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13 - Energy, environment and microbial survival

Published online by Cambridge University Press:  05 September 2012

Byung Hong Kim  and
Geoffrey Michael Gadd
Byung Hong Kim
Affiliation:
Korea Institute of Science and Technology, Seoul
Geoffrey Michael Gadd
Affiliation:
University of Dundee
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Summary

As mentioned repeatedly in this book, the goal of life is preservation of the species through reproduction, but this requires energy. Although there are a few exceptional copiotrophic environments such as foodstuffs and animal guts, most ecosystems where microorganisms are found are oligotrophic. Those organisms that can utilize nutrients efficiently have a better chance of survival in such ecosystems. Further, many microbes synthesize reserve materials, when available nutrients are in excess, and utilize these under starvation conditions, while various resting cells are produced under conditions where growth is difficult. In this chapter, the main bacterial survival mechanisms are discussed in terms of reserve materials and resting cell types.

Survival and energy

As discussed earlier, living microorganisms maintain a certain level of adenylate energy charge (EC) and proton motive force even under starvation conditions (Section 5.6.2). These forms of biological energy are needed for the basic metabolic processes necessary to survive such as transport and the turnover of macromolecules. Maintenance energy is the term used for this energy.

Under starvation conditions, cells utilize cellular components including reserve and non-essential materials for survival. This is referred to as endogenous metabolism. Almost all prokaryotes accumulate at least one type of reserve material under energy-rich conditions. During a period of starvation, the reserve material(s) are consumed through endogenous metabolism before the organism oxidizes other cellular constituents such as proteins and RNA that are not needed under the starvation conditions (Figure 13.1).

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Bacterial Physiology and Metabolism , pp. 482 - 495
Publisher: Cambridge University Press
Print publication year: 2008

