Extremophiles

, Volume 14, Issue 2, pp 171–183 | Cite as

Occurrence and distribution of capB in Antarctic microorganisms and study of its structure and regulation in the Antarctic biodegradative Pseudomonas sp. 30/3

  • Gitika Panicker
  • Nazia Mojib
  • Teruaki Nakatsuji
  • Jackie Aislabie
  • Asim K. Bej
Original Paper

Abstract

The analysis of the cold-shock domain (CSD)-encoding genes, capB and cspA, by PCR amplification showed presence of capB in all 18 Antarctic Pseudomonas isolates, but the absence of cspA. Nucleotide sequence analysis of capB ORF from a biodegradative Pseudomonas 30/3 and its regulatory sequences including the promoter and 5′-UTR was determined and compared with the other CSD-encoding genes. Expression analysis using translational gene fusion of the putative capB promoter and its flanking sequence from Pseudomonas sp. 30/3 with lacZ′ exhibited a significant increase in β-galactosidase activity at 15 and 6°C. Unlike the expression of E. coli CspA, Pseudomonas sp. 30/3 showed a slow but steady increase of the CapB expression at 6°C. Subcellular localization of CapB at 6°C showed accumulation in and around the nucleoid whereas at 22 or 30°C, it was identified around the nucleoid as well as in the cytosol. Our study attempts to elucidate the detailed structure of capB from Pseudomonas 30/3 and the role of 5′UTR in the transcriptional regulation along with the possible role of CapB in transcription and translation suited for the cold adaptation of this bacterium in Antarctic environment.

