1887

Microbiology Society logo

Volume 154, Issue 12

Changes in protein expression in PR1 at pH 5 and 7 with and without nickel Free

Abstract

PR1 (PR1) exhibits pH-dependent nickel (Ni) tolerance, with lower Ni toxicity observed at pH 5 than at pH 7. The Ni tolerance mechanism in PR1 is currently unknown, and traditional mechanisms of Ni resistance do not appear to be present. Therefore, 2D gel electrophoresis was used to examine changes in protein expression in PR1 with and without Ni (3.4 mM) at pH 5 and 7. Proteins with both a statistically significant and at least a twofold difference in expression level between conditions (pH, Ni) were selected and identified using MALDI-TOF-MS or LC-MS. Results showed increased expression of proteins involved in cell shape and membrane composition at pH 5 compared with pH 7. Scanning electron microscopy indicated elongated cells at pH 5 and 6 compared with pH 7 in the absence of Ni. Fatty acid methyl ester analysis showed a statistically significant difference in the percentages of long- and short-chain fatty acids at pH 5 and 7. These findings suggest that changes in membrane structure and function may be involved in the ability of PR1 to grow at higher concentrations of Ni at pH 5 than at pH 7.

  • Received:
  • Accepted:
  • Revised:
  • Published Online:
Keyword(s): ACP, acyl carrier protein , AHL, acylhomoserine lactone , FAME, fatty acid methyl ester , PHA, polyhydroxyalkanoate , PR1, Burkholderia vietnamiensis PR1301 , SEM, scanning electron microscopy , SOD, superoxide dismutase and TFE, 2,2,2-trifluoroethanol
SGM
Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.2008/017178-0
2008-12-01
2024-04-19
Loading full text...

Full text loading...

/deliver/fulltext/micro/154/12/3813.html?itemId=/content/journal/micro/10.1099/mic.0.2008/017178-0&mimeType=html&fmt=ahah

