Plant and Soil

, Volume 174, Issue 1–2, pp 211–224 | Cite as

Biological N2 fixation by heterotrophic and phototrophic bacteria in association with straw

  • Margaret M. Roper
  • J. K. Ladha


Much of the crop residues, including cereal straw, that are produced worldwide are lost by burning. Plant residues, and in particular straw, contain large amounts of carbon (cellulose and hemicellulose) which can serve as substrates for the production of microbial biomass and for biological N2 fixation by a range of free-living, diazotrophic bacteria. Microorganisms with the dual ability to utilise cellulose and fix N2 are rate, but some strains that utilize hemicellulose and fix N2 have been found. Generally, cellulolysis and diazotrophy are carried out by a mixed microbial community in which N2-fixing bacteria utilise cellobiose and glucose produced from straw by cellulolytic microorganisms. N2-fixing bacteria include heterotrophic and phototrophic organisms and the latter are apparently more prominent in flooded soils such as rice paddies than in dryland soils. The relative contributions of N2 fixed by heterotrophic diazotrophic bacteria compared with cyanobacteria and other phototrophic bacteria depend on the availability of substrates from straw decomposition and on environmental pressures. Measurements of asymbiotic N2 fixation are limited and variable but, in rice paddy systems, rates of 25 kg N ha-1 over 30 days have been found, whereas in dryland systems with wheat straw, in situ measurements have indicated up to 12 kg N ha-1 over 22 days. Straw-associated N2 fixation is directly affected by environmental factors such as temperature, moisture, oxygen concentration, soil pH and clay content as well as farm management practices. Modification of managements and use of inoculants offer ways of improving asymbiotic N2 fixation.

In laboratory culture systems, inoculation of straws with cellulolytic and diazotrophic microorganisms has resulted in significant increases in N2 fixation in comparison to uninoculated controls and gains of N of up to 72 mg N fixed g-1 straw consumed have been obtained, indicating the potential of inoculation to improve N gains in composts that can then be used as biofertilisers. Soils, on the other hand, contain established, indigenous microbial populations which tend to exclude inoculant microorganisms by competition. As a consequence, improvements in straw-associated N2 fixation in soils have been achieved mostly by specific straw-management practices which encourage microbial activity by straw-decomposing and N2-fixing microorganisms.

Further research is needed to quantify more accurately the contribution of asymbiotic N2 fixation to cropping systems. New strains of inoculants, including those capable of both cellulolytic and N2-fixing activity, are needed to improve the N content of biofertilisers produced from composts. Developments of management practices in farming systems may result in further improvements in N2 fixation in the field.

