Springer Nature is making SARS-CoV-2 and COVID-19 research free. View research | View latest news | Sign up for updates

Effects of heavy metals in soil on microbial processes and populations (a review)

Abstract

The effects of Cd, Cu, Zn, and Pb on soil microorganisms and microbially mediated soil processes are reviewed. The emphasis is placed on temperate forest soils. The sensitivity of different measurements is discussed, and data compiled to compare relative toxicity of different metals. On the whole the relative toxicity of the metals (on a μg g−1 soil basis) decreased in the order Cd > Cu > Zn > Pb, but differences between different investigations were found. The influence of abiotic factors on metal toxicity is briefly discussed and especially examplified by different soil organic matter content. Evidence of tolerance and adaptation in the soil environment and the time scale involved in the evolution of a metal-tolerant microbial community after metal exposure are also considered.

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

References

  1. Al-Khafaji, A. A. and Tabatabai, M. A.: 1979, Soil Sci. 127, 129.

  2. Arnebrant, K., Bååth, E. and Nordgren, A.: 1987, Mycologia 79, 890.

  3. Ashida, J.: 1965, Ann. Rev. Phytopath. 3, 153.

  4. Ausmus, B. S., Dodson, G. J., and Jackson, D. R.: 1978, Water, Air, and Soil Pollut. 10, 19.

  5. Babich, H., Bewley, R. J. F., and Stotzky, G.: 1983, Arch. Environ. Cont. Toxicol. 12, 421.

  6. Babich, H. and Stotzky, G.: 1977a, Appl. Environ. Microbiol. 33, 696.

  7. Babich, H. and Stotzky, G.: 1977b, Appl. Environ. Microbiol. 33, 1059.

  8. Babich, H. and Stotzky, G.: 1978a, Adv. Appl. Microbiol. 23, 55.

  9. Babich, H. and Stotzky, G.: 1978b, Appl. Environ. Microbiol. 36, 904.

  10. Babich, H. and Stotzky, G.: 1980, CRC Crit. Rev. Microbiol. 8, 99.

  11. Babich, H. and Stotzky, G.: 1982, Ecotox. Environ. Safety 6, 577.

  12. Babich, H. and Stotzky, G.: 1983a, in J. O. Nriagu (ed.), Aquatic Toxicology, Wiley, New York, p. 1.

  13. Babich, H. and Stotzky, G.: 1983b, Adv. Appl. Microbiol. 29, 195.

  14. Babich, H. and Stotzky, G.: 1983c, Environ. Health Perspect. 49, 247.

  15. Babich, H. and Stotzky, G.: 1985, Environ. Res. 36, 111.

  16. Barkay, T., Tripp, S. C., and Olson, B. H.: 1985, Appl. Environ. Microbiol. 49, 333.

  17. Bell, R., Evans, C. S., and Roberts, E. R.: 1988, Pl. Soil 106, 143.

  18. Benson, N. R. and Covey, R. P.: 1976, Hort. Sci. 11, 252.

  19. Benson, L. M., Evans, R. L., and Peterson, P. J.: 1980, Trans. Br. Mycol. Soc. 74, 199.

  20. Berg, B. and Staaf, H.: 1980, Ecol. Bull. 32, 373.

  21. Bewley, R. J. F. and Stotzky, G.: 1983a, Sci. Total Environ. 31, 41.

  22. Bewley, R. J. F. and Stotzky, G.: 1983b, Sci. Total Environ. 31, 57.

  23. Bewley, R. J. F. and Stotzky, G.: 1983c, Arch. Environ. Cont. Toxicol. 12, 285.

  24. Bewley, R. J. F. and Stotzky, G.: 1983d, Environ. Res. 31, 332.

  25. Bhuiya, M. R. H. and Cornfield, A. H.: 1972, Environ. Pollut. 3, 173.

  26. Bhuiya, M. R. H. and Cornfield, A. H.: 1974, Environ. Pollut. 7, 161.

  27. Bisessar, S.: 1982, Water, Air, and Soil Pollut. 17, 305.

  28. Bollag, J.-M. and Barabasz, W.: 1979, J. Environ. Qual. 8, 196.

  29. Bond, H., Lighthart, R., Shimabuku, R., and Russel, L.: 1976, Soil Sci. 121, 278.

  30. Bowen, G. D., Skinner, M. F., and Bevege, D. I.: 1974, Soil Biol. Biochem. 6, 141.

  31. Bradley, R., Burt, A. J., and Read, D. J.: 1981, Nature 292, 335.

  32. Bradley, R., Burt, A. J., and Read, D. J.: 1982, New Phytol. 91, 197.

  33. Brookes, P. C. and McGrath, S. P.: 1984, J. Soil Sci. 35, 341.

  34. Brookes, P. C., McGrath, S. P., and Heijnen, C.: 1986a, Soil Biol. Biochem. 18, 345.

  35. Brookes, P. C., Heijnen, C. E., McGrath, S. P., and Vance, E. D.: 1986b, Soil Biol. Biochem. 18, 383.

  36. Brown, M. T. and Wilkins, D. A.: 1985a, Trans. Br. Mycol. Soc. 84, 367.

  37. Brown, M. T. and Wilkins, D. A.: 1985b, New Phytol. 99, 101.

  38. Carter, A.: 1978, ‘Some Aspects of the Fungal Flora in Nickel-Contaminated and Non-contaminated Soils near Sudbury, Ontario, Canada’, M.Sc. Thesis. University of Ontario.

  39. Chaney, W. R., Kelly, J. M., and Strickland, R. C.: 1978, J. Environ. Qual. 7, 115.

  40. Chang, F.-H. and Broadbent, F. E.: 1981, Soil Sci. 132, 416.

  41. Chang, F.-H. and Broadbent, F. E.: 1982, J. Environ. Qual. 11, 1.

  42. Cole, M. A.: 1977, Appl. Environ. Microbiol. 33, 262.

  43. Colpaert, J. V. and Van Assche, J. A.: 1987, Funct. Ecol. 1, 415.

  44. Cornfield, A. H.: 1977, Geoderma 19, 199.

  45. Coughtrey, P. J., Jones, C. H., Martin, M. H., and Shales, S. W.: 1979, Oecologia 39, 51.

  46. Crist, T. O., Williams, N. R., Amthor, J. S., and Siccama, T. G.: 1985, Environ. Pollut. 38, 295.

  47. Darlington, A. B. and Rauser, W. E.: 1988, Can. J. Bot. 66, 225.

  48. DeCatanzaro, J. B. and Hutchinson, T. C.: 1985, Water, Air, and Soil Pollut. 24, 153.

  49. Denny, H. J. and Wilkins, D. A.: 1987a, New Phytol. 106, 535.

  50. Denny, H. J. and Wilkins, D. A.: 1987b, New Phytol. 106, 545.

  51. Dixon, R. K.: 1988, Soil Biol. Biochem. 20, 555.

  52. Doelman, P.: 1986, in V. Jensen, A. Kjöller, L. H. Sörensen (eds.), Microbial Communities in Soil, Elsevier, London and New York, p. 369.

