Biology and Fertility of Soils

, Volume 6, Issue 3, pp 189–203 | Cite as

Microenvironments of soil microorganisms

  • R. C. Foster


Ultrastructural studies of soil micro-organisms and the microenvironments surrounding them are reviewed. Soil microfauna, and bacteria, actinomycetes and fungi, fixed and embedded in situ, were examined by electron microscopy (both transmission and scanning). In some cases ultrastructural histochemistry was used to detect and identify the organic matter with which microorganisms were associated and to examine the polymeric microbial materials (enzymes, extracellular polysaccharides) they produced. Although some small organisms (0.3 μm diameter) occurred singly in dense fabrics of clay or humified organic matter, larger bacteria occurred in rhizospheres, in small colonies in the larger micropores or associated with substantial deposits of organic matter (faecal pellets, carbohydrate-rich plant cell-wall debris). Whereas rhizospheres had mixed microbial populations, individual microvoids in the bulk soil usually contained only one type of micro-organism. Following chloroform treatment, microorganisms were found only in mucigel deposits or deep in the interiors of micropores, suggesting that these constitute protected sites where microorganisms survive temporarily adverse conditions. Soil microfauna and fungi were mainly confined to the larger voids. Although some live hyphae occurred in the outer regions of aggregates, hyphae deep within soil fabrics were usually devoid of cytoplasmic organelles. Faecal pellets, plant tissues and cell-wall remnants comprised the most frequent, larger organic masses, while the most common micron- and submicron-sized organic matter consisted of fibrous or amorphous humified matter. Unequivocal detection of enzymes was limited to the surface of microorganisms.

Key words

Soil microorganisms Microenvironment Rhizobacteria Spatial distribution Soil enzymes Plant debris Carbohydrates 