Key words

decomposition heterotrophic/phototrophic bacteria N2 fixation, straw 


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  1. Abd-el Malek Y, Monib M, Gohar M R, Rizk S G and Antoun G G 1976 Decomposition of organic matter under different conditions with special reference to changes in plant nutrients. Soil Organic Matter Studies Symp. IAEA-SM-211/27. pp 183–195. IAEA, Vienna.Google Scholar
  2. Alexander M 1961 Introduction to Soil Microbiology. Wiley, New York. p 472.Google Scholar
  3. Araragi M and Tangcham B 1979 Effect of rice straw on the composition of volatile soil gas and microflora in the tropical paddy field. Soil Sci. Plant Nutr. 25, 283–295.Google Scholar
  4. Ayanaba A and Okigbo B N 1975 Mulching for improved soil fertility and crop production. In Organic Material as Fertilizers Report of the FAO/SIDA Expert Consultation, Rome, December 1994. pp 97–119. Food and Agriculture Organization of the United Nations, Rome.Google Scholar
  5. Barder M J and Crawford D L 1981 Effects of carbon and nitrogen supplementation on lignin and cellulose decomposition by a Streptomyces. Can. J. Microbiol. 27, 859–863.Google Scholar
  6. Barrow N J and Jenkinson D S 1962 The effect of water-logging on fixation of nitrogen by soil incubated with straw. Plant and Soil 26, 258–262.Google Scholar
  7. Baver L D 1956 Soil Physics, 3rd edn. John Wiley and Sons, New York.Google Scholar
  8. Brouzes R, Lasik J and Knowles R 1969 The effect of organic amendment, water content, and oxygen on the incorporation of 15N2 by some agricultural and forest soils. Can. J. Microbiol. 15, 899–905.Google Scholar
  9. Brouzes R and Knowles R 1973 Kinetics of nitrogen fixation in a glucose-amended, anaerobically incubated soil. Soil Biol Biochem. 5, 223–229.Google Scholar
  10. Cejudo F J and Paneque A 1986 Short-term nitrate (nitrite) inhibition of nitrogen fixation in Azotobacter chroococcum. J. Bacteriol. 165, 240–243.Google Scholar
  11. Chapman L S, Halsall D M and Gibson A H 1992 Biological nitrogen fixation and sugarcane. In Proceedings of Australian Society of Sugar Cane Technologists. Ed. B T Egan. pp 90–93. Mackay, Queensland.Google Scholar
  12. Charyulu P B B N and Rao R 1979 Nitrogen fixation in some Indian rice soils. Soil Sci. 128, 86–89.Google Scholar
  13. Chatterjee S K and Nandi B 1981 Biodegradation of wheat stubbles by soil micro-organisms and role of the products on soil fertility. Plant and Soil 59, 381–389.Google Scholar
  14. Choudhary N, Gray P P and Dunn N W 1980 Reducing sugar accumulation from alkali pretreated sugar cane bagasse using Cellulomonas. Eur. J. Appl. Microbiol. 11, 50–54.Google Scholar
  15. Christensen B T 1987 Decomposability of organic matter in particle size fractions from field soils with straw incorporation. Soil Biol. Biochem. 19, 429–435.Google Scholar
  16. Cogle A L, Strong W M, Saffigna P G, Ladd J N and Amato M 1987 Wheat straw decomposition in subtropical Australia. II. Effect of straw placement on decomposition and recovery of added 15N-urea. Aust. J. Soil Res. 25, 481–490.Google Scholar
  17. Dalton H 1980 The cultivation of diazotrophic microorganisms. In Methods for Evaluating Biological Nitrogen Fixation. Ed. F J Bergersen. pp 13–64. John Wiley and Sons, Chichester.Google Scholar
  18. Delwiche C C and Wijler J 1956 Non-symbiotic nitrogen fixation in soil. Plant and Soil 7, 113–129.Google Scholar
  19. Dickinson C H 1974 Decomposition of litter in soil. In Biology of Plant Litter Decomposition. Eds. C H Dickinson and G J F Pugh. pp 633–658. Academic Press, London.Google Scholar
  20. Doran J W 1980 Microbial changes associated with residue management with reduced tillage. Soil Sci. Soc. Am. J. 44, 518–524.Google Scholar
