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
2020-07-13
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 Bioeng10:845–864
    [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 Chem273:26670–26674
    [Google Scholar]
  4. Andrews J. F.. 1968; A mathematical model for the continuous culture of microorganisms utilizing inhibitory substrates. Biotechnol Bioeng10:707–723
    [Google Scholar]
  5. Brown A. D.. 1976; Microbial water stress. Bacteriol Rev40:803–846
    [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 J78:1748–1764
    [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 Microbiol4:496–506
    [Google Scholar]
  9. Edwards V. H.. 1970; Influence of high substrate concentrations on microbial kinetics. Biotechnol Bioeng12:679–712
    [Google Scholar]
  10. Galinski E. A.. 1993; Compatible solutes of halophilic eubacteria – molecular principles, water–solute interaction, stress protection. Cell Mol Life Sci49:487–496
    [Google Scholar]
  11. Galinski E. A.. 1995; Osmoadaptation in bacteria. Adv Microb Physiol37:272–328
    [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 Bacteriol184:3078–3085
    [Google Scholar]
  13. Grant W. D.. 2004; Life at low water activity. Philos Trans R Soc Lond B Biol Sci359:1249–1266
    [Google Scholar]
  14. Imhoff J. F., Trüper H. G.. 1977; Ectothiorhodospira halochloris sp. nov., a new extremely halophilic phototrophic bacterium containing bacteriochlorophyll b. Arch Microbiol114:115–121
    [Google Scholar]
  15. Kempf B., Bremer E.. 1998; Uptake and synthesis of compatible solutes as microbial stress responses to high-osmolality environments. Arch Microbiol170:319–330
    [Google Scholar]
  16. Kraegeloh A., Kunte H. J.. 2002; Novel insights into the role of potassium for osmoregulation in Halomonas elongata. Extremophiles6:453–462
    [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 Bacteriol187:1036–1043
    [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 Microbiol147:1–7
    [Google Scholar]
  19. Lee S. J., Gralla J. D.. 2004; Osmo-regulation of bacterial transcription via poised RNA polymerase. Mol Cell14:153–162
    [Google Scholar]
  20. Luong J. H. T.. 1987; Generalization of Monod kinetics for analysis of growth data with substrate inhibition. Biotechnol Bioeng29:242–248
    [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 1527;4–10
    [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 Microbiol19:363–365
    [Google Scholar]
  24. Morbach S., Krämer R.. 2002; Body shaping under water stress: osmosensing and osmoregulation of solute transport in bacteria. ChemBioChem3:384–397
    [Google Scholar]
  25. Oren A.. 1999; Bioenergetic aspects of halophilism. Microbiol Mol Biol Rev63:334–348
    [Google Scholar]
  26. Peters P., Galinski E. A., Trüper H. G.. 1990; The biosynthesis of ectoine. FEMS Microbiol Lett71:157–162
    [Google Scholar]
  27. Poolman B., Glaasker E.. 1998; Regulation of compatible solute accumulation in bacteria. Mol Microbiol29:397–407
    [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 Microbiol44:889–902
    [Google Scholar]
  29. Potts M.. 1994; Desiccation tolerance of prokaryotes. Microbiol Rev58:755–805
    [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 Bioeng57:306–313
    [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 Bioeng54:567–576
    [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 Microbiol138:1629–1638
    [Google Scholar]
  35. Shampine L. F., Reichelt M. W.. 1997; The MATLAB ODE Suite. SIAM J Sci Comput18:1–22
    [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 Biochem150:76–85
    [Google Scholar]
  37. Stouthamer A. H.. 1979; The search for correlation between theoretical and experimental growth yields. In Microbial Biochemistry pp1–47 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 Rev41:100–180
    [Google Scholar]
  39. Ventosa A., Nieto J. J., Oren A.. 1998; Biology of moderately halophilic aerobic bacteria. Microbiol Mol Biol Rev62:504–544
    [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 Bacteriol30:485–495
    [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 Microbiol136:705–712
    [Google Scholar]
  43. Wood J. M.. 1999; Osmosensing by bacteria: signals and membrane-based sensors. Microbiol Mol Biol Rev63:230–262
    [Google Scholar]
  44. Wood J. M.. 2006; Osmosensing by bacteria. Sci STKE357: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 Physiol130:437–460
    [Google Scholar]
  46. Yano T., Koga S.. 1969; Dynamic behavior of the chemostat subject to substrate inhibition. Biotechnol Bioeng11:139–153
    [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...

Most cited this month 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