Keywords

Cold adaptation capB Antarctic microorganism Pseudomonas 30/3 Immunolocalization 

References

  1. Ausubel FM, Brent R, Kingston RE, Moore DD, Smith JG, Sideman JG, Struhl K (eds) (1987) Current protocols in molecular biology. John Wiley & Sons, Inc., New York, pp 2.10–2.11Google Scholar
  2. Azam TA, Hiraga S, Ishihama A (2000) Two types of localization of the DNA-binding proteins within the Escherichia coli nucleoid. Genes Cells 5:613–626CrossRefPubMedGoogle Scholar
  3. Bae W, Xia B, Inouye M, Severinov K (2000) Escherichia coli CspA-family RNA chaperones are transcription antiterminators. Proc Natl Acad Sci USA 97:7784–7789CrossRefPubMedGoogle Scholar
  4. Bej AK, Saul D, Aislabie J (2000) Cold tolerant alkane-degrading Rhodococcus species from Antartica. Polar Biol 23:100–105CrossRefGoogle Scholar
  5. Berger F, Morellet N, Menu F, Potier P (1996) Cold shock and cold acclimation proteins in the psychrotrophic bacterium Arthrobacter globiformis S155. J Bacteriol 178:2999–3007PubMedGoogle Scholar
  6. Berger F, Normand P, Potier P (1997) capA, a cspA-like gene that encodes a cold acclimation protein in the psychrotrophic bacterium Arthrobacter globiformis SI55. J Bacteriol 179:5670–5676PubMedGoogle Scholar
  7. Brandi A, Pietroni P, Gulazeri CO, Pon CL (1996) Post-transcriptional regulation of CspA expression in Escherichia coli. Mol Microbiol 19:231–240CrossRefPubMedGoogle Scholar
  8. Etchegaray JP, Jones PG, Inouye M (1996) Differential thermoregulation of two highly homologous cold-shock genes, cspA and cspB, of Escherichia coli. Genes Cells 1:171–178CrossRefPubMedGoogle Scholar
  9. Fang L, Jiang W, Bae W, Inouye M (1997) Promoter-independent cold-shock induction of cspA and its derepression at 37°C by mRNA stabilization. Mol Microbiol 23:355–364CrossRefPubMedGoogle Scholar
  10. Fang L, Hou Y, Inouye M (1998) Role of the cold-box region in the 5′ untranslated region of the cspA mRNA in its transient expression at low temperature in Escherichia coli. J Bacteriol 180:90–95PubMedGoogle Scholar
  11. Feng W, Tejero R, Zimmerman DE, Inouye M, Montelione GT (1998) Solution NMR structure and backbone dynamics of the major cold shock protein (CspA) from Escherichia coli: evidence for conformational dynamics in the single-stranded RNA-binding site. Biochemistry 37:10881–10896CrossRefPubMedGoogle Scholar
  12. Francis KP, Stewart GS (1997) Detection and speciation of bacteria through PCR using universal major cold-shock protein primer oligomers. J Indust Microbiol Biotechnol 19:286–293CrossRefGoogle Scholar
  13. Giangrossi M, Exley RM, Le Hegarat F, Pon CL (2001) Different in vivo localization of the Escherichia coli proteins CspD and CspA. FEMS Microbiol Lett 202(2):171–176CrossRefPubMedGoogle Scholar
  14. Goldenberg D, Azar I, Oppenheim AB (1996) Differential mRNA stability of the cspA gene in the cold-shock response of Escherichia coli. Mol Microbiol 19:241–248CrossRefPubMedGoogle Scholar
  15. Goldenberg D, Azar I, Oppenheim AB, Brandi A, Pon CL, Gualerzi CO (1997) Role of Escherichia coli cspA promoter sequences and adaptation of translational apparatus in the cold shock response. Mol Gen Genet 256:282–290CrossRefPubMedGoogle Scholar
  16. Goldstein J, Pollit NS, Inouye M (1990) Major cold shock protein of Escherichia coli. Proc Natl Acad Sci USA 87:283–287CrossRefPubMedGoogle Scholar
  17. Graumann P, Marahiel MA (1996) Some like it cold: response of microorganisms to cold shock. Arch Microbiol 166:293–300CrossRefPubMedGoogle Scholar
  18. Graumann PL, Marahiel MA (1998) A superfamily of proteins that contain the cold-shock domain. Trends Biochem Sci 23:286–290CrossRefPubMedGoogle Scholar
  19. Gumley AW, Iniss WE (1996) Cold shock proteins and cold acclimation proteins in the psychrotrophic bacterium Pseudomonas putida Q5 and its transconjugants. Can J Microbiol 42:798–803CrossRefPubMedGoogle Scholar
  20. Harry EJ, Pogliano K, Losick R (1995) Use of immunofluorescence to visualize cell-specific gene expression during sporulation in Bacillus subtilis. J Bacteriol 177(12):3386–3389PubMedGoogle Scholar
  21. Hebraud M, Potier P (1999) Cold shock response and low temperature adaptation in psychrotrophic bacteria. J Mol Microbiol Biotechnol 1:211–219PubMedGoogle Scholar
  22. Hebraud M, Garry P, Labadie J (1993) Ubiquity of low molecular mass cold-shock proteins. Abstracts of the fourth international symposium on pseudomonas, p 59Google Scholar
  23. Hebraud M, Dubois E, Potier P, Labadie J (1994) Effect of growth temperatures on the protein levels in a psychrotrophic bacterium, Pseudomonas fragi. J Bacteriol 176:4017–4024PubMedGoogle Scholar
  24. Jiang W, Jones P, Inouye M (1993) Chloramphenicol induced the transcription of the major cold-shock gene of Escherichia coli, cspA. J Bacteriol 175:5824–5828PubMedGoogle Scholar
  25. Jiang W, Fang L, Inouye M (1996) The role of the 5′-end untranslated region of the mRNA for CspA, the major cold-shock protein of Escherichia coli, in cold-shock adaptation. J Bacteriol 178(16):4919–4925PubMedGoogle Scholar
  26. Lewis PJ, Thaker SD, Errington J (2000) Compartmentalization of transcription and translation in Bacillus subtilis. EMBO J 19:710–718CrossRefPubMedGoogle Scholar