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  1. Alexander M (1961) Introduction to soil microbiology. Wiley, New YorkGoogle Scholar
  2. Bae HC, Cota-Robles EH, Casida LE (1972) Microflora of soil as viewed by transmission electron microscopy. Appl Microbiol 23:637–648Google Scholar
  3. Barber DA, Martin JK (1976) The release of organic substances by cereal roots into soils. New Phytol 76:69–80Google Scholar
  4. Barclay WR, Lewin RA (1985) Microalgal polysaccharide production for the conditioning of agricultural soils. Plant Soil 88:159–169Google Scholar
  5. Barley KP (1970) The configuration of the root system in relation to nutrient uptake. Adv Agron 22:159–201Google Scholar
  6. Berthelin J (1984) Microbial weathering. In: Krumbein WE (ed) Microbial geochemistry. Blackwell Oxford, pp 223–262Google Scholar
  7. Berthelin J, Leyval C (1982) Ability of symbiotic and nonsymbiotic rhizospheric microflora of maize (Zea mays) to weather micas and to promote plant growth and plant nutrition. Plant Soil 68:369–377Google Scholar
  8. Binns ES (1980) Field and laboratory observations on the substrates of the mushroom fungus gnat Lycoriella auripila (Diptera: Sciaridae). Ann Appl Biol 96:143–152Google Scholar
  9. Bisdom EBA (1983) Submicroscopic examination of soils. Adv Agron 36:55–96Google Scholar
  10. Bland DE, Foster RC, Logan AF (1971) The mechanism of permanganate and osmium tetroxide fixation and the distribution of lignin in the wall of Pinus radiata. Holzforschung 25:137–143Google Scholar
  11. Buckley R (1982) Sand rhizosheath of an arid zone grass. Plant Soil 66:417–421Google Scholar
  12. Burns RG (1982) Enzyme activity in soil: location and a possible role in microbial ecology. Soil Biol Biochem 14:423–428Google Scholar
  13. Campbell R, Porter R (1982) Low temperature scanning electron microscopy of microorganisms on soil. Soil Biol Biochem 14:241–245Google Scholar
  14. Chakraborty S, Old KM, Warcup JH (1983) Amoebae from a take-all suppressive soil which feed on Gaeumannnomyces graminis var tritici and other soil fungi. Soil Biol Biochem 15:17–24Google Scholar
  15. Chen Y, Schnitzer M (1976) Scanning electron microscopy of humic acid and of a fulvic acid and its metal and clay complexes. Soil Sci Soc Am Proc 40:682–686Google Scholar
  16. Clarholm M (1985) Possible roles for roots bacteria, protozoa and fungi in supplying nitrogen to plants. In: Fitter AH, Atkinson D, Read DJ, Usher MB (eds) Ecological interactions in soil: Plants, microbes and animals. Blackwell, Oxford, pp 355–365Google Scholar
  17. Clarholm M, Rosswall T (1980) Biomass and turnover of bacteria in a forest soil and a peat. Soil Biol Biochem 12:49–57Google Scholar
  18. Cromack K, Sollins P, Graustein WC, Speidel K, Todd AW, Spycher G, Li CY, Todd RL (1979) Calcium oxalate accumulation and soil weathering in mats of the hypogeous fungus Hysterangium crassum. Soil Biol Biochem 11:463–468Google Scholar
  19. Darbyshire JF, Greaves MP (1967) Protozoa and bacteria in the rhizosphere of Sinapsis alba L., Trifolium repens L. and Lolium perenne L. Can J Microbiol 13:1057–1068Google Scholar
  20. Deacon JW, Mitchell RT (1985) Comparison of rates of natural senescence of the root cortex of wheat (with and without mildew infection), barley, oats and rye. Plant Soil 84:129–131Google Scholar
  21. Dickinson NM (1982) Investigations and measurement of root turnover in semi-permanent grassland. Rev Ecol Biol Sol 19:307–314Google Scholar
  22. Eckhardt FEW (1985) Solubilization, transport and deposition of mineral cations by microorganisms - efficient rock weathering agents. In: Drever JL (ed) The chemistry of weathering. Reidal, pp 161–173Google Scholar
  23. Finch P, Hayes MHB, Stacey M (1971) The biochemistry of soil polysaccharides. In: McLaren AD, Skujins J (eds) Soil biochemistry, vol 2. Dekker, New York, pp 257–319Google Scholar
  24. Flaig W, Beutelspacher H, Rietz E (1975) Chemical composition and physical properties of humic substances. In: Gieseking JE (ed) Soil components, vol 1, Organic components. Springer, Berlin Heidelberg New York, pp 1–211Google Scholar
  25. Fletcher M, Floodgate GD (1973) An electron-microscopic demonstration of the acidic polysaccharide involved in the adhesion of a marine bacterium to solid surfaces. J Gen Microbiol 74: 325–334Google Scholar
  26. Foster RC (1978) Ultramicromorphology of some South Australian soils. In: Emerson WW, Bond RD, Dexter AR (eds) Modification of soil structure. Wiley, New York, pp 103–109Google Scholar
  27. Foster RC (1981 a) Polysaccharides in soil fabrics. Science 214: 665–667Google Scholar