  21. Douglas C L, Allmaras R R, Rasmussen P E, Ramig R E and Roager N C 1980 Wheat straw composition and placement effects on decomposition in dryland agriculture of the Pacific Northwest. Soil Sci. Soc. Am. J. 44, 833–837.Google Scholar
  22. Egawa T 1975 Utilization of organic materials as fertilizers in Japan. In Organic Material as Fertilizers Report of the FAO/SIDA Expert Consultation, Rome, December 1974. pp 253–271. Food and Agriculture Organization of the United Nations, Rome.Google Scholar
  23. Flinn J C and Marciano V P 1984 Rice straw and stubble management. In Organic Matter and Rice. pp 566–593. International Rice Research Institute, Manila.Google Scholar
  24. Forbes R S 1974 Decomposition of agricultural crop debris. In Biology of Plant Litter Decomposition. Eds. C H Dickinson and G J F Pugh. pp 723–742. Academic Press, London.Google Scholar
  25. Gibson A H, Roper M M and Halsall D M 1988 Nitrogen fixation not associated with legumes. In Advances in Nitrogen Cycling in Agricultural Ecosystems. Ed. J R Wilson. pp 66–88. CAB International, Wallingford, UK.Google Scholar
  26. Greene R V and Freer S 1986 Growth characteristics of a novel nitrogen-fixing cellulolytic bacterium. Appl. Environ. Microbiol. 52, 982–986.Google Scholar
  27. Greenwood D J and Goodman D 1964 Oxygen diffusion and aerobic respiration in soil spheres. J. Sci. Food Agric. 15, 579–588.Google Scholar
  28. Habte M and Alexander M 1980 Nitrogen fixation by photosynthetic bacteria in lowland rice culture. Appl. Environ. Microbiol. 39, 342–347.Google Scholar
  29. Halsall D M and Gibson A H 1985 Cellulose decomposition and associated nitrogen fixation by mixed cultures of Cellulomonas gelida and Azospirillum species or Bacillus macerans. Appl. Environ. Microbiol. 50, 1021–1026.Google Scholar
  30. Halsall D M and Gibson A H 1986 Comparison of two Cellulomonas strains and their interaction with Azospirillum brasilense in degradation of wheat straw and associated nitrogen fixation. Appl. Environ. Microbiol. 51, 855–861.Google Scholar
  31. Halsall D M and Gibson A H 1989 Nitrogenase activity by diazotrophs grown on a range of agricultural plant residues. Soil Biol. Biochem. 21, 1037–1043.Google Scholar
  32. Halsall D M, Turner G L and Gibson A H 1985 Straw and xylan utilization by pure cultures of nitrogen-fixing Azospirillum spp. Appl. Environ. Microbiol. 49, 423–428.Google Scholar
  33. Harper S H T and Lynch J M 1981 The chemical components and decomposition of wheat straw leaves, internodes and nodes. J. Sci. Food Agric. 43, 1057–1062.Google Scholar
  34. Harper S H T and Lynch J M 1984 Nitrogen fixation by cellulolytic communities at aerobic-anaerobic interfaces in straw. J. Appl. Bacteriol. 57, 131–137.Google Scholar
  35. Harper S H T and Lynch J M 1986 Dinitrogen fixation by obligate and facultative anaerobic bacteria in association with cellulolytic fungi. Curr. Microbiol. 14, 127–131.Google Scholar
  36. Havelka U D, Boyle M G and Hardy R W F 1982 Biological nitrogen fixation. In Nitrogen in Agricultural Soils. Agronomy Monograph No. 22. pp 365–422. ASA-CSSA-SSSA, Madison, Wisconsin.Google Scholar
  37. Hill N M, Patriquin D G and Sircom K 1990 Increased oxygen consumption at warmer temperatures favours aerobic nitrogen fixation in plant litters. Soil Biol. Biochem. 22, 321–325.Google Scholar
  38. Imshenetsky A A 1967 Decomposition of cellulose in the soil. In The Ecology of Soil Bacteria. An International Symposium. Eds. T R G Gray and D Parkinson. pp 256–269. Liverpool University Press, Liverpool.Google Scholar
  39. Inoko A 1984 Compost as a source of plant nutrients. In Organic Matter and Rice. pp 137–145. International Rice Research Institute, Manila.Google Scholar
  40. Jensen H L and Swaby R J 1941 Association between nitrogen-fixing and cellulose-decomposing microorganisms. Nature 147, 147–148.Google Scholar