References

  1. Adriano D. C. 2001 Trace Elements in Terrestrial Environments: Biogeochemistry, Bioavailability, and Risks of Metals , 2nd edn. New York: Springer;
     [Google Scholar]
  2. Altincicek B., Kollas A. K., Eberl M., Wiesner J., Sanderbrand S., Hintz M., Beck E., Jomaa H. 2001; LytB, a novel gene of the 2- C-methyl-d-erythritol 4-phosphate pathway of isoprenoid biosynthesis in Escherichia coli . FEBS Lett 499:37–40
     [Google Scholar]
  3. Berggren K., Chernokalskaya E., Steinberg T. H., Kemper C., Lopez M. F., Diwu Z., Haugland R. P., Patton W. F. 2000; Background-free, high sensitivity staining of proteins in one- and two-dimensional sodium dodecyl sulfate-polyacrylamide gels using a luminescent ruthenium complex. Electrophoresis 21:2509–2521
     [Google Scholar]
  4. Bradford M. M. 1976; A rapid and sensitive method for quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254
     [Google Scholar]
  5. Brush M. 1998; Laid out flat: mini horizontal electrophoresis devices. Scientist 12:16–22
     [Google Scholar]
  6. Bury-Moné S., Thiberge J. M., Contreras M., Maitournam A., Labigne A., Reuse H. D. 2004; Responsiveness to acidity via metal ion regulators mediates virulence in the gastric pathogen Helicobacter pylori . Mol Microbiol 53:623–638
     [Google Scholar]
  7. Caldas T. D., El Yangoubi A., Richarme G. 1998; Chaperone properties of bacterial elongation factor EF-Tu. J Biol Chem 273:11478–11482
     [Google Scholar]
  8. Chamberlain N. R., Mehrtens B. G., Xiong Z., Kapral F. A., Boardman J. L., Rearick J. I. 1991; Correlation of carotenoid production, decreased membrane fluidity, and resistance to oleic acid killing in Staphylococcus aureus 18Z. Infect Immun 59:4332–4337
     [Google Scholar]
  9. Cobet A. B., Jones G. E., Albright J., Simon H., Wirsen C. 1971; The effect of nickel on a marine bacterium: fine structure of Arthrobacter marinus . J Gen Microbiol 66:185–196
     [Google Scholar]
  10. Conway B. A., Greenberg E. P. 2002; Quorum-sensing signals and quorum-sensing genes in Burkholderia vietnamiensis . J Bacteriol 184:1187–1191
     [Google Scholar]
  11. Dennis J. J., Zylstra G. J. 1998; Plasposons: modular self-cloning minitransposon derivatives for rapid genetic analysis of Gram-negative bacterial genomes. Appl Environ Microbiol 64:2710–2715
     [Google Scholar]
  12. Deshusses J. M. P., Burgess J. A., Scherf A., Wenger Y., Walter N., Converset V., Paesano S., Corthals G. L., Hochstrasser D. F., Sanchez J. C. 2003; Exploitation of specific properties of trifluoroethanol for extraction and separation of membrane proteins. Proteomics 3:1418–1424
     [Google Scholar]
  13. Dusenbery D. B. 1998; Fitness landscapes for effects of shape on chemotaxis and other behaviors of bacteria. J Bacteriol 180:5978–5983
     [Google Scholar]
  14. Ferianc P., Farewell A., Nystrom T. 1998; The cadmium-stress stimulon of Escherichia coli K-12. Microbiology 144:1045–1050
     [Google Scholar]
  15. Fierer N., Jackson R. B. 2006; The diversity and biogeography of soil bacterial communities. Proc Natl Acad Sci U S A 103:626–631
     [Google Scholar]
  16. Formstone A., Errington J. 2005; A magnesium-dependent mreB null mutant: implications for the role of mreB in Bacillus subtilis . Mol Microbiol 55:1646–1657
     [Google Scholar]
  17. Fozo E. M., Quivey R. G. Jr 2004; Shifts in the membrane fatty acid profile of Streptococcus mutans enhance survival in acidic environments. Appl Environ Microbiol 70:929–936
     [Google Scholar]
  18. Gaboriaud F., Bailet S., Dague E., Jorand F. 2005; Surface structure and nanomechanical properties of Shewanella putrefaciens bacteria at two pH values (4 and 10) determined by atomic force microscopy. J Bacteriol 187:3864–3868
     [Google Scholar]
  19. Geslin C., Llanos J., Prieur D., Jeanthon C. 2001; The manganese and iron superoxide dismutases protect Escherichia coli from heavy metal toxicity. Res Microbiol 152:901–905
     [Google Scholar]
  20. Guha C., Mookerjee A. 1979; Effect of nickel on macromolecular synthesis in Escherichia coli K-12. Nucleus 22:45–47
     [Google Scholar]
  21. Gygi S. P., Corthal G. L., Zhang Y., Rochon Y., Aebersold R. 2000; Evaluation of two-dimensional gel electrophoresis-based proteome analysis technology. Proc Natl Acad Sci U S A 97:9390–9395
     [Google Scholar]
  22. Hausinger R. P. 1993 Biochemistry of Nickel , 2nd edn. New York: Plenum;
     [Google Scholar]
  23. Hommais F., Laurent-Winter C., Labas V., Krin E., Tendeng C., Soutourina O., Danchin A., Bertin P. 2002; Effect of mild acid pH on the functioning of bacterial membranes in Vibrio cholerae . Proteomics 2:571–579
     [Google Scholar]
