Skip to main content
Log in

Starvation and penetration of bacteria in soils and rocks

  • Reviews
  • Published:
Experientia Aims and scope Submit manuscript

Summary

The soil and subsurface strata are low nutrient environments and their bacterial inhabitants must adopt starvation responses to survive. These responses include the formation of dormant, viable cells which, although reduced in cell size and volume, are able to respond to any improvement in nutrient availability. Starved bacteria are able to survive for extended periods without nutrients and their reduced size allows them to disperse deeply within rocks and soils greatly improving their penetration. These combined factors may increase opportunities for bacteria to reach a deep waste disposal site.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  1. Albertson, N. A., Jones, G. W., and Kjelleberg, S., The detection of starvation-specific antigens in two marine bacteria. J. gen. Microbiol.133 (1987) 2225–2231.

    CAS  Google Scholar 

  2. Amy, P. S., and Morita, R. Y., Starvation-survival patterns of sixteen freshly isolated open-ocean bacteria. Appl. envir. Microbiol.45 (1983) 1109–1115.

    CAS  Google Scholar 

  3. Anderson, J. I. W., and Heffernan, W. P., Isolation and characterization of filterable marine bacteria. J. Bact.90 (1965) 1713–1718.

    CAS  PubMed  PubMed Central  Google Scholar 

  4. Bae, H. C., Cota-Robles, E. H., and Casida, L. E. Jr, Microflora of soil as viewed by transmission electron microscopy. Appl. Microbiol.23 (1972) 637–648.

    CAS  PubMed  PubMed Central  Google Scholar 

  5. Baker, R. M., Singleton, F. L., and Hood, M. A., Effect of nutrient deprivation onVibrio cholerae. Appl. envir. Microbiol.46 (1983) 930–940.

    CAS  Google Scholar 

  6. Balkwill, D. L., Rucinsky, T. E., and Casida, L. E. Jr, Release of microorganisms from soil with respect to transmission electron microscopy viewing and plate counts. Antonie van Leeuwenhoek43 (1977) 73–87.

    CAS  PubMed  Google Scholar 

  7. Beloin, R. M., Sinclair, J. L., and Ghiorse, W. C., Distribution and activity of microorganisms in subsurface sediments of a pristine study site in Oklahoma. Microb. Ecol.16 (1988) 85–97.

    CAS  PubMed  Google Scholar 

  8. Bone, T. L., and Balkwill, D. L., Morphological and cultural comparison of microorganisms in surface soil and subsurface sediments at a pristine study site in Oklahoma. Microb. Ecol.16 (1988) 49–64.

    CAS  PubMed  Google Scholar 

  9. Boyaval, P., Boyaval, E., and Desmazeaud, M. J., Survival ofBrevibacterium lines during nutrient starvation and intracellular changes. Archs Microbiol.141 (1985) 128–132.

    CAS  Google Scholar 

  10. Boylen, C. W., and Mulks, M. H., The survival of Coryneform bacteria during periods of prolonged nutrient starvation. J. gen. Microbiol.105 (1978) 323–334.

    CAS  Google Scholar 

  11. Boylen, C. W., and Pate, J. L., Fine structure ofArthrobacter crystallopeites during long-term starvation of rod and spherical stage cells. Can. J. Microbiol.19 (1973) 1–5.

    CAS  PubMed  Google Scholar 

  12. Casida, L. E. Jr, Microorganisms in unamended soil as observed by various forms of microscopy and staining. Appl. Microbiol.21 (1971) 1040–1045.

    PubMed  PubMed Central  Google Scholar 

  13. Clark, F. E., Bacteria in soil, in: Soil Biology, pp. 15–19. Eds A. Burges and F. Raw, Academic Press, London/New York 1967.

    Google Scholar 

  14. Crawford, P. B., Possible bacterial correction of stratification problems. Producers Monthly25 (1961) 10–11.

    Google Scholar 

  15. Dawes, E. A., Endogenous metabolism and the survival of starved prokaryotes, in: The Survival of Vegetative Microbes, 26th Symposium for the Society of General Microbiology, pp. 19–53. Eds T. R. G. Gray and J. R. Postgate. Cambridge University Press, Cambridge 1976.

    Google Scholar 

  16. Dawes, E. A., and Large, P. J., Effect of starvation on the viability and cellular constituents ofZymomonas anaerobia andZymomonas mobilis. J. gen. Microbiol.60 (1970) 31–42.