  41. Jensen V 1981 Heterotrophic micro-organisms. In N2 fixation. Vol. 1: Ecology. Ed. W J Broughton. pp 30–56. Clarendon Press, Oxford.Google Scholar
  42. Jones K and Bangs D 1985 Nitrogen fixation by free-living heterotrophic bacteria in an oak forest: the effect of liming. Soil Biol. Biochem. 17, 705–709.Google Scholar
  43. Kalininskaya T A 1972 Decomposition of cellulose and fixation of nitrogen in the soils of various types. Symp. Biol. Hung. 11, 135–138.Google Scholar
  44. Kimura M, Panichsakpatana S, Wada H and Takai Y 1979 Influences of organic debris and rice root on the nitrogen fixation in the submerged soil. Soil Sci. Plant Nutr. 25, 637–640.Google Scholar
  45. Knowles R 1976 Factors affecting dinitrogen fixation by bacteria in natural and agricultural systems. In Proceedings of the 1st International Symposium on N2 Fixation. Vol 2. Eds. W E Newton and C J Nyman. pp 539–555. Washington State University, Washington DC.Google Scholar
  46. Knowles R and Denike D 1974 Effect of ammonium-, nitrite- and nitrate-nitrogen on anaerobic nitrogenase activity in soil. Soil Biol. Biochem. 6, 353–358.Google Scholar
  47. Kobayashi M 1982 The role of phototrophic bacteria in nature and their utilization. In Advances in Agricultural Microbiology. Ed. N S Subba Rao. pp 643–661. Oxford and IBH Publishing Co., New Delhi.Google Scholar
  48. Kobayashi M and Haque M Z 1971 Contribution to nitrogen fixation and soil fertility by photosynthetic bacteria. Plant and Soil, Spec. Vol., 443–456.Google Scholar
  49. Kobayashi M, Takahashi E and Kawaguchi K 1967 Distribution of nitrogen-fixing microorganisms in paddy soils of Southeast Asia. Soil Sci. 104, 113–118.Google Scholar
  50. Ladha J K 1986 Studies on N2 fixation by free-living and rice plant-associated bacteria in wetland rice field. Bionature 6, 47–58.Google Scholar
  51. Ladha J K, Padre A T, Nayak D N, Garcia M and Watanabe I 1986a Nitrogen fixation by single and mixed heterotrophic bacteria in flooded paddy soils amended with hydrogen peroxide treated straw (hemicellulose). In Proceedings of the IV International Symposium on Microbial Ecology. pp 603–608. Ljubljana, Yugoslavia.Google Scholar
  52. Ladha J K, Tirol A C, Daroy M L G, Caldo G, Ventura W and Watanabe I 1986b Plant-associated N2 fixation (C2H2-reduction) by five rice varieties, and relationship with plant growth characters as affected by straw incorporation. Soil Sci. Plant Nutr. 32, 91–106.Google Scholar
  53. Ladha J K, Tirol-Padre A, Daroy M L G, Punzalan G and Watanabe I 1987 The effects on N2 fixation (C2H2 reduction), bacterial population and rice plant growth of two modes of straw application to a wetland rice field. Biol. Fertil. Soils 5, 106–111.Google Scholar
  54. La Rue T A 1977 The bacteria. In A Treatise on Dinitrogen Fixation. Section III, Biology. Eds. R W F Hardy and W S Silver. pp 19–62. John Wiley and Sons, New York.Google Scholar
  55. Leschine S B, Holwell K and Canale-Parola E 1988 Nitrogen fixation by anaerobic cellulolytic bacteria. Science 242, 1157–1159.Google Scholar
  56. Lethbridge G and Davidson M S 1983 Microbial biomass as a source of nitrogen for cereals. Soil Biol. Biochem. 15, 375–376.Google Scholar
  57. Lynch J M 1983 Soil Biotechnology-Microbiological Factors in Crop Productivity. Blackwell Scientific Publications, Oxford, London. 191p.Google Scholar
  58. Lynch J M and Harper S H T 1983 Straw as a substrate for cooperative nitrogen fixation. J. Gen. Microbiol. 129, 251–253.Google Scholar
  59. Macura J and Pavel L 1959 The influence of montmorillonite on nitrogen fixation by Azotobacter Folia Microbiol 4, 82–90.Google Scholar
  60. Magdoff F R and Bouldin D R 1970 Nitrogen fixation in submerged soil-sand-energy material media and the aerobic-anaerobic interface. Plant and Soil 33, 49–61.Google Scholar
