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Significance and Improvement of Rhizospheric N2 Fixation

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Significance and Improvement of Rhizospheric N2 Fixation H.G. Diem and Y.R. Dommergues CNRS!ORSTOM. Dakar, Slnégal 7 Significance and Improvement of Rhizospheric N2Fixation Introduction N: fixation in the rhizosphere of grasses and non-leguminous crops was indicat.ed some time ago (Parker 1957). The first undisputable report on this I process was thar of Hassouna 6r Weireing (1964) who found active N2 fixa- tion in the rhizosphereof ilmnlophila arenaria, which they attributed to Azoto- bacter associated with roots. The introduction of the acetylene reduction technique by the end of the sixties, facilitated investigations-of whatis known as loosetype of symbiosis, -termed“associative symbiosis” by Burns gi Hardy (1975). The present review is an attempt to summarize the enormous volume of research carried out in thisfield during the lastdecade. Populations of N2 fixing bacteria in the rhizosphere MethodologJj Enumeration techniques: Untilrecent years, themost common method used to estimate populations of N2 fixing bacteria (Syn. diazotrophs) in soil was the spreading a soil suspension on a nitrogen-free silica gel medium and counting the colonies. Plates were incubated under aerobic conditions for counting Azotobacter or Beijerinckia andunder anaerobic conditions for ’ counting Clostridium andother anaerobic bacteria. Alternatively, theusual pour plate technique was also used by mixing soil suspensions with an agar medium cooled to 4045°C. These techniques were then modified by Fengle-- rova (1965) who, instead of silica gel plates, used a thin layer of soft agar to enhancethe developmentof Azotobacter. Otherauthors used extinction I90 Significance and Improvement of Rhizospheric NZFixation 191 .. l dilution technique by which the most probable number (MPN) of N2 fixing bacteria could be estimated. This procedure was considered by Abd-el-Malek i & Ishac (1965) as more sensitive than the plating method.' I The MPN method has also been used forestimating Clostridium popula- tion. In this case, the reading of positive tubes is facilitated by the addition of phenosafranine tp the medium (Brouzes et al., 1971; Balandreau. et al., 1975). The extinction dilution technique combined with the acetylene reduction test is now used to estimate the total NZfixing microflora (Villemin et al., 1975; Diem et'al., 197th) or Spirillum populations colonizing peanut toots (Okon et al., 1977). This technique may be combined with the use of Pank- hurst tubes (Campbell Sc .Evans, 1969) to assess the number of facultative and anaerobic nitrogen fixing bacteria. f Spirillum lipoferurn andother microaerophilicbacteria may now be easily. isolated by introducing soil suspensions or root pieces in a soft agar medium where micro-aerophilic bacteria grow at depths characterized by PO-7 most suitable for individual species. This original method first devised by Dober- einer & Day (1976) was based on the fact that most N2 fixing bacteria are P sensitive to oxygen (Dobereiner et al., 1976). In order to separate different NZ.fixing bacteria From mixed population, Rinaudo (personal cornmunica- 2pr was tion) incubated streaked plates in desiccator under anaerobic or microaero- on this . philicconditions. N?tixa- The advent of thefluorescent antibody (FA) technique as a tool forecolo- -lAIoro- gical studiesallowed DeVille & Tchan (1970) to estimate Azotobacter duction populations in natural soil. Using this method, Diem er al. (197Yb) were able known to count Beijerinckia ceils (cells count technique) in the midst of spermo- ums & & sphereor rhizospheremicroflora. When theplating procedure was used, ormous colonies of a given bacteria were assessed by Unger Sr Wagner'smethod. (1965) which consisted of staining impressed enumeration plates with Ruores- cent labelled antiserum. Immunofluorescence techniques (Schmidt 1973, 1974, 1975) especially the F.4-membrane fìlter counting method allows quaniificatbn of a speciiic mi- . croorganism Nitrobarter at densities as low as lv-103 per gram of soil in the method midst of a complete mixed microbial population (Rennie Sr Schmidt, 1977). 