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BioMed Research International
Volume 2015 (2015), Article ID 847945, 14 pages
http://dx.doi.org/10.1155/2015/847945
Review Article

Bioenergetics and the Role of Soluble Cytochromes c for Alkaline Adaptation in Gram-Negative Alkaliphilic Pseudomonas

T. Matsuno1,2 and I. Yumoto1,2

1Laboratory of Environmental Microbiology, Graduate School of Agriculture, Hokkaido University, Kita-ku, Sapporo 060-8589, Japan
2Bioproduction Research Institute, National Institute of Advanced Industrial Science and Technology (AIST), 2-17-2-1 Tsukisamu-Higashi Toyohira-ku, Sapporo 062-8517, Japan

Received 25 April 2014; Revised 27 November 2014; Accepted 29 November 2014

Academic Editor: Stanley Brul

Copyright © 2015 T. Matsuno and I. Yumoto. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. K. Horikoshi, “Prologue: definition, categories, distribution, origin and evolution, pioneering studies, and emerging studies, and emerging fields of extremophiles,” in Extremophiles Handbook, K. Horikoshi, G. Antranikian, A. T. Bull, F. T. Robb, and K. O. Stetter, Eds., 15, p. 3, Springer, Tokyo, Japan, 2011. View at Publisher · View at Google Scholar
  2. G. Antranikian and K. Egorova, “Extremophiles, a unique resource of biocatalysts for industrial biotechnology,” in Physiology and Biochemistry of Extremophiles, C. Gerday and N. Glansdorff, Eds., pp. 361–406, ASM Press, Washington, DC, USA, 2007. View at Google Scholar
  3. K. Horikoshi, Alkaliphiles, Kodansha, Tokyo, Japan; Springer, Berlin, Germany, 2006.
  4. T. Goto, T. Matsuno, M. Hishinuma-Narisawa et al., “Cytochrome c and bioenergetic hypothetical model for alkaliphilic Bacillus spp.,” Journal of Bioscience and Bioengineering, vol. 100, no. 4, pp. 365–379, 2005. View at Publisher · View at Google Scholar · View at Scopus
  5. I. Yumoto, “Environmental and taxonomic biodiversities of Gram-positive alkaliphiles,” in Physiology and Biochemistry of Extremophiles, C. Gerday and N. Glansdorff, Eds., pp. 295–310, ASM Press, Washington, DC, USA, 2007. View at Google Scholar
  6. T. A. Krulwich, D. B. Hicks, T. Swartz, and M. Ito, “Bioenergetic adaptations that support alkaliphily,” in Physiology and Biochemistry of Extremophiles, C. Gerday and N. Glansdorff, Eds., pp. 311–329, ASM Press, Washington, DC, USA, 2007. View at Publisher · View at Google Scholar
  7. I. Yumoto, K. Hirota, and K. Yoshimune, “Environmental distribution and taxonomic diversity of alkaliphiles,” in Extremophiles Handbook, K. Horikoshi, G. Antranikian, A. T. Bull, F. T. Robb, and K. O. Stetter, Eds., pp. 55–79, Springer, Tokyo, Japan, 2011. View at Google Scholar
  8. K. Horikoshi, “General physiology of alkaliphiles,” in Extremophiles Handbook, K. Horikoshi, G. Antranikian, A. T. Bull, F. T. Robb, and K. O. Stetter, Eds., pp. 99–118, Springer, Tokyo, Japan, 2011. View at Google Scholar
  9. T. A. Krulwich, J. Liu, M. Morino, M. Fujisawa, M. Ito, and D. B. Hicks, “Adaptive mechanisms of extreme alkaliphiles,” in Extremophiles Handbook, K. Horikoshi, G. Antranikian, A. T. Bull, F. T. Robb, and K. O. Stetter, Eds., pp. 119–139, Springer, Tokyo, Japan, 2011. View at Google Scholar
  10. R. Aono, M. Ito, and K. Horikoshi, “Occurrence of teichuronopeptide in cell walls of group 2 alkaliphilic Bacillus spp,” Journal of General Microbiology, vol. 139, no. 11, pp. 2739–2744, 1993. View at Publisher · View at Google Scholar · View at Scopus
  11. R. Aono, M. Ito, K. N. Joblin, and K. Horikoshi, “A high cell wall negative charge is necessary for the growth of the alkaliphile Bacillus lentus C-125 at elevated pH,” Microbiology, vol. 141, no. 11, pp. 2955–2964, 1995. View at Publisher · View at Google Scholar · View at Scopus
  12. R. Aono, M. Ito, and T. Machida, “Contribution of the cell wall component teichuronopeptide to pH homeostasis and alkaliphily in the alkaliphile Bacillus lentus C-125,” Journal of Bacteriology, vol. 181, no. 21, pp. 6600–6606, 1999. View at Google Scholar · View at Scopus
  13. R. Gilmour, P. Messner, A. A. Guffanti et al., “Two-dimensional gel electrophoresis analyses of pH-dependent protein expression in facultatively alkaliphilic Bacillus pseudofirmus OF4 lead to characterization of an S-layer protein with a role in alkaliphily,” Journal of Bacteriology, vol. 182, no. 21, pp. 5969–5981, 2000. View at Publisher · View at Google Scholar · View at Scopus
  14. I. Yumoto, “Bioenergetics of alkaliphilic Bacillus spp,” Journal of Bioscience and Bioengineering, vol. 93, no. 4, pp. 342–353, 2002. View at Publisher · View at Google Scholar · View at Scopus
  15. I. Yumoto, “Electron transport system in alkaliphilic Bacillus spp,” Recent Research Developments in Bacteriology, vol. 1, pp. 131–149, 2003. View at Google Scholar
  16. P. Mitchell, “Coupling of phosphorylation to electron and hydrogen transfer by a chemi-osmotic type of mechanism,” Nature, vol. 191, no. 4784, pp. 144–148, 1961. View at Publisher · View at Google Scholar · View at Scopus