  28. Foster RC (1981 b) The ultrastructure and histochemistry of the rhizosphere. New Phytol 89:263–273Google Scholar
  29. Foster RC (1981 c) Mycelial strands of Pinus radiata D Don: Ultrastructure and histochemistry. New Phytol 88:705–712Google Scholar
  30. Foster RC (1981 d) Localization of organic materials in situ in ultrathin sections of natural soil fabrics by using cytochemical techniques. In: Bisdom EBA (ed) Submicroscopic techniques as applied to thin sections of undisturbed soil materials. Pudoc Press, Wageningen, Holland, pp 309–317Google Scholar
  31. Foster RC (1985) The biology of the rhizosphere. In: Parker CA, Rovira AD, Moore KJ, Wong PTW, Kollmorgen JF (eds) Ecology and management of soil borne plant pathogens. Am Phytopath Soc, St Paul, Minnesota, pp 75–79Google Scholar
  32. Foster RC (1986) In situ identification of organic materials in soils. Questiones Entomologicae 21:609–633Google Scholar
  33. Foster RC, Bowen GD (1982) Plant surfaces and bacterial growth: The rhizosphere and rhizoplane. In: Mount MS, Lacy GH (eds) Phytopathogenic prokaryotes, vol 1. Academic Press, New York, pp 159–185Google Scholar
  34. Foster RC, Marks GC (1967) Observations on the mycorrhizas of forest trees. II. The rhizosphere of Pinus radiata D. Don. Aust J Biol Sci 20:915–926Google Scholar
  35. Foster RC, Martin JK (1981) In situ analysis of soil components of biological origin. In: Paul EA, Ladd JN (eds) Soil biochemistry, vol 5. Dekker, New York, pp 75–110Google Scholar
  36. Foster RC, Rovira AD (1978) The ultrastructure of the rhizosphere of Trifolium subterraneum L. In: Loutit MW, Miles JAR (eds) Microbial ecology. Springer, Berlin Heidelberg New York, pp 278–290Google Scholar
  37. Foster RC, Rovira AD, Cock TW (1983) Ultrastructure of the root-soil interface. Am Phytopath Soc, St Paul, Minn, USAGoogle Scholar
  38. Frehel C, Ryter A (1982) Electron microscopic cytochemical study of cell-wall polysaccharides in Bacillus subtilis and two strains of Bacillus megaterium. J Ultrastruct Res 81:66–77Google Scholar
  39. Gianinazzi S, Gianinazzi-Pearson V, Dexheimer J (1979) Enzymatic studies on the metabolism of vesicular-arbuscular mycorrhiza. III. Ultrastructural localization of acid and alkaline phosphatase in onion roots infected by Glomus mosseae (Nicol & Gerd). New Phytol 82:127–132Google Scholar
  40. Gianinazzi S, Dexheimer J, Gianinazzi-Pearson V, Marx C (1983) Role of the host - arbuscule interface in the VA mycorrhizal symbiosis: Ultracytological studies of the processes involved in phosphate and carbohydrate exchange. Plant Soil 71:211–215Google Scholar
  41. Greenland DJ, Oades JM (1975) Saccharides. In: Gieseking JE (ed) Soil components, vol 1, Organic components. Springer, Berlin Heidelberg New York, pp 213–261Google Scholar
  42. Griffin DM (1981) Water and microbial stress. In: Alexander M (ed) Advances in microbial ecology, vol 5. Plenum, New York, pp 91–136Google Scholar
  43. Hattori T, Hattori R (1976) The physical environment in soil microbiology: An attempt to extend the principles of microbiology to soil microorganisms. Crit Rev Microbiol 4:423–461Google Scholar
  44. Head GC (1967) Studies of growing roots by time-lapse cinematography. Trans 9th Int Congr Soil Sci, vol 1, pp 751–758Google Scholar
  45. Henry CM, Deacon JW (1981) Natural (non-pathogenic) death of the cortex of wheat and barley seminal roots, as evidenced by nuclear staining with acridine orange. Plant Soil 60:255–274Google Scholar
  46. Heritage AD, Foster RC (1984) Catalase and sulfur in the rice rhizosphere: An ultrastructural histochemical demonstration of a symbiotic relationship. Microbiol Ecol 10:115–121Google Scholar
  47. Hillis WE, Ishikura N, Foster RC (1968) The role of extractives in the formation of ectrotropic mycorrhizae. Phytochemistry 7: 409–410Google Scholar
  48. Hissett R, Gray TRG (1976) Microsites and time changes in soil microbe ecology. In: Anderson JM, MacFadyen A (eds) The role of terrestrial and aquatic organisms in decomposition processes. Blackwell, Oxford, pp 23–39Google Scholar
  49. Jenkinson DS, Ladd JN (1981) Microbial biomass in soil: Measurement and turnover. In: Paul EA, Ladd JN (eds) Soil biochemistry, vol 5. Dekker, New York, pp 415–471Google Scholar
  50. Jenkinson DS, Powlson DS (1976) The effects of biocidal treatments on metabolism in soil. V. A method for measuring soil biomass. Soil Biol Biochem 8:209–213Google Scholar
  51. Jenny H, Grossenbacher KA (1963) Root-soil boundary zones as seen in the electron microscope. Soil Sci Soc Am Proc 27:273–277Google Scholar
