1887

Abstract

Many molecular details of the ecophysiology of halophilic bacteria that use compatible solutes to maintain osmotic equilibrium have been examined. We ask whether the details are consistent and complete enough to predict growth and osmoregulation in these bacteria by integrating this information in a mathematical model. Parameterized for the halophilic organism , the model predicts the substrate and salt dependence of growth, the uptake of potassium and ectoine and the synthesis of ectoine. It is shown that salt (NaCl) dependence of growth can be modelled by substrate inhibition kinetics. Osmoregulation is known to involve accumulation of both ectoine and potassium glutamate in . Using published and newly determined parameters, osmoregulatory models using either direct turgor or two-step (turgor and potassium) signalling are compared. The results are consistent with a role for potassium as a second messenger for hyperosmotic stress. Simulations of osmotic upshifts show a transient overregulation of the intracellular solute levels, as has been previously observed in experiments. A possible adaptive value of this overregulation as ‘pre-emptive’ behaviour in an environment with frequent dry periods leading to steadily increasing osmolarity is proposed. As a result of growth parameter estimation, a maximum P : O value of 2 for can be inferred. In conclusion, the model developed here reproduces essential aspects of growth and osmoregulation in halophilic bacteria with a minimal set of assumptions.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.2007/012237-0
2008-10-01
2024-03-28
Loading full text...

Full text loading...

/deliver/fulltext/micro/154/10/2956.html?itemId=/content/journal/micro/10.1099/mic.0.2007/012237-0&mimeType=html&fmt=ahah