  53. Doelman, P. and Haanstra, L.: 1979a, Soil Biol. Biochem. 11, 475.

  54. Doelman, P. and Haanstra, L.: 1979b, Soil Biol. Biochem. 11, 481.

  55. Doelman, P. and Haanstra, L.: 1979c, Soil Biota Biochem. 11, 487.

  56. Doelman, P. and Haanstra, L.: 1984, Pl. Soil 79, 317.

  57. Doelman, P. and Haanstra, L.: 1986, Biol. Fert. Soils 2, 231.

  58. Domsch, K. H.: 1984, Pl. Soil 76, 367.

  59. Dueck, Th. A., Visser, P., Ernst, W. H. O., and Schat, H.: 1986, Soil Biol. Biochem. 18, 331.

  60. Duxbury, T.: 1985, in K. C. Marshall (ed.) Advances in Microbial Ecology, Plenum Press, New York and London, p. 185.

  61. Duxbury, T. and Bicknell, B.: 1983, Soil Biol. Biochem. 15, 243.

  62. Ebregt, A. and Boldewijn, J. M. A. M.: 1977, Pl. Soil 47, 137.

  63. Eiland, F.: 1981, Danish J. Plant Soil Sci. 85, 39.

  64. Frankenberger, W. T. and Tabatabai, M. A.: 1981, Soil Sci. Soc. Am. J. 45, 1124.

  65. Freedman, B. and Hutchinson, T. C.: 1980a, Can. J. Bot. 58, 108.

  66. Freedman, B. and Hutchinson, T. C.: 1980b, Can. J. Bot. 58, 1722.

  67. Friedland, A. J., Johnson, A. H., and Siccama, T. G.: 1986, Can. J. Bot. 64, 1349.

  68. Gadd, G. M.: 1984, Trans. Br. mycol. Soc. 82, 546.

  69. Gadd, G. M. and Griffiths, A. J.: 1978, Microb. Ecol. 4, 303.

  70. Garcia-Toledo, A., Babich, H., and Stotzky, G.: 1985, Can. J. Microbiol. 31, 485.

  71. Gast, C. H., Jansen, E., Bierling, J., and Haanstra, L.: 1988, Chemosphere 17, 789.

  72. Giashuddin, M. and Cornfield, A. H.: 1978, Environ. Pollut. 15, 231.

  73. Giashuddin, M. and Cornfield, A. H.: 1979, Environ. Pollut. 19, 67.

  74. Gildon, A. and Tinker, P. B.: 1983a, New Phytol. 95, 247.

  75. Gildon, A. and Tinker, P. B.: 1983b, New Phytol. 95, 263.

  76. Gilmore, A. E.: 1971, J. Am. Soc. Hort. Sci. 96, 35.

  77. Graham, J. H., Timmer, L. W., and Fardelmann, D.: 1986, Phytopath. 76, 66.

  78. Greszta, J., Braniewski, S., Marezynska-Galkowska, K., and Nosek, A.: 1979, Ekol. Polska 27, 397.

  79. Haanstra, L. and Doelman, P.: 1984, Soil Biol. Biochem. 16, 595.

  80. Haanstra, L., Doelman, P. and Once Voshaar, J. H.: 1985, Pl. Soil 84, 293.

  81. Hartman, L. M.: 1976, ‘Fungal flora of the Soils as Conditioned by Varying Concentrations of Heavy Metals’, Ph.D. Thesis. University of Montana.

  82. Hayakawa, M., Iino, S., and Nonomura, H.: 1982, Hakkokogaku 60, 1.

  83. Hayman, D. S. and Tavares, M.: 1985, New Phytol. 100, 367.

  84. Inman, J. C. and Parker, G. R.: 1978, Environ. Pollut. 17, 39.

  85. Jackson, D. R. and Watson, A. P.: 1977, J. Environ. Qual. 6, 331.

  86. Jones, M. D. and Hutchinson, T. C.: 1986, New Phytol. 102, 429.

  87. Jones, M. D., Browning, M. H. R., and Hutchinson, T. C.: 1986, Water, Air, and Soil Pollut. 31, 441.

  88. Jordan, M. J. and Lechevalier, M. P.: 1975, Can. J. Microbiol. 21, 1855.

  89. Juma, M. G. and Tabatabai, M. A.: 1977, Soil Sci. Soc. Am. J. 41, 343.

  90. Kalin, M. and Stokes, P. M.: 1981, Sci. Total Environ. 19, 83.

  91. Kendrick, W. B.: 1962, Can. J. Microbiol. 8, 639.

  92. Khan, D. H. and Frankland, B.: 1984, Environ. Pollut. 33, 63.

  93. Killham, K. and Firestone, M. K.: 1983, Pl. Soil 72, 39.

  94. Klotz, R. L.: 1981, Environ. Pollut. 24, 1.

  95. Kuusi, T., Laaksovirta, K., Liukkonen-Lilja, H., Lodenius, M., and Piepponen, S.: 1981, Z. Lebensm. Untersuch. Forsch. 173, 261.