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References

Aertsen, A. & Michiels, C. (2004). Stress and how bacteria cope with death and survival. Critical Reviews in Microbiology 30, 263–273.CrossRefGoogle Scholar
Aertsen, A. & Michiels, C. W. (2005). Diversify or die: generation of diversity in response to stress. Critical Reviews in Microbiology 31, 69–78.CrossRefGoogle ScholarPubMed
Engelberg-Kulka, H. & Glaser, G. (1999). Addiction modules and programmed cell death and antideath in bacterial cultures. Annual Review of Microbiology 53, 43–70.CrossRefGoogle ScholarPubMed
Errington, J., Daniel, R. A. & Scheffers, D. J. (2003). Cytokinesis in bacteria. Microbiology and Molecular Biology Reviews 67, 52–65.CrossRefGoogle ScholarPubMed
Ferenci, T. (2001). Hungry bacteria: definition and properties of a nutritional state. Environmental Microbiology 3, 605–611.CrossRefGoogle ScholarPubMed
Lazazzera, B. A. (2000). Quorum sensing and starvation: signals for entry into stationary phase. Current Opinion in Microbiology 3, 177–182.CrossRefGoogle ScholarPubMed
Lewis, K. (2000). Programmed death in bacteria. Microbiology and Molecular Biology Reviews 64, 503–514.CrossRefGoogle ScholarPubMed
Matic, I., Taddei, F. & Radman, M. (2004). Survival versus maintenance of genetic stability: a conflict of priorities during stress. Research in Microbiology 155, 337–341.CrossRefGoogle ScholarPubMed
Morita, R. Y. (1999). Is H2 the universal energy source for long-term survival?Microbial Ecology 38, 307–320.CrossRefGoogle Scholar
Mukamolova, G. V., Kaprelyants, A. S., Kell, D. B. & Young, M. (2003). Adoption of the transiently non-culturable state – a bacterial survival strategy?Advances in Microbial Physiology 47, 65–129.CrossRefGoogle Scholar
Nystroem, T. (1998). To be or not to be: the ultimate decision of the growth-arrested bacterial cell. FEMS Microbiology Reviews 21, 283–290.CrossRefGoogle Scholar
Nystrom, T. (2004). Growth versus maintenance: a trade-off dictated by RNA polymerase availability and sigma factor competition?Molecular Microbiology 54, 855–862.CrossRefGoogle ScholarPubMed
Peterson, C. N., Mandel, M. J. & Silhavy, T. J. (2005). Escherichia coli starvation diets: essential nutrients weigh in distinctly. Journal of Bacteriology 187, 7549–7553.CrossRefGoogle ScholarPubMed
Rice, K. C. & Bayles, K. W. (2003). Death's toolbox: examining the molecular components of bacterial programmed cell death. Molecular Microbiology 50, 729–738.CrossRefGoogle ScholarPubMed
Romling, U., Gomelsky, M. & Galperin, M. Y. (2005). C-di-GMP: the dawning of a novel bacterial signalling system. Molecular Microbiology 57, 629–639.CrossRefGoogle ScholarPubMed
Wai, S. N., Mizunoe, Y. & Yoshida, S. (1999). How Vibrio cholerae survive during starvation. FEMS Microbiology Letters 180, 123–131.CrossRefGoogle ScholarPubMed
Aldor, I. S. & Keasling, J. D. (2003). Process design for microbial plastic factories: metabolic engineering of polyhydroxyalkanoates. Current Opinion in Biotechnology 14, 475–483.CrossRefGoogle ScholarPubMed
Alvarez, H. M. & Steinbuchel, A. (2002). Triacylglycerols in prokaryotic microorganisms. Applied Microbiology and Biotechnology 60, 367–376.Google ScholarPubMed
Arguelles, J. C. (2000). Physiological roles of trehalose in bacteria and yeasts: a comparative analysis. Archives of Microbiology 174, 217–224.Google ScholarPubMed
Brown, M. R. & Kornberg, A. (2004). Inorganic polyphosphate in the origin and survival of species. Proceedings of the National Academy of Sciences, USA 101, 16085–16087.CrossRefGoogle ScholarPubMed
Garcia-Contreras, R., Celis, H. & Romero, I. (2004). Importance of Rhodospirillum rubrum H+-pyrophosphatase under low-energy conditions. Journal of Bacteriology 186, 6651–6655.CrossRefGoogle ScholarPubMed
Kornberg, A. (1995). Inorganic polyphosphate: towards making a forgotten polymer unforgettable. Journal of Bacteriology 177, 491–496.CrossRefGoogle Scholar
Kulaev, I. & Kulakovskaya, T. (2000). Polyphosphate and phosphate pump. Annual Review of Microbiology 54, 709–734.CrossRefGoogle ScholarPubMed