    CAS  PubMed  Google Scholar 

  17. Dawes, E. A., and Ribbons, D. W., The endogeous metabolism of microorganisms. A. Rev. Microbiol.16 (1962) 241–264.

    CAS  Google Scholar 

  18. Dawson, M. P., Humphrey, B. A., and Marshall, K. C., Adhesion: a tactic in the survival strategy of a marineVibrio during starvation. Curr. Microbiol.6 (1981) 195–199.

    Google Scholar 

  19. Ensign, J. C. Long-term starvation of rod and spherical cells ofArthrobacter crystallopoites. J. Bact.103 (1970) 569–577.

    CAS  PubMed  PubMed Central  Google Scholar 

  20. Guckert, J. B., Hood, M. A., and White, D. C., Phospholipid esterlinked fatty acid profile changes during nutrient deprivation ofVibrio cholerae: increases in the trans/cis ratio and proportions of cyclopropyl fatty acids. Appl. envir. Microbiol.52 (1986) 794–801.

    CAS  Google Scholar 

  21. Harder, W., and Dijkhuizen, L., Physiological responses to nutrient limitation. A. Rev. Microbiol.37 (1983) 1–23.

    CAS  Google Scholar 

  22. Harrison, A. P. Jr, and Lawrence, F. R., Phenotypic, genotypic and chemical changes in starving populations ofAerobacter aerogenes. J. Bact.85 (1963) 742–750.

    CAS  PubMed  PubMed Central  Google Scholar 

  23. Hart, R. T., Fekete, T., and Flock, D. L., The plugging effect of bacteria in sandstone systems. Can. Min. Metall. Bull.53 (1960) 495–501.

    Google Scholar 

  24. Hofle, M. G., Transient responses of glucose-limited cultures ofCytophaga johnsonae to nutrient excess and starvation. Appl. envir. Microbiol.47 (1984) 356–362.

    CAS  Google Scholar 

  25. Hood, M. A., Guckert, J. B., White, D. C., and Deck, F., Effect of nutrient deprivation on lipid, carbohydrate, DNA, RNA and protein levels inVibrio cholerae. Appl. envir. Microbiol.52 (1986) 788–793.

    CAS  Google Scholar 

  26. Hood, M. A., and MacDonell, M. T., Distribution of ultramicrobacteria in a Gulf coast estuary and induction of ultramicrobacteria. Microb. Ecol.14 (1987) 113–127.

    CAS  PubMed  Google Scholar 

  27. Humphrey, B., Kjelleberg, S., and Marshall, K. C., Responses of marine bacteria under starvation conditions at a solid-water interface. Appl. envir. Microbiol.45 (1983) 43–47.

    CAS  Google Scholar 

  28. Jack, T. R., Shaw, J. C., Wardlaw, N. C., and Costerton, J. W., Microbial plugging in enhanced oil recovery, in: Microbial Enhancement of Oil Recovery. Eds E. C. Donaldson, G. V. Chilingarian and T. F. Yen. Elsevier, Amsterdam 1985.

    Google Scholar 

  29. Jang, L. K., Chang, P. W., Findley, J. E., and Yen, T. F., Selection of bacteria with favorable transport properties through porous rock for the application of microbial enhanced oil recovery. Appl. envir. Microbiol.46 (1983) 1066–1072.

    CAS  Google Scholar 

  30. Jenneman, G. E., Knapp, R. M., McInerney, M. J., Menzie, D. E., and Revus, D. E., Experimental studies of in-situ microbial enhanced oil recovery. Soc. Petrol Engng J.24 (1984) 33–37.

    CAS  Google Scholar 

  31. Jenneman, G. E., McInerney, M. J., and Knapp, R. M., Microbial penetration through nutrient-saturated Berea sandstone. Appl. envir. Microbiol.50 (1985) 383–391.

    CAS  Google Scholar 

  32. Jensen, H. L., Survival ofRhizobium meliloti in soil culture. Nature192 (1961) 682–683.

    Google Scholar 

  33. Jones, K. L., and Rhodes-Roberts, M. E., The survival of marine bacteria under starvation conditions. J. appl. Bact.50 (1981) 247–258.

    CAS  Google Scholar 

  34. Kefford, B., Humphrey, B. A., and Marshall, K. C., Adhesion: a possible survival strategy for leptospires under starvation conditions. Curr. Microbiol.13 (1986) 247–250.

    CAS  Google Scholar 

  35. Kjelleberg, S., Humphrey, B. A., and Marshall, K. C., Effect of interfaces on small, starved marine bacteria. Appl. envir. Microbiol.43 (1982) 1166–1172.

    CAS  Google Scholar 

  36. Kjelleberg, S., Humphrey, B. A., and Marshall, K. C., Initial phases of starvation and activity of bacteria at surfaces. Appl. envir. Microbiol.46 (1983) 978–984.