References

  1. Adam G., Läuger P., Stark G. 1977 Physikalische Chemie und Biophysik Berlin, Heidelberg, New York: Springer-Verlag;
    [Google Scholar]
  2. Aiba S., Shoda M., Nagatami M. 1968; Kinetics of product inhibition in alcohol fermentation. Biotechnol Bioeng 10:845–864
    [Google Scholar]
  3. Ajouz B., Berrier C., Garrigues A., Besnard M., Ghazi A. 1998; Release of thioredoxin via the mechanosensitive channel MscL during osmotic downshock of Escherichia coli cells. J Biol Chem 273:26670–26674
    [Google Scholar]
  4. Andrews J. F. 1968; A mathematical model for the continuous culture of microorganisms utilizing inhibitory substrates. Biotechnol Bioeng 10:707–723
    [Google Scholar]
  5. Brown A. D. 1976; Microbial water stress. Bacteriol Rev 40:803–846
    [Google Scholar]
  6. Burnham K. P., Anderson D. R. 2002 Model Selection and Multimodel Inference: a Practical Information-Theoretic Approach, 2nd edn. New York: Springer-Verlag;
    [Google Scholar]
  7. Cayley D. S., Guttman H. J., Record M. T. Jr 2000; Biophysical characterization of changes in amounts and activity of Escherichia coli cell and compartment water and turgor pressure in response to osmotic stress. Biophys J 78:1748–1764
    [Google Scholar]
  8. Claus D., Fahmy F., Rolf H. J., Tosunoglu N. 1983; Sporosarcina halophila sp. nov., an obligate, slightly halophilic bacterium from salt marsh soils. Syst Appl Microbiol 4:496–506
    [Google Scholar]
  9. Edwards V. H. 1970; Influence of high substrate concentrations on microbial kinetics. Biotechnol Bioeng 12:679–712
    [Google Scholar]
  10. Galinski E. A. 1993; Compatible solutes of halophilic eubacteria – molecular principles, water–solute interaction, stress protection. Cell Mol Life Sci 49:487–496
    [Google Scholar]
  11. Galinski E. A. 1995; Osmoadaptation in bacteria. Adv Microb Physiol 37:272–328
    [Google Scholar]
  12. Grammann K., Volke A., Kunte H. J. 2002; New type of osmoregulated solute transporter identified in halophilic members of the Bacteria domain: TRAP transporter TeaABC mediates uptake of ectoine and hydroxyectoine in Halomonas elongata DSM 2581T . J Bacteriol 184:3078–3085
    [Google Scholar]
  13. Grant W. D. 2004; Life at low water activity. Philos Trans R Soc Lond B Biol Sci 359:1249–1266
    [Google Scholar]
  14. Imhoff J. F., Trüper H. G. 1977; Ectothiorhodospira halochloris sp. nov., a new extremely halophilic phototrophic bacterium containing bacteriochlorophyll b . Arch Microbiol 114:115–121
    [Google Scholar]
  15. Kempf B., Bremer E. 1998; Uptake and synthesis of compatible solutes as microbial stress responses to high-osmolality environments. Arch Microbiol 170:319–330
    [Google Scholar]
  16. Kraegeloh A., Kunte H. J. 2002; Novel insights into the role of potassium for osmoregulation in Halomonas elongata . Extremophiles 6:453–462
    [Google Scholar]
  17. Kraegeloh A., Amendt B., Kunte H. J. 2005; Potassium transport in a halophilic member of the Bacteria domain: identification and characterization of the K+ uptake systems TrkH and TrkI from Halomonas elongata DSM 2581T . J Bacteriol 187:1036–1043
    [Google Scholar]
  18. Larsen P. I., Sydnes L. K., Landfald B., Strøm A. R. 1987; Osmoregulation in Escherichia coli by accumulation of organic osmolytes: betaines, glutamic acid and trehalose. Arch Microbiol 147:1–7
    [Google Scholar]
  19. Lee S. J., Gralla J. D. 2004; Osmo-regulation of bacterial transcription via poised RNA polymerase. Mol Cell 14:153–162
    [Google Scholar]
  20. Luong J. H. T. 1987; Generalization of Monod kinetics for analysis of growth data with substrate inhibition. Biotechnol Bioeng 29:242–248
    [Google Scholar]
  21. Maskow T., Babel W. 2001; Calorimetrically obtained information about the efficiency of ectoine synthesis from glucose in Halomonas elongata . Biochim Biophys Acta 15274–10
    [Google Scholar]
  22. McMeekin T. A., Olley J. N., Ross T., Ratkowsky D. A. 1993 Predictive Microbiology, Theory and Application, , 1st edn. Taunton: Research Studies Press;
    [Google Scholar]
  23. Miguelez E., Gilmour D. J. 1994; Regulation of cell-volume in the salt-tolerant bacterium Halomonas elongata . Lett Appl Microbiol 19:363–365
    [Google Scholar]
  24. Morbach S., Krämer R. 2002; Body shaping under water stress: osmosensing and osmoregulation of solute transport in bacteria. ChemBioChem 3:384–397
    [Google Scholar]
  25. Oren A. 1999; Bioenergetic aspects of halophilism. Microbiol Mol Biol Rev 63:334–348
    [Google Scholar]
  26. Peters P., Galinski E. A., Trüper H. G. 1990; The biosynthesis of ectoine. FEMS Microbiol Lett 71:157–162
    [Google Scholar]
  27. Poolman B., Glaasker E. 1998; Regulation of compatible solute accumulation in bacteria. Mol Microbiol 29:397–407
    [Google Scholar]
  28. Poolman B., Blount P., Folgering J. H. A., Friesen R. H. E., Moe P. C., van der Heide T. 2002; How do membrane proteins sense water stress?. Mol Microbiol 44:889–902
    [Google Scholar]
  29. Potts M. 1994; Desiccation tolerance of prokaryotes. Microbiol Rev 58:755–805
    [Google Scholar]
  30. Sauer T. 1995 Untersuchung zur Nutzung von Halomonas elongata für die Gewinnung kompatibler Solute PhD Thesis Rheinische Friedrich-Wilhelms Universität Bonn; Bonn, Germany:
    [Google Scholar]
  31. Sauer T., Galinski E. A. 1998; Bacterial milking: a novel bioprocess for production of compatible solutes. Biotechnol Bioeng 57:306–313
    [Google Scholar]
  32. Schröder M., Müller C., Posten C., Deckwer W.-D., Hecht V. 1997; Inhibition kinetics of phenol degradation from unstable steady-state data. Biotechnol Bioeng 54:567–576
    [Google Scholar]
  33. Seber G. A. F., Wild C. J. 1989 Nonlinear Regression New York: Wiley;
    [Google Scholar]
  34. Severin J., Wohlfahrt A., Galinski E. A. 1992; The predominant role of recently discovered tetrahydropyrimidines for the osmoadaptation of halophilic eubacteria. J Gen Microbiol 138:1629–1638
    [Google Scholar]
  35. Shampine L. F., Reichelt M. W. 1997; The MATLAB ODE Suite. SIAM J Sci Comput 18:1–22
    [Google Scholar]
  36. Smith P. K., Krohn R. I., Hermanson G. T., Mallia A. K., Gartner F. H., Provenzano M. D., Fujimoto E. K., Goeke N. M., Olson B. J., Klenk D. C. 1985; Measurement of protein using bicinchoninic acid. Anal Biochem 150:76–85
    [Google Scholar]
  37. Stouthamer A. H. 1979; The search for correlation between theoretical and experimental growth yields. In Microbial Biochemistry pp 1–47 Edited by Quayle J. R. Baltimore: University Park Press;
    [Google Scholar]
  38. Thauer R. K., Jungermann K., Decker K. 1977; Energy conservation in chemotrophic anaerobic bacteria. Bacteriol Rev 41:100–180
    [Google Scholar]
  39. Ventosa A., Nieto J. J., Oren A. 1998; Biology of moderately halophilic aerobic bacteria. Microbiol Mol Biol Rev 62:504–544
    [Google Scholar]
  40. Vreeland R. H. 1999; The family Halomonadaceae. In The Prokaryotes , edn 3.0. Edited by Dworkin M. New York: Springer;
    [Google Scholar]
  41. Vreeland R. H., Litchfield C. D., Martin E. L., Elliot E. 1980; Halomonas elongata, a new genus and species of extremely salt-tolerant bacteria. Int J Syst Bacteriol 30:485–495
    [Google Scholar]
  42. Wohlfarth A., Severin J., Galinski E. A. 1990; The spectrum of compatible solutes in heterotrophic halophilic eubacteria of the family Halomonadaceae. J Gen Microbiol 136:705–712
    [Google Scholar]
  43. Wood J. M. 1999; Osmosensing by bacteria: signals and membrane-based sensors. Microbiol Mol Biol Rev 63:230–262
    [Google Scholar]
  44. Wood J. M. 2006; Osmosensing by bacteria. Sci STKE 357:pe43
    [Google Scholar]
  45. Wood J. M., Bremer E., Csonka L. N., Kraemer R., Poolman B., van der Heide T., Smith L. T. 2001; Osmosensing and osmoregulatory compatible solute accumulation by bacteria. Comp Biochem Physiol A Mol Integr Physiol 130:437–460
    [Google Scholar]
  46. Yano T., Koga S. 1969; Dynamic behavior of the chemostat subject to substrate inhibition. Biotechnol Bioeng 11:139–153
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.2007/012237-0
Loading
/content/journal/micro/10.1099/mic.0.2007/012237-0
Loading

Data & Media loading...

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