  17. G. Seltman and O. Holst, The Bacterial Cell Wall, Springer, Berlin, Germany, 2002.
  18. K. Taira, J. Hirose, S. Hayashida, and K. Furukawa, “Analysis of bph operon from the polychlorinated biphenyl-degrading strain of Pseudomonas pseudoalcaligenes KF707,” The Journal of Biological Chemistry, vol. 267, no. 7, pp. 4844–4853, 1992. View at Google Scholar · View at Scopus
  19. S. Fedi, M. Carnevali, F. Fava, A. Andracchio, S. Zappoli, and D. Zannoni, “Polychlorinated biphenyl degradation activities and hybridization analyses of fifteen aerobic strains isolated from a PCB-contaminated site,” Research in Microbiology, vol. 152, no. 6, pp. 583–592, 2001. View at Publisher · View at Google Scholar · View at Scopus
  20. K. Hirota, K. Yamahira, K. Nakajima, Y. Nodasaka, H. Okuyama, and I. Yumoto, “Pseudomonas toyotomiensis sp. nov., a psychrotolerant facultative alkaliphile that utilizes hydrocarbons,” International Journal of Systematic and Evolutionary Microbiology, vol. 61, no. 8, pp. 1842–1848, 2011. View at Publisher · View at Google Scholar · View at Scopus
  21. N. J. Palleroni, “Genus I. Pseudomonas Migula 1894, 237AL,” in Bergy’s Manual of Systematic Bacteriology—Volume 2: The Proteobacteria Part B: The Gammaproteobacteria, D. J. Brenner, N. R. Krieg, J. T. Staley, and G. M. Garrity, Eds., pp. 323–379, Springer, New York, NY, USA, 2nd edition, 2005. View at Google Scholar
  22. Y. Sardessai and S. Bhosle, “Tolerance of bacteria to organic solvents,” Research in Microbiology, vol. 153, no. 5, pp. 263–268, 2002. View at Publisher · View at Google Scholar · View at Scopus
  23. Y. Ni, L. Song, X. Qian, and Z. Sun, “Proteomic analysis of Pseudomonas putida reveals an organic solvent tolerance-related gene mmsB,” PLoS ONE, vol. 8, no. 2, Article ID e55858, 2013. View at Publisher · View at Google Scholar · View at Scopus
  24. I. Yumoto, K. Yamazaki, M. Hishinuma et al., “Pseudomonas alcaliphila sp. nov., a novel facultatively psychrophilic alkaliphile isolated from seawater,” International Journal of Systematic and Evolutionary Microbiology, vol. 51, no. 2, pp. 349–355, 2001. View at Google Scholar · View at Scopus
  25. A. K. Borsodi, A. Micsinai, A. Rusznyák et al., “Diversity of alkaliphilic and alkalitolerant bacteria cultivated from decomposing reed rhizomes in a Hungarian soda lake,” Microbial Ecology, vol. 50, no. 1, pp. 9–18, 2005. View at Publisher · View at Google Scholar · View at Scopus
  26. B.-T. Wong and D.-J. Lee, “Pseudomonas yangmingensis sp. nov., an alkaliphilic denitrifying species isolated from a hot spring,” Journal of Bioscience and Bioengineering, vol. 117, no. 1, pp. 71–74, 2014. View at Publisher · View at Google Scholar · View at Scopus
  27. A. A. Guffanti and D. B. Hicks, “Molar growth yields and bioenergetic parameters of extremely alkaliphilic Bacillus species in batch cultures, and growth in a chemostat at pH 10.5,” Journal of General Microbiology, vol. 137, no. 10, pp. 2375–2379, 1991. View at Publisher · View at Google Scholar · View at Scopus
  28. S. Ogami, S. Hijikata, T. Tsukahara et al., “A novel membrane-anchored cytochrome c-550 of alkaliphilic Bacillus clarkii K24-1U: expression, molecular features and properties of redox potential,” Extremophiles, vol. 13, no. 3, pp. 491–504, 2009. View at Publisher · View at Google Scholar · View at Scopus
  29. K. Yoshimune, H. Morimoto, Y. Hirano, J. Sakamoto, H. Matsuyama, and I. Yumoto, “The obligate alkaliphiles Bacillus clarkii K24-1U retains extruded protons at the beginning of respiration,” Journal of Bioenergetics and Biomembrane, vol. 42, no. 2, pp. 111–116, 2010. View at Google Scholar