  27. Lim J, Thomas T, Cavicchioli R (2000) Low temperature regulated DEAD-box RNA helicase from the Antarctic archaeon, Methanococcoides burtonii. J Mol Biol 297:553–567CrossRefPubMedGoogle Scholar
  28. Michel V, Lehoux I, Depret G, Anglade P, Labadie J, Hebraud M (1997) The cold shock response of the psychrotrophic bacterium Pseudomonas fragi involves four low-molecular-mass nucleic acid-binding proteins. J Bacteriol 179:7331–7342PubMedGoogle Scholar
  29. Miller JH (1972) Experiments in molecular genetics. Cold Spring Laboratory, Cold Spring Harbor, NY, pp 352–355Google Scholar
  30. Mitta M, Fang L, Inouye M (1997) Deletion analysis of cspA of Escherichia coli: requirement of the AT-rich UP element for cspA transcription and the downstream box in the coding region for its cold shock induction. Mol Microbiol 26:321–335CrossRefPubMedGoogle Scholar
  31. Newkirk K, Feng W, Jiang W, Tejero R, Emerson SD, Inouye M, Montelione GT (1994) Solution NMR structure of the major cold shock protein (CspA) from Escherichia coli: identification of a binding epitope for DNA. Proc Natl Acad Sci USA 91:5114–5118CrossRefPubMedGoogle Scholar
  32. Notredame C, Higgins DG, Heringa J (2000) T-Coffee: a novel method for fast and accurate multiple sequence alignment. J Mol Biol 302:205–217CrossRefPubMedGoogle Scholar
  33. Panicker G, Aislabie J, Saul D, Bej A (2002) Cold tolerance of Pseudomonas sp. 30/3 isolated from oil-contaminated soil, Antarctica. Pol Biol 225:5–11CrossRefGoogle Scholar
  34. Phadtare S, Alsina J, Inouye M (1999) Cold-shock response and cold-shock proteins. Curr Opin Microbiol 2(2):175–180CrossRefPubMedGoogle Scholar
  35. Pikuta EV, Hoover RB (2007) Microbial extremophiles at the limits of life. Crit Rev Microbiol 33:183–209CrossRefPubMedGoogle Scholar
  36. Roberts ME, Inniss WE (1992) The synthesis of cold shock proteins and cold acclimation proteins in the psychrophilic bacterium Aquaspirillum articum. Curr Microbiol 25:275–278CrossRefGoogle Scholar
  37. Schindelin H, Marahiel MA, Heinemann U (1993) Universal nucleic acid-binding domain revealed by crystal structure of the B. subtilis major cold-shock protein. Nature 364:164–168CrossRefPubMedGoogle Scholar
  38. Schindelin H, Jiang W, Inouye M, Heinemann U (1994) Crystal structure of CspA, the major cold shock protein of Escherichia coli. Proc Natl Acad Sci USA 91:5119–5123CrossRefPubMedGoogle Scholar
  39. Schindler T, Graumann PL, Perl D, Ma S, Schmid FX, Marahiel MA (1999) The family of cold shock proteins of Bacillus subtilis. Stability and dynamics in vitro and in vivo. J Biol Chem 274:3407–3413CrossRefPubMedGoogle Scholar
  40. Somerville J (1999) Activities of cold-shock domain proteins in translation control. Bioessays 21:319–325CrossRefGoogle Scholar
  41. Tanabe H, Goldstein J, Yang M, Inouye M (1992) Identification of the promoter region of the Escherichia coli major cold shock gene, cspA. J Bacteriol 174:3867–3873PubMedGoogle Scholar
  42. Thieringer HA, Jones PG, Inouye M (1998) Cold shock adaptation. BioEssays 20:49–57CrossRefPubMedGoogle Scholar
  43. Wang N, Yamanka K, Inouye M (1999) CspI, the ninth member of the CspA family of Escherichia coli, is induced upon cold shock. J Bacteriol 181:1603–1609PubMedGoogle Scholar
  44. Weber MHW, Volkov AV, Fricke I, Marahiel MA, Graumann PL (2001) Localization of cold shock proteins to cytosolic spaces surrounding nucleoids in Bacillus subtilis depends on active transcription. J Bacteriol 183(21):6435–6443CrossRefPubMedGoogle Scholar
  45. Whyte LG, Inniss WE (1992) Cold shock proteins and cold acclimation proteins in a psychrotrophic bacterium. Can J Microbiol 38:1281–1285CrossRefGoogle Scholar
  46. Wolffe AP (1994) Structural and functional properties of the evolutionarily ancient Y-box family of nucleic acid binding proteins. Bioessays 16:245–251CrossRefPubMedGoogle Scholar
  47. Wolffe AP, Tafuri S, Ranjan M, Familari M (1992) The Y-box factors: a family of nucleic acid binding proteins conserved from Escherichia coli to man. New Biol 4:290–298PubMedGoogle Scholar
  48. Wouters JA, Rombouts FM, Kuipers OP, de Vos WM, Abee T (2000) The role of cold-shock proteins in low-temperature adaptation of food-related bacteria. Syst Appl Microbiol 23:165–173PubMedGoogle Scholar
  49. Yamanka K, Fang L, Inouye M (1998) The CspA family in Escherichia coli: multiple gene duplication for stress adaptation. Mol Microbiol 27:247–255CrossRefGoogle Scholar
  50. Yamanka K, Mitta M, Inouye M (1999) Mutation analysis of the 5′ untranslated region of the cold shock cspA mRNA of Escherichia coli. J Bacteriol 181:6284–6291Google Scholar

Copyright information

© Springer 2009

Authors and Affiliations

  • Gitika Panicker
    • 1
    • 2
  • Nazia Mojib
    • 1
  • Teruaki Nakatsuji
    • 1
    • 3
  • Jackie Aislabie
    • 4
  • Asim K. Bej
    • 1
    • 5
  1. 1.Department of BiologyUniversity of Alabama at BirminghamBirminghamUSA
  2. 2.Center for Disease Control and PreventionAtlantaUSA
  3. 3.VA Medical CenterUniversity of California at San DiegoSan DiegoUSA
  4. 4.Landcare ResearchHamiltonNew Zealand
  5. 5.Department of BiologyUniversity of Alabama at BirminghamBirminghamUSA

Personalised recommendations