  61. Marshall K C 1975 Clay mineralogy in relation to survival of soil bacteria. Ann. Rev. Phytopathol. 13, 357–373.Google Scholar
  62. Matsuguchi T 1979 Factors affecting heterotrophic nitrogen fixation in submerged rice soils. In Nitrogen and Rice. pp 207–222. International Rice Research Institute, Manila.Google Scholar
  63. Matsuguchi T and Yoo I D 1981 Stimulation of phototrophic N2 fixation in paddy fields through rice straw application. In Nitrogen Cycling in Southeast Asian Wet Monsoonal Ecosystems. Eds. R Wetselaar, J R Simpson and T Rosswall. pp 18–25. Australian Academy of Science, Canberra.Google Scholar
  64. Nayak D N, Ladha J K and Watanabe I 1986 The fate of marker Azospirillum lipoferum inoculated into rice and its effect on growth, yield and N2 fixation of plants studied by acetylene reduction, 15N2 feeding and 15N dilution techniques. Biol. Fertil. Soils 2, 7–14.Google Scholar
  65. Neue H U and Scharpenseel H W 1984 Gaseous products of the decomposing of organic matter in submerged soils. In Organic Matter and Rice. pp 311–328. International Rice Research Institute, Manila.Google Scholar
  66. Novak B 1972 Effect of increasing amounts of nitrogen on the microbial transformation of straw in soil. Symp. Biol. Hung. II, 49–53.Google Scholar
  67. Novakova J and Sisa R 1984 Effect of clays on the cellulolytic activity of soil. Zentralbl. Mikrobiol. 139, 505–510.Google Scholar
  68. Pal D, Broadbent F E and Mikkelsen D S 1975 Influence of temperature on the kinetics of rice straw decomposition in soils. Soil Sci. 120, 442–449.Google Scholar
  69. Parr J F and Papendick R I 1978 Factors affecting the decomposition of crop residues by microorganisms. In Crop Residue Management Systems. Am. Soc. Agron. Spec. Publ. pp 101–129. Am. Soc. Agron., Madison, Wisconsin.Google Scholar
  70. Patriquin D G 1982 Nitrogen fixation in sugar cane litter. Biol. Agric. Hort. 1, 39–64.Google Scholar
  71. Peoples M B, Herridge D F and Ladha J K 1995 Biological Nitrogen Fixation: an efficient source of nitrogen for sustainable agricultural production? Plant and Soil 174.Google Scholar
  72. Ponnamperuma F N 1984 Straw as source of nutrients for wetland rice. In Organic Matter and Rice. pp 117–136. International Rice Research Institute, Manila.Google Scholar
  73. Rao V R 1976 Nitrogen fixation as influenced by moisture content, ammonium sulphate and organic sources in a paddy soil. Soil Biol. Biochem. 8, 445–448.Google Scholar
  74. Rao V R 1978 Effect of carbon sources on asymbiotic nitrogen fixation in a paddy soil. Soil Biol. Biochem. 10, 319–321.Google Scholar
  75. Rao V R 1980 Changes in nitrogen fixation in flooded paddy field soil amended with rice straw and ammonium sulphate. Riso 28, 29–34.Google Scholar
  76. Reddy K R and Patrick W H 1979 Nitrogen fixation in flooded soil. Soil Sci. 128, 80–85.Google Scholar
  77. Rice W A 1979 Influence of the nitrogen content of straw amendments on nitrogenase activity in waterlogged soil. Soil Biol. Biochem. 11, 187–191.Google Scholar
  78. Rice W A and Paul E A 1972 The organisms and biological process involved in asymbiotic nitrogen fixation in waterlogged soil amended with straw. Can J. Microbiol. 18, 715–723.Google Scholar
  79. Rice W A, Paul E A and Wetter L R 1967 The role of anaerobiosis in asymbiotic nitrogen fixation. Can. J. Microbiol. 13, 829–836.Google Scholar
  80. Richardson A E, Connell L R, Halsall D M, Gibson A H and Watson J M 1991 Towards the development of cellulolytic diazotrophs. In Proceedings of the 9th Australian Nitrogen Fixation Conference, Australian National University, Canberra, January 1991. Eds. A E Richardson and M B Peoples. pp 11–12. Australian Soc. for Nitrogen Fixation.Google Scholar
  81. Roger P A and Kulasooriya S A 1980 Blue-green algae and rice. International Rice Research Institute, Manila. 112p.Google Scholar