  30. P. Scherrer, U. Alexiev, T. Marti, H. G. Khorana, and M. P. Heyn, “Covalently bound pH-indicator dye at selected extracellular or cytoolasmic sites in bacteriorhodopsin. 1. Proton migration along the surface of bacteriorhodopsin micelles and delayed transfer from surface to bulk,” Biochemistry, vol. 33, no. 46, pp. 13684–13692, 1994. View at Publisher · View at Google Scholar
  31. U. Alexiev, “Covalently bound pH-indicator dyes at selected extracellular or cytoplasmic sites in bacteriorhodopsin. 2. Rotational orientation of helices D and e and kinetic correlation between M formation and proton release in bacteriorhodopsin micelles,” Biochemistry, vol. 33, no. 46, pp. 13693–13699, 1994. View at Publisher · View at Google Scholar · View at Scopus
  32. M. Gutman and E. Nachliel, “The dynamics of proton exchange between bulk and surface groups,” Biochimica et Biophysica Acta—Bioenergetics, vol. 1231, no. 2, pp. 123–138, 1995. View at Publisher · View at Google Scholar · View at Scopus
  33. Y. Marantz, O. Einarsdóttir, E. Nachliel, and M. Gutman, “Proton-collecting properties of bovine heart cytochrome c oxidase: kinetic and electrostatic analysis,” Biochemistry, vol. 40, no. 50, pp. 15086–15097, 2001. View at Publisher · View at Google Scholar · View at Scopus
  34. T. H. Haines and N. A. Dencher, “Cardiolipin: a proton trap for oxidative phosphorylation,” FEBS Letters, vol. 528, no. 1–3, pp. 35–39, 2002. View at Publisher · View at Google Scholar · View at Scopus
  35. J. I. Shioi, S. Matsuura, and Y. Imae, “Quantitative measurements of proton motive force and motility in Bacillus subtilis,” Journal of Bacteriology, vol. 144, no. 3, pp. 891–897, 1980. View at Google Scholar · View at Scopus
  36. T. Hirabayashi, T. Goto, H. Morimoto, K. Yoshimune, H. Matsuyama, and I. Yumoto, “Relationship between rates of respiratory proton extrusion and ATP synthesis in obligately alkaliphilic Bacillus clarkii DSM 8720T,” Journal of Bioenergetics and Biomembranes, vol. 44, no. 2, pp. 265–272, 2012. View at Publisher · View at Google Scholar · View at Scopus
  37. A. Y. Mulkidjanian, “Proton in the well and through the desolvation barrier,” Biochimica et Biophysica Acta: Bioenergetics, vol. 1757, no. 5-6, pp. 415–427, 2006. View at Publisher · View at Google Scholar · View at Scopus
  38. D. H. Murgida and P. Hildebrandt, “Proton-coupled electron transfer of cytochrome c,” Journal of the American Chemical Society, vol. 123, no. 17, pp. 4062–4068, 2001. View at Publisher · View at Google Scholar · View at Scopus
  39. R. J. Lewis, S. Belkina, and T. A. Krulwich, “Alkalophiles have much higher cytochrome contents than conventional bacteria and than their own non-alkalophilic mutant derivatives,” Biochemical and Biophysical Research Communications, vol. 95, no. 2, pp. 857–863, 1980. View at Publisher · View at Google Scholar · View at Scopus
  40. A. A. Guffanti, O. Finkelthal, D. B. Hicks et al., “Isolation and characterization of new facultatively alkalophilic strains of Bacillus species,” Journal of Bacteriology, vol. 167, pp. 766–773, 1986. View at Google Scholar · View at Scopus
  41. I. Yumoto, Y. Fukumori, and T. Yamanaka, “Purification and characterization of two membrane-bound c-type cytochromes from a facultative alkalophilic Bacillus,” Journal of Biochemistry, vol. 110, no. 2, pp. 267–273, 1991. View at Google Scholar · View at Scopus
  42. I. Yumoto, K. Nakajima, and K. Ikeda, “Comparative study on cytochrome content of alkaliphilic Bacillus strains,” Journal of Fermentation and Bioengineering, vol. 83, no. 5, pp. 466–469, 1997. View at Publisher · View at Google Scholar · View at Scopus