  24. Hornbaek T., Jakibsen M., Dynesen J., Nielson A. K. 2004; Global transcription profiles and intracellular pH regulation measured in Bacillus licheniformis upon external pH upshifts. Arch Microbiol 182:467–474
     [Google Scholar]
  25. Kang D., Gho Y. S., Suh M., Kang C. 2002; Highly sensitive and fast protein detection with Coomassie brilliant blue in sodium dodecyl sulfate-polyacrylamide gel electrophoresis. Bull Korean Chem Soc 23:1511–1512
     [Google Scholar]
  26. Kannenberg E. L., Poralla K. 1999; Hopanoid biosynthesis and function in bacteria. Naturwissenschaften 86:168–176
     [Google Scholar]
  27. Konings W. N., Albers S. V., Koning S., Driessen A. J. M. 2002; The cell membrane plays a crucial role in survival of bacteria and archaea in extreme environments. Antonie van Leeuwenhoek 81:61–72
     [Google Scholar]
  28. Kruse T., Bork-Jensen J., Gerdes K. 2005; The morphogenetic MreBCD proteins of Escherichia coli form an essential membrane-bound complex. Mol Microbiol 55:78–89
     [Google Scholar]
  29. Kudlicki W., Coffman A., Kramer G., Hardesty B. 1997; Renaturation of rhodanese by translational elongation factor (EF) Tu. Protein refolding by EF-Tu flexing. J Biol Chem 272:32206–32210
     [Google Scholar]
  30. Lanne B., Panfilov O. 2005; Protein staining influences the quality of mass spectra obtained by peptide mass fingerprinting after separation on 2-D gels. A comparison of staining with coomassie brilliant blue and Sypro Ruby. J Proteome Res 4:175–179
     [Google Scholar]
  31. Leaphart A. B., Thompson D. K., Huang K., Aim E., Wan X. F., Arkin A., Brown S. D., Wu L., Yan T. other authors 2006; Transcriptome profiling of Shewanella oneidensis gene expression following exposure to acidic and alkaline pH. J Bacteriol 188:1633–1642
     [Google Scholar]
  32. Lee S. Y. 1996; Bacterial polyhydroxyalkanoates. Biotechnol Bioeng 49:1–14
     [Google Scholar]
  33. Len A. C. L., Harty D. W. S., Jacques N. A. 2004; Stress-responsive proteins are upregulated in Streptococcus mutans during acid tolerance. Microbiology 150:1339–1351
     [Google Scholar]
  34. Lewenza S., Conway B., Greenberg E. P., Sokol P. A. 1999; Quorum sensing in Burkholderia cepacia: identification of the LuxRI homologs CepRI. J Bacteriol 181:748–756
     [Google Scholar]
  35. Lodish H., Berk A., Zipursky S. L., Matsudaira P., Baltimore D., Darnell J. E. 2000 Molecular Cell Biology , 4th edn. New York: W. H. Freeman;
     [Google Scholar]
  36. Lutter E., Lewenza S., Dennis J. J., Visser M. B., Sokol P. A. 2001; Distribution of quorum-sensing genes in the Burkholderia cepacia complex. Infect Immun 69:4661–4666
     [Google Scholar]
  37. Malott R. J., Sokol P. A. 2003; Cell-cell signaling mechanisms of the Burkholderia cepacia complex. Recent Res Dev Infect Immun 1:277–292
     [Google Scholar]
  38. Malott R. J., Sokol P. A. 2007; Expression of the bviIR and cepIR quorum-sensing systems of Burkholderia vietnamiensis . J Bacteriol 189:3006–3016
     [Google Scholar]
  39. Marrero J., Auling G., Coto O., Nies D. H. 2006; High-level resistance to cobalt and nickel but probably no transenvelope efflux: metal resistance in the Cuban Serratia marcescens strain C-1. Microb Ecol 53:123–133
     [Google Scholar]
  40. Miller M. B., Bassler B. L. 2001; Quorum sensing in bacteria. Annu Rev Microbiol 55:165–199
     [Google Scholar]
  41. Mirete S., de Figueras C. G., González-Pastor J. E. 2007; Novel nickel-resistance genes from the rhizosphere metagenome of acid mine drainage-adapted plants. Appl Environ Microbiol 73:6001–6011
     [Google Scholar]
  42. Molloy M. P., Herbert B. R., Walsh B. J., Tyler M. I., Traini M., Sanchez J. C., Hochstrasser D. F., Williams K. L., Gooley A. A. 1998; Extraction of membrane proteins by differential solubilization for separation using two-dimensional gel electrophoresis. Electrophoresis 19:837–844
     [Google Scholar]
  43. Müller D. J., Engel A. 1999; Voltage and pH-induced channel closure of porin OmpF visualized by atomic force microscopy. J Mol Biol 285:1347–1351
     [Google Scholar]
  44. Nies D. H. 2003; Efflux-mediated heavy metal resistance in prokaryotes. FEMS Microbiol Rev 27:313–319
     [Google Scholar]
  45. Nriagu J. O. 1980; Global cycle and properties of nickel. In Nickel in the Environment pp 1–26 Edited by Nriagu J. O. New York: Wiley;
     [Google Scholar]
  46. Park J.-H., Hwang I.-G., Kim J.-W., Lee S.-O., Conway B., Greenberg E. P., Lee K. 2001; Characterization of quorum-sensing signaling molecules produced by Burkholderia cepacia G4. J Microbiol Biotechnol 11:804–811
     [Google Scholar]
  47. Proctor J., Woodell S. R. J. 1975; The ecology of serpentine soils. Adv Ecol Res 9:255–366
     [Google Scholar]