  82. Roger P A and Watanabe I 1986 Technologies for utilizing biological nitrogen fixation in wetland rice: potentialities, current usage, and limiting factors. Fert. Res. 9, 39–77.Google Scholar
  83. Roper M M 1983 Field measurements of nitrogenase activity in soils amended with wheat straw. Aust. J. Agric. Res. 34, 725–739.Google Scholar
  84. Roper M M 1985 Straw decomposition and nitrogenase activity (C2H2 reduction): effects of soil moisture and temperature. Soil Biol. Biochem. 17, 65–71.Google Scholar
  85. Roper M M, Gault R R and Smith N A 1994b Contribution to the nitrogen status of soil by free-living nitrogen-fixing bacteria in a lucerne stand. Soil Biol. Biochem. (In press).Google Scholar
  86. Roper M M and Halsall D M 1986 Use of products of straw decomposition by N2-fixing (C2H2-reducing) populations of bacteria in three soils from wheat-growing areas. Aust. J. Agric. Res. 37, 1–9.Google Scholar
  87. Roper M M, Marschke G W and Smith N A 1989 Nitrogenase activity (C2H2 reduction) in soils following wheat straw retention: effects of straw management. Aust. J. Agric. Res. 40, 241–253.Google Scholar
  88. Roper M M and Smith N A 1991 Straw decomposition and nitrogenase activity (C2H2 reduction) by free-living microorganisms from soil: effects of pH and clay content. Soil Biol. Biochem. 23, 275–283.Google Scholar
  89. Roper M M, Turpin J A and Thompson J P 1994a Nitrogenase activity (C2H2 reduction) by free-living bacteria in soil in a longterm tillage and stubble management experiment on a vertisol. Soil Biol. Biochem. 26, 1087–1091.Google Scholar
  90. Sain P and Broadbent F E 1977 Decomposition of rice straw in soils as affected by some management factors. J. Environ. Qual. 6, 96–100.Google Scholar
  91. Saito M, Wada H and Takai Y 1977a Microbial ecology of cellulose decomposition in paddy soils. I. Modification of Tribe's cellophane film method and staining methods for the observation of microorganisms growing on cellulose material. Nippon Dojohiryo Gaku Zasshi 48, 313–317 (In Japanese).Google Scholar
  92. Saito M, Wada H and Takai Y 1977b Microbial ecology of cellulose decomposition in paddy soils. II. Succession of microorganisms growing on cellulose material. Nippon Dojohiryo Gaku Zasshi 48, 318–322 (In Japanese).Google Scholar
  93. Santiago-Ventura T, Bravo M, Daez C, Ventura V, Watanabe I and App A A 1986 Effects of N-fertilizers, straw and dry fallow on the nitrogen balance of a flooded soil planted with rice. Plant and Soil 93, 405–411.Google Scholar
  94. Shintani Y 1987 Effect of nitrite on growth and anaerobic nitrogen fixation in Bacillus polymyxa. J. Gen. Appl. Microbiol. 33, 93–97.Google Scholar
  95. Smith J H and Peckenpaugh R E 1986 Straw decomposition in irrigated soil: comparison of twenty-three cereal straws. Soil Sci. Soc. Am J. 50, 928–932.Google Scholar
  96. Sorensen L H 1974 Rate of decomposition of organic matter in soil as influenced by repeated air drying-rewetting and repeated additions of organic material. Soil Biol. Biochem. 6, 287–292.Google Scholar
  97. Staley J T (Ed.) 1989 Bergey's Manual of Systematic Bacteriology. Vol. 3. Williams and Wilkins, Baltimore.Google Scholar
  98. Stanier R, Doudoroff M and Adelberg E A 1974 General Microbiology. MacMillan, India. 873p.Google Scholar
  99. Stewart W D P 1980 Systems involving blue-green algae (cyanobacteria). In Methods for Evaluating Biological Nitrogen Fixation. Ed. F J Bergersen. pp 583–635. John Wiley and Sons, Chichester.Google Scholar
  100. Stotzky G 1972 Activity, ecology, and population dynamics of microorganisms in soil. CRC Crit. Rev. Microbiol. 2, 59–137.Google Scholar
  101. Subba Rao N S 1982 Utilization of farm wastes and residues in agriculture. In Advances in Agricultural Microbiology. Ed. N S Subba Rao. pp 509–521. Oxford and IBH Publishing Co., New Delhi.Google Scholar