  96. Lapeyrie, F., Chilvers, G. A., and Bhem, C. A.: 1987, New Phytol. 106, 139.

  97. Laub, E., Waligorski, F., and Woller, R.: 1977, Z. Lebensm. Untersuch. Forsch. 164, 267.

  98. Lees, H.: 1948, Biochem. J. 42, 534.

  99. Liang, C. N. and Tabatabai, M. A.: 1977, Environ. Pollut. 12, 141.

  100. Liang, C. N. and Tabatabai, M. A.: 1978, J. Environ. Qual. 7, 291.

  101. Lighthart, B.: 1980, Ant. Leeuwenh. 46, 161.

  102. Lighthart, B., Baham, J., and Volk, V. V.: 1983, J. Environ. Qual. 12, 543.

  103. LoBuglio, K. F. and Wilcox, H. F.: 1988, Can. J. Bot. 66, 55.

  104. Mahler, I., Levinson, H. S., Wang, Y., and Halvorson, H. O.: 1986, Appl Environ. Microbiol. 52, 1293.

  105. Malajczuk, N. and Cromack, K. Jr.: 1982, New Phytol. 92, 527.

  106. Maliszewska, W., Dec, S., Wierzbicka, H., and Wozniakowska, A.: 1985, Environ. Pollut. 37, 195.

  107. Malloch, D. and Duja, A. L.: 1979, Can. J. Bot. 57, 1848.

  108. Marx, D. H. and Artman, J. D.: 1979, Reclam. Rev. 2, 23.

  109. Mathur, S. P. and Rayment, A. F.: 1977, Can. J. Soil Sci. 57, 397.

  110. Mathur, S. P. and Sanderson, R. B.: 1978, Can. J. Soil Sci. 58, 125.

  111. Mathur, S. P. and Preston, C. M.: 1981, Can. J. Soil Sci. 61, 445.

  112. Mathur, S. P., Hamilton, H. A., and Levesque, M. P.: 1979, Soil Sci. Soc. Am. J. 43, 200.

  113. Mathur, S. P., MacDougall, J. I., and McGrath, M.: 1980, Soil Sci. 129, 376.

  114. McGrath, S. P., Brookes, P. C., and Giller, K. E.: 1988, Soil Biol. Biochem. 20, 415.

  115. McIlveen, W. D. and Cole, Jr. H.: 1974, Phytopath. 64, 583.

  116. McIlveen, W. D. and Cole, Jr. H.: 1978/1979, Agr. Environ. 4, 245.

  117. McKenney, D. J. and Vriesacker, J. R.: 1985, Environ. Pollut. 38, 221.

  118. Mikkelsen, J. P.: 1974, Tids. Planteavl 78, 509.

  119. Minnich, M. M. and McBride, M. B.: 1986, Pl. Soil 91, 231.

  120. Morrissey, R. F.: 1975, ‘The Influence of Heavy Metals on Microbially Mediated Nitrogen Transformations in Soil: Nitrification and Ammonification’, Ph. D. Thesis. University of Connecticut.