  48. Putra S. R., Disch A., Bravo J. M., Rohmer M. 1998; Distribution of mevalonate and glyceraldehyde 3-phosphate/pyruvate routes for isoprenoid biosynthesis in some gram-negative bacteria and mycobacteria. FEMS Microbiol Lett 164:169–175
     [Google Scholar]
  49. Quivey R. G. Jr, Faustoferri R., Monahan K., Marquis R. 2000; Shifts in membrane fatty acid profiles associated with acid adaptations of Streptococcus mutans . FEMS Microbiol Lett 189:89–92
     [Google Scholar]
  50. Sabirova J. S., Ferrer M., Regenhardt D., Timmis K. N., Golyshin P. N. 2006; Proteomic insights into metabolic adaptations in Alcanivorax borkumensis induced by alkane utilization. J Bacteriol 188:3763–3773
     [Google Scholar]
  51. Sasser M. 1990 Identification of bacteria by gas chromatography of cellular fatty acids, MIDI Technical Note 101 Newark, DE: MIDI Inc;
     [Google Scholar]
  52. Sigler K., Chaloupka J., Brozmanová J., Stadler N., Höfer M. 1999; Oxidative stress in microorganisms. I. Microbial vs. higher cells – damage and defenses in relation to cell aging and death. Folia Microbiol (Praha) 44:587–624
     [Google Scholar]
  53. Simkiss K., Taylor M. G. 1995; Transport of metals across membranes. In Metal Speciation and Bioavailability in Aquatic Systems pp 2–44 Edited by Tessier A., Turner D. R. Chichester: Wiley;
     [Google Scholar]
  54. Singh R., Beriault R., Middaugh J., Hamel R., Chemier D., Appanna V. D., Kalyuzhuyi S. 2005; Aluminum-tolerant Pseudomonas fluorescens: ROS toxicity and enhanced NADPH production. Extremophiles 9:367–373
     [Google Scholar]
  55. Storch J., Schachter D. 1984; Dietary induction of acyl chain desaturases alters the lipid composition and fluidity of rat hepatocyte plasma membranes. Biochemistry 23:1165–1170
     [Google Scholar]
  56. Thanbichler M., Wang S. C., Shapiro L. 2005; The bacterial nucleoid: a highly organized and dynamic structure. J Cell Biochem 96:506–521
     [Google Scholar]
  57. Tian J., He A., Lawrence A. G., Liu P., Watson N., Sinskey A. J., Stubbe J. 2005; Analysis of transient polyhydroxybutyrate production in Wautersia eutropha H16 by quantitative western analysis and transmission electron microscopy. J Bacteriol 187:3825–3832
     [Google Scholar]
  58. Todt J. C., Rocque W. J., McGroarty E. J. 1992; Effects of pH on bacterial porin function. Biochemistry 31:10471–10478
     [Google Scholar]
  59. Van Nostrand J. D., Sowder A., Bertsch P. M., Morris P. J. 2005; Effect of pH on the toxicity of nickel and other divalent metals to Burkholderia cepacia PR1301 . Environ Toxicol Chem 24:2742–2750
     [Google Scholar]
  60. Van Nostrand J. D., Khijniak T. V., Gentry T. J., Novak M. T., Sowder A. G., Zhou J. Z., Bertsch P. M., Morris P. J. 2007a; Isolation and characterization of four Gram-positive nickel-tolerant microorganisms from contaminated sediments. Microb Ecol 53:670–682
     [Google Scholar]
  61. Van Nostrand J. D., Khijniak T. J., Neely B., Sattar M. A., Sowder A. G., Mills G., Bertsch P. M., Morris P. J. 2007b; The use of hydroxylapatite to reduce the toxicity of nickel and uranium to Burkholderia vietnamiensis PR1301 . Environ Sci Technol 41:1877–1882
     [Google Scholar]
  62. Wieczorek R., Pries A., Steinbüchel A., Mayer F. 1995; Analysis of a 24-kilodalton protein associated with the polyhydroxyalkanoic acid granules in Alcaligenes eutrophus . J Bacteriol 177:2425–2435
     [Google Scholar]
  63. Wilkins J. C., Homer K. A., Beighton D. 2001; Altered protein expression of Streptococcus oralis cultured at low pH revealed by two-dimensional gel electrophoresis. Appl Environ Microbiol 67:3396–3405
     [Google Scholar]
  64. Ybarra G. R., Webb R. 1998; Differential responses of GroEL and metallothionein genes to divalent metal cations and the oxyanions of arsenic in the cyanobacterium Synechococcus sp. strain PCC7942. In Proceedings of the 1998 Conference on Hazardous Waste Research Snowbird, UT, USA: 18–21 May 1998
     [Google Scholar]
  65. York G. M., Stubbe J., Sinskey A. J. 2001a; New insight into the role of the PhaP phasin of Ralstonia eutropha in promoting the synthesis of polyhydroxybutyrate. J Bacteriol 183:2394–2397
     [Google Scholar]
  66. York G. M., Junker B. H., Stubbe J., Sinskey A. J. 2001b; Accumulation of the PhaP phasin of Ralstonia eutropha is dependent on production of polyhydroxybutyrate in cells. J Bacteriol 183:4217–4226
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.2008/017178-0
Loading
Changes in protein expression in Burkholderia vietnamiensis PR1301 at pH 5 and 7 with and without nickel
Microbiology 154, 3813 (2008); https://doi.org/10.1099/mic.0.2008/017178-0
/content/journal/micro/10.1099/mic.0.2008/017178-0
/content/journal/micro/10.1099/mic.0.2008/017178-0
Loading

Data & Media loading...

Most cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error