  52. Kilbertus G (1980) Etude des microhabitats contenus dans les aggrégats du sol, leur relation avec la biomasse bactériene et la taille des procaryotes presents. Rev Ecol Biol Sol 17:543–557Google Scholar
  53. Kilbertus G, Reisinger O (1975) Déegradation du matériel végétal activité in vitro et in situ de quelques microorganismes. Rev Ecol Biol Sol 12:363–374Google Scholar
  54. Knight DP, Lewis PR (1977) General cytochemical methods. In: Lewis PR, Knight DP (eds) Staining methods for sectioned material. Elsevier/North Holland, Amsterdam, pp 77–135Google Scholar
  55. Knutson DM, Hutchins AS, Cromack K (1980) The association of calcium oxalate-utilizing Streptomyces with conifer ectomycorrhizae. Antonie van Leeuwenhoek; J Microbiol Serol 46: 611–619Google Scholar
  56. Ladd JN, Paul EA (1973) Changes in enzymatic activity and distribution of acid-soluble, amino acid-nitrogen in soil during nitrogen immobilization and mineralization. Soil Biol Biochem 5:825–840Google Scholar
  57. Ladd JN, Oades JM, Amato M (1981) Microbial biomass formed from 14C, 15N-labelled plant material decomposing in soils in the field. Soil Biol Biochem 13:119–126Google Scholar
  58. Lyda SD (1981) Alleviating pathogen stress. In: Arkin GF, Taylor HM (eds) Modifying the root environment to reduce crop stress. ASAE monograph No 4. Am Soc Agric Eng, Michigan, pp 195–214Google Scholar
  59. Luft JH (1976) The structure and properties of the cell surface coat. Int Rev Cytol 45:291–382Google Scholar
  60. Lundgren B (1984) Size classification of soil bacteria: Effects on microscopically estimated biovolumes. Soil Biol Biochem 16: 283–284Google Scholar
  61. Malajczuk N (1979a) Biological suppression of Phytophthora cinnamomi in eucalypts and avocados in Australia. In: Schippers B, Gams W (eds) Soil-borne plant pathogens. Academic Press, London, pp 635–652Google Scholar
  62. Malajczuk N (1979b) The microflora of unsuberized roots of Eucalyptus calophylla R. Br and E. marginata Donn ex Sm. Seedlings grown in soils suppressive and conducive to Phytophthora cinnamomi: II. Mycorrhizal roots and associated microflora. Aust J Bot 27:255–272Google Scholar
  63. Malajczuk N, Cromack K (1982) Accumulation of calcium oxalate in the mantle of ectomycorrhizal roots of Pinus radiata and Eucalyptus marginata. New Phytol 92:527–531Google Scholar
  64. Marinozzi V (1961) Silver impregnation of ultrathin sections for electron microscopy. J Biophys Biochem Cytol 9:121–133Google Scholar
  65. Marks GC, Foster RC (1973) Structure, morphogenesis and ultrastructure of ectomycorrhizae. In: Marks GC, Kozlowski TT (eds) Ectomycorrhizae: Their ecology and physiology. Academic Press, New York, pp 1–41Google Scholar
  66. Martin JK (1977) Factors influencing the loss of organic carbon from wheat roots. Soil Biol Biochem 9:1–9Google Scholar
  67. Martin JK, Foster RC (1985) A model system for studying the biochemistry and biology of the root-soil interface. Soil Biol Biochem 17:261–269Google Scholar
  68. Martin JK, Puckridge DW (1982) Carbon flow through the rhizosphere of wheat crops in South Australia. In: Galbally IE, Freney JR (eds) The cycling of carbon, nitrogen, sulfur and phosphorus in terrestrial and aquatic ecosystems. Austr Acad Sci, Canberra, Australia, pp 77–82Google Scholar
  69. Martinez R, McLaren AD (1966) Some factors influencing the determination of phosphatase activity in native soils and in soils sterilized by irradiation. Enzymologia 31:22–38Google Scholar
  70. Martinez AT, Montez C, Toutain F, Mangenot F (1980) Influence d'épaisseur de la litière et du type sol sur les processus de biodegradation de feuilles de hêtre. Rev Ecol Biol Sol 17:307–325Google Scholar
  71. Mugwira LM, Elgawhary SM (1979) Aluminum accumulation and tolerance of triticale and wheat in relation to root cation exchange capacity. Soil Sci Soc Am Proc 43:736–740Google Scholar
  72. Oades JM, Ladd JN (1977) Biochemical properties: Carbon and nitrogen metabolism. In: Russel JS, Greacen EL (eds) Soil factors in crop production in a semi-arid environment. University of Queensland Press, Australia, pp 127–160Google Scholar
  73. Pears AGE (1972) Histochemistry: Theoretical and applied, vol 1, 3rd edn. Churchill, LondonGoogle Scholar
  74. Pickett-Heaps JD (1967) Preliminary attempts at ultrastructural polysaccharide localization in root tip cells. J Histochem Cytochem 15:442–455Google Scholar
  75. Poindexter JS (1981) Oligotrophy: Fast and famine existence. In: Alexander M (ed) Advances in microbial ecology vol 5. Plenum, New York, pp 63–89Google Scholar