  121. Morsfelt, A. F. W., Smits, W. T. M., and Limonard, T.: 1986, Pl. Soil 96, 417.

  122. Mowll, J. L. and Gadd, G. M.: 1985, Trans. Br. Mycol. Soc. 84, 685.

  123. Muskett, C. J. and Jones, M. P.: 1981, Water, Air, and Soil Pollut. 15, 329.

  124. Necker, U. and Kunze, C.: 1986, Angew. Bot. 60, 81.

  125. Nohrstedt, H.-Ö.: 1987, Scand. J. For. Res. 2, 13.

  126. Nordgren, A., Bååth, E., and Söderström, B.: 1983, Appl. Environ. Microbiol. 46, 1829.

  127. Nordgren, A., Bååth, E., and Söderström, B.: 1985, Can. J. Bot. 63, 448.

  128. Nordgren, A., Kauri, T., Bååth, E., and Söderström, B.: 1986, Environ. Pollut. 41, 89.

  129. Nordgren, A., Bååth, E., and Söderström, B.: 1988, Soil Biol. Biochem. 20, 949.

  130. Ohya, H., Komai, Y., and Yamaguchi, M.: 1985, Biol. Fert. Soils 1, 117.

  131. Ohya, H., Komai, Y., and Yamaguchi, M.: 1986, Biol. Fert. Soils 2, 59.

  132. Okamoto, K. and Fuwa, K.: 1974, Agr. Biol. Chem. 38, 1405.

  133. Olsen, R. A. and Bakken, L. R.: 1987, Microb. Ecol. 13, 59.

  134. Olson, B. H. and Thornton, I.: 1982, J. Soil Sci. 33, 271.

  135. Pancholy, S. K., Rice, E. L., and Turner, J. A.: 1975, J. Appl. Ecol. 12, 337.

  136. Porter, J. R. and Sheridan, R. P.: 1981, Pl. Physiol. 68, 143.

  137. Premi, P. R. and Cornfield, A. H.: 1969, Pl. Soil 31, 345.

  138. Preve, R. E., Burger, J. A., and Kreh, R. E.: 1984, J. Environ. Qual. 13, 387.

  139. Pyatt, F. B.: 1973, Trans, Br. Mycol. Soc. 61, 189.

  140. Quraishi, M. S. I. and Cornfield, A. H.: 1973, Environ. Pollut. 4, 159.

  141. Rogers, J. E. and Li, S. W.: 1985, Bull. Environ. Contam. Toxicol. 34, 858.

  142. Ross, I. S.: 1975, Trans. Br. Mycol. Soc. 64, 175.

  143. Ross, D. S., Sjogren, R. E., and Bartlett, R. J.: 1981, J. Environ. Qual. 10, 145.

  144. Rother, J. A., Millbank, J. W., and Thornton, J.: 1982a, J. Soil Sci. 33, 101.

  145. Rother, J. A., Millbank, J. W., and Thornton, J.: 1982b, Pl. Soil 69, 239.

  146. Rühling, Å.: 1983, Swedish Natural Environment Protection Board, PM 1727.

  147. Rühling, Å., Bååth, E., Nordgren, A., and Söderström, B.: 1984, Ambio 13, 34.

  148. Rühling, Å. and Tyler, G.: 1973, Oikos 24, 402.

  149. Rühling, Å. and Tyler, G.: 1979, Swedish Natural Environment Protection Board, PM 1150.

  150. Seeger, R.: 1978, Z. Lebensm. Untersuch. Forsch. 166, 23.

  151. Skujins, J., Nohrstedt, H. -O. and Oden, S.: 1986, Swedish J. Agr. Res. 16, 81.

  152. Spalding, B. P.: 1979, J. Environ. Qual. 8, 105.

  153. Stott, D. E., Dick, W. A., and Tabatabai, M. A.: 1985, Soil Sci. 139, 112.

  154. Strojan, C. L.: 1978, Oecologia 32, 203.