  43. M. W. Davidson, K. A. Gray, D. B. Knaff, and T. A. Krulwich, “Purification and characterization of two soluble cytochromes from the alkalophile Bacillus firmus RAB,” Biochimica et Biophysica Acta—Bioenergetics, vol. 933, no. 3, pp. 470–477, 1988. View at Publisher · View at Google Scholar · View at Scopus
  44. I. H. M. Vandenberghe, Y. Guisez, S. Ciurli, S. Benini, and J. J. Van Beeumen, “Cytochrome c-553 from the alkalophilic bacterium Bacillus pasteurii has the primary structure characteristics of a lipoprotein,” Biochemical and Biophysical Research Communications, vol. 264, no. 2, pp. 380–387, 1999. View at Publisher · View at Google Scholar · View at Scopus
  45. S. Benini, A. Gonzalez, W. R. Rypniewski, K. S. Wilson, J. J. Van Beeumen, and S. Ciurli, “Crystal structure of oxidized Bacillus pasteurii cytochrome c553 at 0.97-Å resolution,” Biochemistry, vol. 39, no. 43, pp. 13115–13126, 2000. View at Publisher · View at Google Scholar · View at Scopus
  46. C. Von Wachenfeldt and L. Hederstedt, “Physico-chemical characterisation of membrane-bound and water-soluble forms of Bacillus subtilis cytochrome c-550,” European Journal of Biochemistry, vol. 212, no. 2, pp. 499–509, 1993. View at Publisher · View at Google Scholar · View at Scopus
  47. P. Brzezinski and G. Larsson, “Redox-driven proton pumping by heme-copper oxidases,” Biochimica et Biophysica Acta—Bioenergetics, vol. 1605, no. 1–3, pp. 1–13, 2003. View at Publisher · View at Google Scholar · View at Scopus
  48. A. Higashibata, T. Fujiwara, and Y. Fukumori, “Studies on the respiratory system in alkaliphilic Bacillus; a proposed new respiratory mechanism,” Extremophiles, vol. 2, no. 2, pp. 83–92, 1998. View at Publisher · View at Google Scholar · View at Scopus
  49. T. Matsuno, N. Morishita, K. Yamazaki et al., “Cytochrome c-552 from gram-negative alkaliphilic Pseudomonas alcaliphila AL15-21T alters the redox properties at high pH,” Journal of Bioscience and Bioengineering, vol. 103, no. 3, pp. 247–254, 2007. View at Publisher · View at Google Scholar · View at Scopus
  50. T. Matsuno, Y. Mie, K. Yoshimune, and I. Yumoto, “Physiological role and redox properties of a small cytochrome c5, cytochrome c-552, from alkaliphile, Pseudomonas alcaliphila AL15-21T,” Journal of Bioscience and Bioengineering, vol. 108, no. 6, pp. 465–470, 2009. View at Publisher · View at Google Scholar · View at Scopus
  51. R. S. Pitcher, M. R. Cheesman, and N. J. Watmough, “Molecular and spectroscopic analysis of the cytochrome cbb3 oxidase from Pseudomonas stutzeri,” The Journal of Biological Chemistry, vol. 277, no. 35, pp. 31474–31483, 2002. View at Publisher · View at Google Scholar · View at Scopus
  52. A. Urbani, S. Gemeinhardt, A. Warne, and M. Saraste, “Properties of the detergent solubilised cytochrome c oxidase (cytochrome cbb3) purified from Pseudomonas stutzeri,” FEBS Letters, vol. 508, no. 1, pp. 29–35, 2001. View at Publisher · View at Google Scholar · View at Scopus
  53. T. Matsuno, K. Yoshimune, and I. Yumoto, “Physiological function of soluble cytochrome c-552 from alkaliphilic Pseudomonas alcaliphila AL15-21T,” Journal of Bioenergetics and Biomembranes, vol. 43, no. 5, pp. 473–481, 2011. View at Publisher · View at Google Scholar · View at Scopus
  54. K.-H. Choi and H. P. Schweizer, “An improved method for rapid generation of unmarked Pseudomonas aeruginosa deletion mutants,” BMC Microbiology, vol. 5, article 30, 2005. View at Publisher · View at Google Scholar · View at Scopus