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.
Similar content being viewed by others
References
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.
Amy, P. S., and Morita, R. Y., Starvation-survival patterns of sixteen freshly isolated open-ocean bacteria. Appl. envir. Microbiol.45 (1983) 1109–1115.
Anderson, J. I. W., and Heffernan, W. P., Isolation and characterization of filterable marine bacteria. J. Bact.90 (1965) 1713–1718.
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.
Baker, R. M., Singleton, F. L., and Hood, M. A., Effect of nutrient deprivation onVibrio cholerae. Appl. envir. Microbiol.46 (1983) 930–940.
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.
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.
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.
Boyaval, P., Boyaval, E., and Desmazeaud, M. J., Survival ofBrevibacterium lines during nutrient starvation and intracellular changes. Archs Microbiol.141 (1985) 128–132.
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.
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.
Casida, L. E. Jr, Microorganisms in unamended soil as observed by various forms of microscopy and staining. Appl. Microbiol.21 (1971) 1040–1045.
Clark, F. E., Bacteria in soil, in: Soil Biology, pp. 15–19. Eds A. Burges and F. Raw, Academic Press, London/New York 1967.
Crawford, P. B., Possible bacterial correction of stratification problems. Producers Monthly25 (1961) 10–11.
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.
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.
Dawes, E. A., and Ribbons, D. W., The endogeous metabolism of microorganisms. A. Rev. Microbiol.16 (1962) 241–264.
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.
Ensign, J. C. Long-term starvation of rod and spherical cells ofArthrobacter crystallopoites. J. Bact.103 (1970) 569–577.
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.
Harder, W., and Dijkhuizen, L., Physiological responses to nutrient limitation. A. Rev. Microbiol.37 (1983) 1–23.
Harrison, A. P. Jr, and Lawrence, F. R., Phenotypic, genotypic and chemical changes in starving populations ofAerobacter aerogenes. J. Bact.85 (1963) 742–750.
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.
Hofle, M. G., Transient responses of glucose-limited cultures ofCytophaga johnsonae to nutrient excess and starvation. Appl. envir. Microbiol.47 (1984) 356–362.
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.
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.
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.
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.
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.
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.
Jenneman, G. E., McInerney, M. J., and Knapp, R. M., Microbial penetration through nutrient-saturated Berea sandstone. Appl. envir. Microbiol.50 (1985) 383–391.
Jensen, H. L., Survival ofRhizobium meliloti in soil culture. Nature192 (1961) 682–683.
Jones, K. L., and Rhodes-Roberts, M. E., The survival of marine bacteria under starvation conditions. J. appl. Bact.50 (1981) 247–258.
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.
Kjelleberg, S., Humphrey, B. A., and Marshall, K. C., Effect of interfaces on small, starved marine bacteria. Appl. envir. Microbiol.43 (1982) 1166–1172.
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.
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.
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.
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.
Lipman, C. B., The discovery of living micro-organisms in ancient rocks. Science68 (1928) 272–273.
Lipman, C. B., Living micro-organisms in ancient rocks. J. Bact.22 (1931) 183–198.
Lipman, C. B., Further evidence of the amazing longevity of bacteria in coal. Science79 (1934) 230–231.
MacDonell, M. T., and Hood, M. A., Isolation and characterization of ultramicrobacteria from a Gulf coast estuary. Appl. envir. Microbiol.43 (1982) 566–571.
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.
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.
Marshall, K. C., Adhesion and growth of bacteria at surfaces in oligotrophic habitats. Can. J. Microbiol.34 (1988) 503–506.
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.
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.
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.
Morita, R. Y., Bioavailability of energy and its relationship to growth and starvation survival in nature. Can. J. Microbiol.34 (1988) 436–441.
Myers, G. E., and McCready, R. G. L., Bacteria can penetrate rock. Can. J. Microbiol.12 (1966) 477–484.
Myers, G. E., and Slabyj, B. M., The microbiological quality of injection water used in Alberta oil-fields. Producers MonthlyMay (1962) 12–14.
Nissen, H., Long term starvation of a marine bacterium,Alteromonas denitrificans, isolated from a Norwegian fjord. FEMS Microbiol. Ecol.45 (1987) 173–183.
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.
Novitsky, J. A., and Morita, R. Y., Survival of a psychrophilic marineVibrio under long-term nutrient starvation. Appl. envir. Microbiol.33 (1977) 635–641.
Novitsky, J. A., and Morita, R. Y., Possible strategy for the survival of marine bacteria under starvation conditions. Mar. Biol.48 (1978) 289–295.
Oppenheimer, C. H., The membrane filter in marine microbiology. J. Bact.64 (1952) 783–786.
Postgate, J. R., and Hunter, J. R., The survival of starved bacteria. J. gen. Microbiol.29 (1962) 233–263.
Raleigh, J. T., and Flock, D. L., A study of formation plugging with bacteria. J. Petrol Technol.February (1965) 201–206.
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.
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.
Ryan, F. J., Spontaneous mutation in non-dividing bacteria. Genetics40 (1955) 726.
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.
Scherer, C. G., and Boylen, C. W., Macromolecular synthesis and degradation inArthrobacter during periods of nutrient deprivation. J. Bact.132 (1977) 584–589.
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.
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.
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.
Thomas, T. D., and Batt, R. D., Survival ofStreptococcus lactis in starvation conditions. J. gen. Microbiol.50 (1968) 367–382.
Tkachenko, A. G., and Chudinov, A. A., Energy aspects of the growth ofEscherichia coli synchronized by starvation. Microbiology56 (1987) 47–52.
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.
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.
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.
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.
Zechman, J. M., and Casida, L. E. Jr, Death ofPseudomonas aeruginosa in soil. Can. J. Microbiol.28 (1982) 788–794.
Author information
Authors and Affiliations
Rights 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
Published:
Issue Date:
DOI: https://doi.org/10.1007/BF01935529