  155. Svenson, A.: 1986, Pl. Soil 94, 227.

  156. Swaminathan, K. and Verma, B. C.: 1979, New Phytol. 82, 481.

  157. Tabatabai, M. A.: 1977, Soil Biol. Biochem. 9, 9.

  158. Timmer, L. W. and Leyden, R. F.: 1980, New Phytol. 85, 15.

  159. Tyler, G.: 1974a, Swedish Natural Environment Protection Board, PM 542.

  160. Tyler, G.: 1974b, Pl. Soil 41, 303.

  161. Tyler, G.: 1975a, Nature 255, 701.

  162. Tyler, G.: 1975b, International Conference on Heavy Metals in the Environment. Toronto, Canada, p. 217.

  163. Tyler, G.: 1977, Swedish Natural Environment Protection Board, PM 861.

  164. Tyler, G.: 1980, Trans. Br. Mycol. Soc. 74, 41.

  165. Tyler, G.: 1981, in E. A. Paul and J. N. Ladd (eds.), Soil Biochemistry 5, Marcel Dekker, New York and Basel, p. 371.

  166. Tyler, G.: 1982, Trans. Br. Mycol. Soc. 79, 239.

  167. Tyler, G.: 1983, Ecological Effects of Acid Deposition, National Swedish Environment Protection Board, PM 1636, p. 245.

  168. Tyler, G.: 1984, Ambio 134, 18.

  169. Tyler, G., Mörnsjö, B., and Nilsson, B.: 1974, Pl. Soil 40, 237.

  170. Tyler, G. and Westman, L.: 1979, Swedish Natural Environment Protection Board, PM 1203.

  171. Vesper, S. J. and Weidensaul, T. C.: 1978, Water, Air, and Soil Pollut. 9, 413.

  172. Walter, C. and Stadelmann, F.: 1979, Schweiz Landwirts. Forsch. 18, 311.

  173. Warcup, J. H.: 1955, Trans. Br. Mycol Soc. 38, 298.

  174. Watson, A. P.: 1975, Proceedings of the Annual Conference on Trace Substances and Environmental Health, University of Missouri, p. 227.

  175. Williams, S. T., McNeilly, T., and Wellington, E. M. H.: 1977, Soil Biol. Biochem. 9, 271.

  176. Wilson, D. O.: 1977a, Soil Biol. Biochem. 9, 277.

  177. Wilson, D. O.: 1977b, Environ. Pollut. 12, 73.

  178. Yamamoto, H., Tatsuyama, K., Egawa, H., and Furuta, T.: 1981, Japan. J. Soil Sci. Pl. Nutr. 52, 119.

  179. Yamamoto, H., Tatsuyama, K., and Uchiwa, T.: 1985, Soil Biol. Biochem. 17, 785.

  180. Yang, S. H. and Ehrlich, H.: 1976, in J. M. Miles and A. M. Kaplan (eds.), Proceedings of the Third International Biodegradation Symposium, Applied Science Publishers, London, p. 867.

  181. Zibilski, L. M. and Wagner, G. H.: 1982, Soil Sci. 134, 364.

Download references

Author information

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Bååth, E. Effects of heavy metals in soil on microbial processes and populations (a review). Water Air Soil Pollut 47, 335–379 (1989). https://doi.org/10.1007/BF00279331

Download citation

Keywords

  • Heavy Metal
  • Organic Matter
  • Toxicity
  • Microbial Community
  • Soil Organic Matter