  76. Powlson DS (1980) The effects of grinding on microbial and nonmicrobial organic matter in soil. J Soil Sci 31:77–85Google Scholar
  77. Ramsay AJ (1984) Extraction of bacteria from soil: Efficiency of shaking or ultrasonication as indicated by direct counts and autoradiography. Soil Biol Biochem 16:475–481Google Scholar
  78. Robinson JM, Karnovsky MJ (1983) Ultrastructural localization of several phosphatases with cerium. J Histochem Cytochem 31:1197–1208Google Scholar
  79. Roland JC (1978) General preparation and staining of thin sections. In: Hall JL (ed) Electron microscopy and cytochemistry of plant cells. Elsevier/North Holland, Amsterdam, pp 1–62Google Scholar
  80. Rovira AD (1965) Plant root exudates and their influence upon soil microorganisms. In: Baker KF, Snyder WC (eds) Ecology of soil-borne plant pathogens. University of California Press, Berkeley, Los Angeles, pp 170–184Google Scholar
  81. Rovira AD, Greacen EL (1957) The effect of aggregate disruption on the activity of microorganisms in soil. Austr J Agric Res 8: 659–673Google Scholar
  82. Rybicka K (1981) Simultaneous demonstration of glycogen and protein in glycosomes of cardiac tissue. J Histochem Cytochem 29:4–8Google Scholar
  83. Shields JA, Paul EA, Lowe WE, Parkinson D (1973) Turnover of microbial tissue in soil under field conditions. Soil Biol Biochem 5:753–764Google Scholar
  84. Skinner FA, Jones PCT, Mollison JE (1952) A comparison of a direct and a plate counting technique for the quantitative estimation of soil microorganisms. J Gen Microbiol 6:261–271Google Scholar
  85. Smart P (1974) Electron microscope methods in soil micromorphology. In: Rutherford GK (ed) Soil microscopy. Limestone Press, Kingston, Ontario, pp 190–206Google Scholar
  86. Sollins P, Fogel R, Ching YL (1981) Role of low molecular weight organic acids in the inorganic nutrition of fungi and higher plants. In: Wicklow DT, Carrol GC (eds) The fungal community. Dekker, New York, pp 607–619Google Scholar
  87. Sparling GP (1985) The soil biomass. In: Vaughan D, Malcolm RE (eds) Soil organic matter and biological activity. Martinus Nijhoff Junk, Dordrecht, pp 223–262Google Scholar
  88. Sparling GP, Cheshire MV (1985) Effect of periodate oxidation on the polysaccharide content and microaggregate stability of rhizosphere and non rhizosphere soils. Plant Soil 88:113–122Google Scholar
  89. Stout JD, Heal OW (1967) Protozoa. In: Burges A, Raw F (eds) Soil biology. Academic Press, London, pp 149–195Google Scholar
  90. Swift JA, Saxton CA (1967) The ultrastructural location of the periodate-Schiffs reactive basement membrane at the dermoepidermal junctions of human scalp and monkey gingiva. J Ultra Res 17:23–33Google Scholar
  91. Taylor JSH, Fawcett JW, Hirst L (1984) The use of backscattered electrons to examine selectively stained nerve fibres in the scanning electron microscope. Stain Technol 59:335–341Google Scholar
  92. Thièry JP (1967) Mise en évidence des polysaccharides sur coupes fines en microscopie électronique. J Microsc (Paris) 6:987–1018Google Scholar
  93. Toogood JA, Lynch DL (1959) Effect of cropping systems and fertilizers on mean weight-diameter of aggregates of Breton plot soil. Can J Soil Sci 83:151–156Google Scholar
  94. Tyler G (1981) Heavy metals in soil biology and biochemistry. In: Paul EA, Ladd JN (eds) Soil biochemistry, vol 5. Dekker, New York, pp 371–414Google Scholar
  95. Van Vuurde JWL, Schippers B (1980) Bacterial colonization of seminal wheat roots. Soil Biol Biochem 12:559–565Google Scholar
  96. Van Vuurde JWL, Kruyswyk CJ, Schippers B (1979) Bacterial colonization of wheat roots in a root-soil model system. In: Schippers B, Gams W (eds) Soil-borne plant pathogens. Academic Press, London, pp 229–234Google Scholar
  97. Visser S (1985) Role of the soil invertebrates in determining the composition of soil microbial communities. In: Fitter AH, Atkinson D, Read DJ, Usher MB (eds) Ecological interactions in soil: Plants, microbes and animals. Blackwell, Oxford, pp 297–317Google Scholar
  98. Whitehead DC, Buchan H, Hartley RD (1979) Composition and decomposition of roots of ryegrass and red clover. Soil Biol Biochem 11:619–628Google Scholar
  99. Woods LE, Cole CV, Elliot ET, Anderson RV, Coleman DC (1982) Nitrogen transformations in soil as affected by bacterialmicrofaunal interactions. Soil Biol Biochem 14:93–98Google Scholar

Copyright information

© Springer-Verlag 1988

Authors and Affiliations

  • R. C. Foster
    • 1
  1. 1.CSIRO Division of SoilsSouth AustraliaAustralia

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