Kulaev, I., Vagabov, V. & Kulakovskaya, T. (1999). New aspects of inorganic polyphosphate metabolism and function. Journal of Bioscience and Bioengineering 88, 111–129.CrossRefGoogle ScholarPubMed
Ladygina, N., Dedyukhina, E. G. & Vainshtein, M. B. (2006). A review on microbial synthesis of hydrocarbons. Process Biochemistry 41, 1001–1014.CrossRefGoogle Scholar
Luengo, J. M., Garcia, B., Sandoval, A., Naharro, G. & Olivera, E. R. (2003). Bioplastics from microorganisms. Current Opinion in Microbiology 6, 251–260.CrossRefGoogle ScholarPubMed
Stubbe, J., Tian, J., He, A., Sinskey, A. J., Lawrence, A. G. & Liu, P. (2005). Nontemplate-dependent polymerization processes: polyhydroxyalkanoate synthases as a paradigm. Annual Review of Biochemistry 74, 433–480.CrossRefGoogle Scholar
Waltermann, M. & Steinbuchel, A. (2005). Neutral lipid bodies in prokaryotes: recent insights into structure, formation, and relationship to eukaryotic lipid depots. Journal of Bacteriology 187, 3607–3619.CrossRefGoogle ScholarPubMed
Barer, M. R. & Harwood, C. R. (1999). Bacterial viability and culturability. Advances in Microbial Physiology 41, 93–137.CrossRefGoogle ScholarPubMed
Cohen-Gonsaud, M., Keep, N. H., Davies, A. P., Ward, J., Henderson, B. & Labesse, G. (2004). Resuscitation-promoting factors possess a lysozyme-like domain. Trends in Biochemical Sciences 29, 7–10.CrossRefGoogle ScholarPubMed
Errington, J. (2001). Septation and chromosome segregation during sporulation in Bacillus subtilis. Current Opinion in Microbiology 4, 660–666.CrossRefGoogle ScholarPubMed
Hilbert, D. W. & Piggot, P. J. (2004). Compartmentalization of gene expression during Bacillus subtilis spore formation. Microbiology and Molecular Biology Reviews 68, 234–262.CrossRefGoogle ScholarPubMed
Hoch, J. A. (1998). Initiation of bacterial development. Current Opinion in Microbiology 1, 170–174.CrossRefGoogle ScholarPubMed
Kaprelyants, A. S., Gottschal, J. C. & Kell, D. B. (1993). Dormancy in non-sporulating bacteria. FEMS Microbiology Reviews 104, 271–286.CrossRefGoogle Scholar
Keep, N. H., Ward, J. M., Cohen-Gonsaud, M. & Henderson, B. (2006). Wake up! Peptidoglycan lysis and bacterial non-growth states. Trends in Microbiology 14, 271–276.CrossRefGoogle ScholarPubMed
Kell, D. B. & Young, M. (2000). Bacterial dormancy and culturability: the role of autocrine growth factors. Current Opinion in Microbiology 3, 238–243.CrossRefGoogle ScholarPubMed
Leadbetter, J. R. (2003). Cultivation of recalcitrant microbes: cells are alive, well and revealing their secrets in the 21st century laboratory. Current Opinion in Microbiology 6, 274–281.CrossRefGoogle ScholarPubMed
Moir, A. (2003). Bacterial spore germination and protein mobility. Trends in Microbiology 11, 452–454.CrossRefGoogle ScholarPubMed
Nystrom, T. (2004). Stationary-phase physiology. Annual Review of Microbiology 58, 161–181.CrossRefGoogle ScholarPubMed
Oliver, J. D. (2005). The viable but nonculturable state in bacteria. Journal of Microbiology-Seoul 43, 93–100.Google Scholar
Paredes, C. J., Alsaker, K. V. & Papoutsakis, E. T. (2005). A comparative genomic view of clostridial sporulation and physiology. Nature Reviews Microbiology 3, 969–978.CrossRefGoogle ScholarPubMed
Setlow, P. (2003). Spore germination. Current Opinion in Microbiology 6, 550–556.CrossRefGoogle ScholarPubMed
Stephenson, K. & Hoch, J. A. (2002). Evolution of signalling in the sporulation phosphorelay. Molecular Microbiology 46, 297–304.CrossRefGoogle ScholarPubMed
Tyson, G. W. & Banfield, J. F. (2005). Cultivating the uncultivated: a community genomics perspective. Trends in Microbiology 13, 411–415.CrossRefGoogle ScholarPubMed
Vainshtein, M. B. & Kudryashova, E. B. (2000). Nanobacteria. Microbiology-Moscow 69, 129–138.CrossRefGoogle Scholar
Zhang, C. C., Laurent, S., Sakr, , Peng, S. & Bedu, S. (2006). Heterocyst differentiation and pattern formation in cyanobacteria: a chorus of signals. Molecular Microbiology 59, 367–375.CrossRefGoogle ScholarPubMed