    CAS  Google Scholar 

  37. Kjelleberg, S., Hermansson, M., and Marden, P., The transient phase between growth and nongrowth of heterotrophic bacteria, with emphasis on the marine environment. A. Rev. Microbiol.41 (1987) 25–49.

    CAS  Google Scholar 

  38. Lappin-Scott, H. M., Cusack, F., MacLeod, A., and Costerton, J. W., Starvation and nutrient resuscitation ofKlebsiella pneumoniae isolated from oilwell waters. J. appl. Bact.64 (1988a) 541–549.

    CAS  Google Scholar 

  39. Lappin-Scott, H. M., Cusack, F., and Costerton, J. W., Nutrient resuscitation and growth of starved cells in sandstone cores: a novel approach to enhanced oil recovery. Appl. envir. Microbiol.54 (1988) 1373–1382.

    CAS  Google Scholar 

  40. Lipman, C. B., The discovery of living micro-organisms in ancient rocks. Science68 (1928) 272–273.

    CAS  PubMed  Google Scholar 

  41. Lipman, C. B., Living micro-organisms in ancient rocks. J. Bact.22 (1931) 183–198.

    CAS  PubMed  PubMed Central  Google Scholar 

  42. Lipman, C. B., Further evidence of the amazing longevity of bacteria in coal. Science79 (1934) 230–231.

    CAS  PubMed  Google Scholar 

  43. MacDonell, M. T., and Hood, M. A., Isolation and characterization of ultramicrobacteria from a Gulf coast estuary. Appl. envir. Microbiol.43 (1982) 566–571.

    CAS  Google Scholar 

  44. MacLeod, F. A., Lappin-Scott, H. M., and Costerton, J. W., Plugging of a model rock system by using starved bacteria. Appl. envir. Microbiol.54 (1988) 1365–1372.

    CAS  Google Scholar 

  45. Marden, P., Tunlid, A., Malmcrona-Friberg, K., Odham, G., and Kjelleberg, S., Physiological and morphological changes during short term starvation of marine bacterial isolates. Arch. Microbiol.142 (1985) 326–332.

    Google Scholar 

  46. Marshall, K. C., Adhesion and growth of bacteria at surfaces in oligotrophic habitats. Can. J. Microbiol.34 (1988) 503–506.

    Google Scholar 

  47. Massa, E. M., Lopez Vinals, A., and Farias, R. N., Influence of unsaturated fatty acid membrane component on sensitivity of anEscherichia coli fatty acid auxotroph to conditions of nutrient deprivation. Appl. envir. Microbiol.54 (1988) 2107–2111.

    CAS  Google Scholar 

  48. Montague, M. D., and Dawes, E. A., The survival ofPeptococcus prevotii in relation to the adenylate energy charge. J. gen. Microbiol.80 (1974) 291–299.

    CAS  PubMed  Google Scholar 

  49. Morita, R. Y., Starvation and miniaturisation of heterotrophs, with special emphasis on maintenance of the starved viable state, in: Bacteria in Their Natural Environments, pp. 111–130. Eds M. Fletcher and G. D. Floodgate. Academic Press, London 1985.

    Google Scholar 

  50. Morita, R. Y., Bioavailability of energy and its relationship to growth and starvation survival in nature. Can. J. Microbiol.34 (1988) 436–441.

    CAS  Google Scholar 

  51. Myers, G. E., and McCready, R. G. L., Bacteria can penetrate rock. Can. J. Microbiol.12 (1966) 477–484.

    Google Scholar 

  52. Myers, G. E., and Slabyj, B. M., The microbiological quality of injection water used in Alberta oil-fields. Producers MonthlyMay (1962) 12–14.

    Google Scholar 

  53. Nissen, H., Long term starvation of a marine bacterium,Alteromonas denitrificans, isolated from a Norwegian fjord. FEMS Microbiol. Ecol.45 (1987) 173–183.

    CAS  Google Scholar 

  54. Novitsky, J. A., and Morita, R. Y., Morphological characterization of small cells resulting from nutrient starvation of a psychrophilic marineVibrio. Appl. envir. Microbiol.32 (1976) 617–622.

    CAS  Google Scholar 

  55. Novitsky, J. A., and Morita, R. Y., Survival of a psychrophilic marineVibrio under long-term nutrient starvation. Appl. envir. Microbiol.33 (1977) 635–641.

    CAS  Google Scholar 

  56. Novitsky, J. A., and Morita, R. Y., Possible strategy for the survival of marine bacteria under starvation conditions. Mar. Biol.48 (1978) 289–295.