  102. Summerell B A and Burgess L W 1989 Decomposition and chemical composition of cereal straw. Soil Biol. Biochem. 21, 551–559.Google Scholar
  103. Swift M J 1982 Microbial succession during the decomposition of organic matter. In Experimental Microbial Ecology. Eds. R G Burns and J H Slater. pp 164–177. Blackwell Scientific Publications, Oxford, UK.Google Scholar
  104. Theander O and Åman P 1978 Chemical composition of some Swedish cereal straws. Swedish J. Agric. Res. 8, 189–194.Google Scholar
  105. Theander O and Åman P 1984 Anatomical and chemical characteristics. In Straw and Other Fibrous By-products as Feed. Eds. F Sundstol and O Owen. pp 45–78. Elsevier Publishers, Amsterdam.Google Scholar
  106. Veal D A and Lynch J M 1984 Biochemistry of cellulose breakdown by mixed cultures. Biochem. Soc. Trans. Vol: 1142–1144.Google Scholar
  107. Vostrov I S and Dolgikh Y R 1970 Microflora of submerged soils of the rice field. Izv. Akad. Naukkaz. SSR Ser. Biol. 1, 64–69 (In Russian).Google Scholar
  108. Waksman S A and Gerretsen F C 1931 Influence of temperature and moisture upon the nature and extent of decomposition of plant residues by microorganisms. Ecology 12, 33–60.Google Scholar
  109. Wada H, Panichsakpatana S, Kimura M and Takai Y 1979 Organic debris as micro-site for nitrogen fixation. Soil Sci. Plant Nutr. 25, 453–456.Google Scholar
  110. Watanabe I 1984 Anaerobic decomposition of organic matter in flooded rice soils. In Organic Matter and Rice. pp 237–258. International Rice Research Institute, Manila.Google Scholar
  111. Watanabe I and Furusaka C 1980 Microbial ecology of flooded rice soils. Adv. Microbiol. Ecol. 4, 125–168.Google Scholar
  112. Watanabe I, Lee K K and Alimagno B V 1978 Seasonal change of N2-fixing rate in rice field assayed by in situ acetylene reduction technique. I. Experiments in long-term fertility plots. Soil Sci. Plant Nutr. 24, 1–13.Google Scholar
  113. Waterbury J B, Calloway C B and Turner R D 1983 A cellulolytic nitrogen-fixing bacterium cultured from the gland of deshayes in shipworms (Bivalvia: Teredinidae). Science 221, 1401–1403.Google Scholar
  114. Yadav K S and Subba Rao N S 1980 Use of cellulolytic microorganisms in composting. In Recycling Residues of Agriculture and Industry. Proceedings of a Symposium at the Punjab Agricultural University. Ed. M S Kalra. pp 267–273. Ludhiana, India.Google Scholar
  115. Yoneyama T, Lee K K and Yoshida T 1977 Decomposition of rice residues in tropical soils. IV. The effect of rice straw on nitrogen fixation by heterotrophic bacteria in some Philippine soils. Soil Sci. Plant Nutr. 23, 287–295.Google Scholar
  116. Yoo I D, Wada H and Takai Y 1982 Paddy Nitrogen. VII. Effects of rice straw application on N2 fixation in paddy fields with special reference to phototrophic N2 fixers on surface-placed rice straw. In International Seminar on Productivity of Soil Ecosystems. pp 243–248. Nodai Research Institute, Tokyo Univ. Agric.Google Scholar
  117. Yoshida T 1975 Microbial metabolism of flooded soils. In Soil Biochemistry, Vol 3. Eds. E A Paul and A D McLaren. pp 83–122. Marcel Dekker Inc., New York.Google Scholar
  118. Zeikus J G 1981 Lignin metabolism and the carbon cycle. Polymer biosynthesis, biodegradation, and environmental recalcitrance. Adv. Microbiol. Ecol. 5, 211–243.Google Scholar
  119. Zielinski J 1980 The effect of nitrogen content on the rate of organic matter decomposition. Pol. Ecol. Stud. 6, 167–182.Google Scholar

Copyright information

© Kluwer Academic Publishers 1995

Authors and Affiliations

  • Margaret M. Roper
    • 1
    • 2
  • J. K. Ladha
    • 1
    • 2
  1. 1.CSIRO Centre for Mediterranean Agricultural ResearchWembley
  2. 2.International Rice Research InstituteManilaPhilippines

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