1 in soil Enumeration of colonies grown on a membrane tilter previously placed on the um and surface of an appropriate medium was alsorecommended by Hegazi 8 ons <or Niemela (1976) For routine quantitative estimation OF rlzorobacier. ons fa Working with an isolate of Beijrrinckia artificially introduced into non- e usual sterile soil, Diem (not published) was also able ta calculate the MPN of rtie ;In asar bacteria at a level IWcell/g by using an enrichment culture technique coupi- Fengle- rd with FA staining (Fig. 1). agar X Microscopic obsemations: Many modern methods, inclutiins transmission iincrim and scanning electron microscopy, are now widely used to observe the esta- blishment and the behaviour of microorganisms in the root re~on.As far as H'e irnOK,' 1 germinatior natural rnir (1976) snow lings by soi which deve! plate conta periment a ernbedied 1 vation. By were able t ments of tt ! Other 17 .saprophyre Modern re' Fig. 1. Fluorescing colonies of Beijerinckia sp. mixed with non fiuorwcing mine micrc cells of unidentified soil bacteria (arrowj afrer srainins with fiuorescent besides the antibodies against Beijerinckio sp. 1976), stair 1977) or fi (Benbough exernpliñec habitats (V biotic mis auxotroph- Suroe!. of t Qualitc presumed high poter Spirillacea Bacteri mobacteri~ 1961; Koc bacteria hi 1977). There i ture on N inhabitant which'car The abilit: been conc Fig. 2. Root system of rice seedlings embedded in dried agar pellicle to assimili after removal from the plastic plate. rer species Significance and Improvement of Rhizospheric NZFixation 193 we know, Jackson & Brown (1966) first used the FA technique to follow the germination of Azotobacter encysted cells and the growth of the bacterium in natural rhizosphere conditions. Using qelectron microscope, Hamad-Fares (1976) showed extensive colonization of the root surface of axenic-rice seed- lings by some N2fixing bacteria. Diem et al. (197Sb) proposed a method in which developing roots grew on an agar layer poured on a plastic plate. The plate containing the soil was placed at an angle of 45”. At the end of the ex- periment and after drying, the agar pellicle on which the plant roots were f T embeddedcould be easily removed(Fig. 1) andstained for microscopicobser- vation. By using this method in conjunction with FA stairling, these authors were able to observe the behaviour of Beijerinckia sp. in different compart- ments of the rice seedling rhizosphere. Other methods to be explored: General methods devised for studying soil saprophytes can also be used to investigate the ecology of N2 fixing bacteria. Modern techniques have been developed recently (Rosswall, 1973). To exa- acing . mine microbial competition and estimate the number-of soil microorganisms cent besides the use of such methods as electron microscopy (Foster & Rovira, I 1976), staining with a fluorescentbrightener (Trolldenier, 1973; Soderstrom .. 1977) or fluorescent antibodies(Schmidt, 1973) or radio-labelledantibodies (Benbough & Martin, 1976), there are a number of attractive techniques as exemplified by auto-radiography to detect active microbial cells in natural habitats (Waid er al., 1973; Fliermans Sr Schmidt, 1975) and the use of anti- biotic resistant mutants (Obaton, 1971; Schwinghamer Sr Dudman, 1973) or auxotrophic markers (Johnston & Beringer, 1975). Survey of the microorganism Qualitdue distribution: From the data regularly reporteá, it may be presumed that NZfixing bacteria are widely distributed taxonomically, but high potentials of NZfixation seem to belong to species of Azotobacteriaceae, *! Spirillaceae and, io some extent, Enterobacteriaceae and Bacillaceae. Bacteria of widespread families such as Pseudomonadaceae and Achro- mobacteriaceae are also sporadicallyrecorded to Lx NZ (Paul & Newton, 1961; Koch & Oya, 1974). Further details on the taxonomy of NZhing .. bacteria have already been reviewed (Postgate, 1971; Knowles, 1977: Stewart, 1977). 4 There are somemain considerationswhich emerge from a review of litera- ture on NZfixing bacteria: Some of the N?fixers recorded are not true root inhabitants. The best known exampie is that of some ‘gzoiobacrer species which cannot be definitively consideredas rhizosphere microorganisms. The ability ro fix N?by the so-called N2fixing microorganisms has not always been conclusively demonstrated. Some Arthobacter were claimed to be able to assimilate N?(Cacciari Sr Lippi, 1973). However, a number of drthroiiuc- rer species have been tested by lMulder Sr Brotonegoro (1974) and founa Got p:. ;y. l$,.> I94 Recent Advances in Biological hrìrrogen Fixation to possessany hi1 fixing ability.Reoently, interest has been devoted to' (Dobzreiner E Íacultrrtive anaerobic or microaerophiiic N2fixers such as Spiriliun1 (= Azospi- i (Evans et ai., rillurn) lipoferum, Bacillus polymyxa, B. macerans, Enterobacrer cloocae, E. zospheres, as I nerogenes and somespecies of Klebsielfo. Surprisingly, little attention has been i ' of loose specii paid in the past to obligate anaerobic N2 fixing bacteria in the rhizosphere A certain : although they may be abundant in.soi1 and well-adapted to a wide variety of kneous and a edaphic conditions (Katznelson er al., 1948). Rinaudo (1970) suggested that j some varieries KZfixation in rice soils was partly due to Clostridium. This is plausible since association De .. warerlogging in paddy soils increased the number of ailaerobic. sites at least of wheai was in the outer rhizosphere where OZexcreted by roots cannot diffuse. Anaero- of the
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