Aertsen, A. & Michiels, C. (2004). Stress and how bacteria cope with death and survival. Critical Reviews in Microbiology 30, 263–273.CrossRefGoogle Scholar
Aertsen, A. & Michiels, C. W. (2005). Diversify or die: generation of diversity in response to stress. Critical Reviews in Microbiology 31, 69–78.CrossRefGoogle ScholarPubMed
Engelberg-Kulka, H. & Glaser, G. (1999). Addiction modules and programmed cell death and antideath in bacterial cultures. Annual Review of Microbiology 53, 43–70.CrossRefGoogle ScholarPubMed
Errington, J., Daniel, R. A. & Scheffers, D. J. (2003). Cytokinesis in bacteria. Microbiology and Molecular Biology Reviews 67, 52–65.CrossRefGoogle ScholarPubMed
Ferenci, T. (2001). Hungry bacteria: definition and properties of a nutritional state. Environmental Microbiology 3, 605–611.CrossRefGoogle ScholarPubMed
Lazazzera, B. A. (2000). Quorum sensing and starvation: signals for entry into stationary phase. Current Opinion in Microbiology 3, 177–182.CrossRefGoogle ScholarPubMed
Lewis, K. (2000). Programmed death in bacteria. Microbiology and Molecular Biology Reviews 64, 503–514.CrossRefGoogle ScholarPubMed
Matic, I., Taddei, F. & Radman, M. (2004). Survival versus maintenance of genetic stability: a conflict of priorities during stress. Research in Microbiology 155, 337–341.CrossRefGoogle ScholarPubMed
Morita, R. Y. (1999). Is H2 the universal energy source for long-term survival?Microbial Ecology 38, 307–320.CrossRefGoogle Scholar
Mukamolova, G. V., Kaprelyants, A. S., Kell, D. B. & Young, M. (2003). Adoption of the transiently non-culturable state – a bacterial survival strategy?Advances in Microbial Physiology 47, 65–129.CrossRefGoogle Scholar
Nystroem, T. (1998). To be or not to be: the ultimate decision of the growth-arrested bacterial cell. FEMS Microbiology Reviews 21, 283–290.CrossRefGoogle Scholar
Nystrom, T. (2004). Growth versus maintenance: a trade-off dictated by RNA polymerase availability and sigma factor competition?Molecular Microbiology 54, 855–862.CrossRefGoogle ScholarPubMed
Peterson, C. N., Mandel, M. J. & Silhavy, T. J. (2005). Escherichia coli starvation diets: essential nutrients weigh in distinctly. Journal of Bacteriology 187, 7549–7553.CrossRefGoogle ScholarPubMed
Rice, K. C. & Bayles, K. W. (2003). Death's toolbox: examining the molecular components of bacterial programmed cell death. Molecular Microbiology 50, 729–738.CrossRefGoogle ScholarPubMed
Romling, U., Gomelsky, M. & Galperin, M. Y. (2005). C-di-GMP: the dawning of a novel bacterial signalling system. Molecular Microbiology 57, 629–639.CrossRefGoogle ScholarPubMed
Wai, S. N., Mizunoe, Y. & Yoshida, S. (1999). How Vibrio cholerae survive during starvation. FEMS Microbiology Letters 180, 123–131.CrossRefGoogle ScholarPubMed
Aldor, I. S. & Keasling, J. D. (2003). Process design for microbial plastic factories: metabolic engineering of polyhydroxyalkanoates. Current Opinion in Biotechnology 14, 475–483.CrossRefGoogle ScholarPubMed
Alvarez, H. M. & Steinbuchel, A. (2002). Triacylglycerols in prokaryotic microorganisms. Applied Microbiology and Biotechnology 60, 367–376.Google ScholarPubMed
Arguelles, J. C. (2000). Physiological roles of trehalose in bacteria and yeasts: a comparative analysis. Archives of Microbiology 174, 217–224.Google ScholarPubMed
Brown, M. R. & Kornberg, A. (2004). Inorganic polyphosphate in the origin and survival of species. Proceedings of the National Academy of Sciences, USA 101, 16085–16087.CrossRefGoogle ScholarPubMed
Garcia-Contreras, R., Celis, H. & Romero, I. (2004). Importance of Rhodospirillum rubrum H+-pyrophosphatase under low-energy conditions. Journal of Bacteriology 186, 6651–6655.CrossRefGoogle ScholarPubMed
Kornberg, A. (1995). Inorganic polyphosphate: towards making a forgotten polymer unforgettable. Journal of Bacteriology 177, 491–496.CrossRefGoogle Scholar
Kulaev, I. & Kulakovskaya, T. (2000). Polyphosphate and phosphate pump. Annual Review of Microbiology 54, 709–734.CrossRefGoogle ScholarPubMed
