futatsugi L, Nakamura T, Bakker E P and N Uozomi 2004 Na+-dependent K+ uptake Ktr system from the cyanobacterium Synechocystis sp. PCC 6803 and its role in early phases of cell adaptation to hyperosmotic shock; J. Biol. Chem. 279 54952–54962PubMedCrossRefGoogle Scholar
  40. May G, Faatz E, Villarejo M and Bremer E 1986 Binding protein-dependent transport of glycine betaine and its osmotic regulation in Escherichia coli K-12; Mol. Gen. Genet. 205 225–233PubMedCrossRefGoogle Scholar
  41. McLaggan D, Naprstek J, Buurman T, Ed and Epstein W 1994 Interdependence of K+ and glutamate accumulation during osmotic adaptation of Escherichia coli; J. Biol. Chem. 269 1911–1917PubMedGoogle Scholar
  42. Nakashima K, Sugiura A, Kanamaru K and Mizuno T 1993 Signal transduction between the two regulatory components involved in the regulation of the kdpABC operon in Escherichia coli-phosphorylation-dependent functioning of the positive regulator KdpE; Mol. Microbiol. 7 109–116PubMedCrossRefGoogle Scholar
  43. Nakashima K, Sugiura A, Momoi H and Mizuno T 1992 Phosphotransfer signal transduction between two regulatory factors involved in the osmoregulated kdp operon in Escherichia coli; Mol. Microbiol. 6 1777–1784PubMedCrossRefGoogle Scholar
  44. Polarek J W, Williams G and Epstein W 1992 The products of kdpDE operon are required for expression of the Kdp-ATPase of Escherichia coli; J. Bacteriol. 174 2145–2151PubMedGoogle Scholar
  45. Poolman B and E Glaasker 1998 Regulation of compatible solute accumulation in bacteria; Mol Microbiol. 29 397–407PubMedCrossRefGoogle Scholar
  46. Prince W S and Villarejo M R 1990 Osmotic control of proU transcription is mediated through direct action of potassium glutamate on the transcription complex; J. Biol. Chem. 265 17673–17679PubMedGoogle Scholar
  47. Puppe W, Zimmann P, Jung K, Lucassen M and Altendorf K 1996 Characterization of truncated forms of the KdpD protein, the sensor kinase of the K+-translocating Kdp system of Escherichia coli; J. Biol. Chem. 271 25027–25034PubMedCrossRefGoogle Scholar
  48. Rhoads D B, Laimins L and Epstein W 1978 Functional Organization of the kdp genes of Escherichia coli K-12; J. Bacteriol. 135 445–452PubMedGoogle Scholar
  49. Rothenbucher M C, Facey S J, Kiefer D, Kossmann M and Kuhn A 2006 The cytoplasmic C-terminal domain of the Escherichia coli KdpD protein functions as K+ sensor; J. Bacteriol. 188 1959–1958CrossRefGoogle Scholar
  50. Schleussinger E, Schmid R and Bakker E P 2006 New type of kdp region with a split sensor-kinase kdpD gene located within two divergent kdp operons from the thermoacidophilic bacterium Alicyclobacillus acidocaldarius; Biochim. Biophys. Acta 1759 437–441PubMedGoogle Scholar
  51. Steyn A J, Joseph J and Bloom B R 2003 Interaction of the sensor module of Mycobacterium tuberculosis H37Rv KdpD with members of the Lpr family; Mol. Microbiol. 47 1075–1089PubMedCrossRefGoogle Scholar
  52. Stumpe S, Schlösser A, Schleyer M and Bakker E P 1996 K+ circulation across the procaryotic cell membrane: K+-uptake systems; in Handbook of biological physics, (eds) W N Konings, H R Kaback and J S Lolkema Vol. 2. (Amsterdam: Elsevier Science B V) pp 473–499Google Scholar
  53. Suelter C H 1970 Enzymes activated by monovalent cations: patterns and predictions for the enzyme-catalyzed based reactions are explored; Science 168 789–795PubMedCrossRefGoogle Scholar
  54. Sugiura A, Hirokawa K, Nakashima K and Mizuno T 1994 Signalsensing mechanisms of the putative osmosensor KdpD in Escherichia coli; Mol. Microbiol. 14 929–938PubMedCrossRefGoogle Scholar
  55. Treuner-Lange A, Kuhn A and Dürre P 1997 The kdp system of Clostridium acetobutylicum: Cloning, sequencing, and transcriptional regulation in response to potassium concentration; J. Bacteriol. 179 4501–4512PubMedGoogle Scholar
  56. Voelkner P, Puppe W and Altendorf K 1993 Characterisation of the KdpD protein, the sensor kinase of the K+-translocating system of Escherichia coli; Eur. J. Biochem. 217 1019–1026PubMedCrossRefGoogle Scholar
  57. Walderhaug M O, Litwack E D and Epstein W 1989 Wide distribution of homologs of Escherichia coli Kdp K+-ATPase among Gram-negative bacteria; J. Bacteriol. 171 1192–1195PubMedGoogle Scholar
  58. Walderhaug M O, Polarek J W, Voelkner P, Daniel J M, Hesse J E, Altendorf K and Epstein W 1992 KdpD and KdpE, proteins that control expression of the kdpABC operon, are members of the two-component sensor-effector class of regulators; J. Bacteriol. 174 2152–2159PubMedGoogle Scholar
  59. Walker J E, Saraste M, Runswick M and Gay N J 1982 Distantly related sequences in α-and β-subunits of ATP synthase, myosin kinases and other ATP requiring enzymes and a common nucleotide binding fold; EMBO J. 1 945–951PubMedGoogle Scholar
  60. White O, Eisen J A, Heidelberg J F, Hickey E K, Peterson J D, Dodson R J et al 1999 Genome sequence of the radioresistant bacterium Deinococcus radiodurans R1; Science 286 1571–1577PubMedCrossRefGoogle Scholar
  61. Zimmann P, Puppe W and Altendorf K 1995 Membrane topology analysis of the sensor kinase KdpD of Escherichia coli; J. Biol. Chem. 270 28282–28288PubMedCrossRefGoogle Scholar

Copyright information

© Indian Academy of Sciences 2007

Authors and Affiliations

  1. 1.Molecular Biology DivisionBhabha Atomic Research CentreTrombay, MumbaiIndia

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