    Google Scholar 

  57. Oppenheimer, C. H., The membrane filter in marine microbiology. J. Bact.64 (1952) 783–786.

    CAS  PubMed  PubMed Central  Google Scholar 

  58. Postgate, J. R., and Hunter, J. R., The survival of starved bacteria. J. gen. Microbiol.29 (1962) 233–263.

    CAS  PubMed  Google Scholar 

  59. Raleigh, J. T., and Flock, D. L., A study of formation plugging with bacteria. J. Petrol Technol.February (1965) 201–206.

    Google Scholar 

  60. Reece, P., Toth, D., and Dawes, E. A., Fermentation of purines and their effect on the adenylate energy charge and viability of starvedPeptococcus prevotii. J. gen. Microbiol.97 (1976) 63–71.

    CAS  PubMed  Google Scholar 

  61. Reeve, C. A., Bockman, A. T., and Matin, A., Role of protein degradation in the survival of carbon-starvedEscherichia coli andSalmonella typhimurium. J. Bact.157 (1984) 758–763.

    CAS  PubMed  PubMed Central  Google Scholar 

  62. Ryan, F. J., Spontaneous mutation in non-dividing bacteria. Genetics40 (1955) 726.

    CAS  PubMed  PubMed Central  Google Scholar 

  63. Rybkin, A. I., and Ravin, V. K., Depression of synthetic activity as the possible cause of death ofEscherichia coli during amino acid starvation. Microbiology56 (1987) 170–174.

    Google Scholar 

  64. Scherer, C. G., and Boylen, C. W., Macromolecular synthesis and degradation inArthrobacter during periods of nutrient deprivation. J. Bact.132 (1977) 584–589.

    CAS  PubMed  PubMed Central  Google Scholar 

  65. Schimz, K.-L., and Overhoff, B., Investigations of the influence of carbon starvation on the carbohydrate storage compounds (trehalose, glycogen), viability, adenylate pool, and adenylate energy charge inCellulomonas sp. (DMS20108). FEMS Microbiol. Letts40 (1987) 333–337.

    CAS  Google Scholar 

  66. Shaw, J. C., Bramhill, B., Wardlaw, N. C., and Costerton, J. W., Bacterial fouling in a model core system. Appl. envir. Microbiol.49 (1985) 693–701.

    CAS  Google Scholar 

  67. Tabor, P. S., Ohwada, K., and Colwell, R. R., Filterable marine bacteria found in the deep sea: distribution, taxonomy, and response to starvation. Microb. Ecol.7 (1981) 67–83.

    CAS  PubMed  Google Scholar 

  68. Thomas, T. D., and Batt, R. D., Survival ofStreptococcus lactis in starvation conditions. J. gen. Microbiol.50 (1968) 367–382.

    CAS  PubMed  Google Scholar 

  69. Tkachenko, A. G., and Chudinov, A. A., Energy aspects of the growth ofEscherichia coli synchronized by starvation. Microbiology56 (1987) 47–52.

    Google Scholar 

  70. Torrella, F., and Morita, R. Y., Microcultural study of bacterial size changes and microcology and ultramicrocolony formation by heterotrophic bacteria in seawater. Appl. envir. Microbiol.41 (1981) 518–527.

    CAS  Google Scholar 

  71. Updegraff, D. M., Plugging and penetration of reservoir rock by microorganisms, in: International Conference on the Microbial Enhancement of Oil Recovery Proceedings, pp. 80–85. Eds E. C. Donaldson and J. B. Clark. U.S. Department of Energy, Bartlesville, Oklahoma 1982.

    Google Scholar 

  72. Updegraff, D. M., and Wren, G. B., The release of oil from petroleum-bearing material by sulfate-reducing bacteria. Appl. Microbiol.2 (1954) 309–322.

    CAS  PubMed  PubMed Central  Google Scholar 

  73. Winslow, C.-E. A., and Falk, I. S., Studies on salt action VIII. The influence of calcium and sodium salts at various hydrogen ion concentrations upon the viability ofBacterium coli. J. Bact.8 (1923) 215.

    CAS  PubMed  PubMed Central  Google Scholar 

  74. Zechman, J. M., and Casida, L. E. Jr, Death ofPseudomonas aeruginosa in soil. Can. J. Microbiol.28 (1982) 788–794.

    CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Lappin-Scott, H.M., Costerton, J.W. Starvation and penetration of bacteria in soils and rocks. Experientia 46, 807–812 (1990). https://doi.org/10.1007/BF01935529

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF01935529

Key words

Navigation