Kulaev, I., Vagabov, V. & Kulakovskaya, T. (1999). New aspects of inorganic polyphosphate metabolism and function. Journal of Bioscience and Bioengineering 88, 111–129.CrossRefGoogle ScholarPubMed
Ladygina, N., Dedyukhina, E. G. & Vainshtein, M. B. (2006). A review on microbial synthesis of hydrocarbons. Process Biochemistry 41, 1001–1014.CrossRefGoogle Scholar
Luengo, J. M., Garcia, B., Sandoval, A., Naharro, G. & Olivera, E. R. (2003). Bioplastics from microorganisms. Current Opinion in Microbiology 6, 251–260.CrossRefGoogle ScholarPubMed
Stubbe, J., Tian, J., He, A., Sinskey, A. J., Lawrence, A. G. & Liu, P. (2005). Nontemplate-dependent polymerization processes: polyhydroxyalkanoate synthases as a paradigm. Annual Review of Biochemistry 74, 433–480.CrossRefGoogle Scholar
Waltermann, M. & Steinbuchel, A. (2005). Neutral lipid bodies in prokaryotes: recent insights into structure, formation, and relationship to eukaryotic lipid depots. Journal of Bacteriology 187, 3607–3619.CrossRefGoogle ScholarPubMed
Barer, M. R. & Harwood, C. R. (1999). Bacterial viability and culturability. Advances in Microbial Physiology 41, 93–137.CrossRefGoogle ScholarPubMed
Cohen-Gonsaud, M., Keep, N. H., Davies, A. P., Ward, J., Henderson, B. & Labesse, G. (2004). Resuscitation-promoting factors possess a lysozyme-like domain. Trends in Biochemical Sciences 29, 7–10.CrossRefGoogle ScholarPubMed
Errington, J. (2001). Septation and chromosome segregation during sporulation in Bacillus subtilis. Current Opinion in Microbiology 4, 660–666.CrossRefGoogle ScholarPubMed
Hilbert, D. W. & Piggot, P. J. (2004). Compartmentalization of gene expression during Bacillus subtilis spore formation. Microbiology and Molecular Biology Reviews 68, 234–262.CrossRefGoogle ScholarPubMed
Hoch, J. A. (1998). Initiation of bacterial development. Current Opinion in Microbiology 1, 170–174.CrossRefGoogle ScholarPubMed
Kaprelyants, A. S., Gottschal, J. C. & Kell, D. B. (1993). Dormancy in non-sporulating bacteria. FEMS Microbiology Reviews 104, 271–286.CrossRefGoogle Scholar
Keep, N. H., Ward, J. M., Cohen-Gonsaud, M. & Henderson, B. (2006). Wake up! Peptidoglycan lysis and bacterial non-growth states. Trends in Microbiology 14, 271–276.CrossRefGoogle ScholarPubMed
Kell, D. B. & Young, M. (2000). Bacterial dormancy and culturability: the role of autocrine growth factors. Current Opinion in Microbiology 3, 238–243.CrossRefGoogle ScholarPubMed
Leadbetter, J. R. (2003). Cultivation of recalcitrant microbes: cells are alive, well and revealing their secrets in the 21st century laboratory. Current Opinion in Microbiology 6, 274–281.CrossRefGoogle ScholarPubMed
Moir, A. (2003). Bacterial spore germination and protein mobility. Trends in Microbiology 11, 452–454.CrossRefGoogle ScholarPubMed
Nystrom, T. (2004). Stationary-phase physiology. Annual Review of Microbiology 58, 161–181.CrossRefGoogle ScholarPubMed
Oliver, J. D. (2005). The viable but nonculturable state in bacteria. Journal of Microbiology-Seoul 43, 93–100.Google Scholar
Paredes, C. J., Alsaker, K. V. & Papoutsakis, E. T. (2005). A comparative genomic view of clostridial sporulation and physiology. Nature Reviews Microbiology 3, 969–978.CrossRefGoogle ScholarPubMed
Setlow, P. (2003). Spore germination. Current Opinion in Microbiology 6, 550–556.CrossRefGoogle ScholarPubMed
Stephenson, K. & Hoch, J. A. (2002). Evolution of signalling in the sporulation phosphorelay. Molecular Microbiology 46, 297–304.CrossRefGoogle ScholarPubMed
Tyson, G. W. & Banfield, J. F. (2005). Cultivating the uncultivated: a community genomics perspective. Trends in Microbiology 13, 411–415.CrossRefGoogle ScholarPubMed
Vainshtein, M. B. & Kudryashova, E. B. (2000). Nanobacteria. Microbiology-Moscow 69, 129–138.CrossRefGoogle Scholar
Zhang, C. C., Laurent, S., Sakr, , Peng, S. & Bedu, S. (2006). Heterocyst differentiation and pattern formation in cyanobacteria: a chorus of signals. Molecular Microbiology 59, 367–375.CrossRefGoogle ScholarPubMed

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