Soilborne disease suppressiveness / conduciveness : analysis of microbial community dynamics

Thesis (M.Sc. (Microbiology))--North-West University, Potchefstroom Campus, 2004.

Take-all is the name given to the disease caused by a soilborne fungus Gaeumannomyces graminis (Sacc.) von Arx and Olivier var. tritici Walker (Ggt), an ascomycete of the family Magnaportheaceae (Cook, 2003). This fungus is an aggressive soil-borne pathogen causing root rot of wheat (primary host), barley and rye crops (secondary host). The flowering, seedling, and vegetative growth stages can be affected by the infection of the whole plant, leaves, roots, and stems. Infections of roots result in losses in crop yield and quality primarily due to a lowering in nutrient uptake. Take-all is most common in regions where wheat is cultivated without adequate crop rotation. Crop rotation allows time between the planting dates of susceptible crops, which causes a decrease in the inoculum potential of soilborne plant pathogens to levels below an economic threshold by resident antagonistic soil microbial communities. Soilborne disease suppressiveness is an inherent characteristic of the physical, chemical, and/or biological structure of a particular soil which might be induced by agricultural practices and activities such as the cultivation of crops, or the addition of organisms or nutritional amendments, causing a change in the microfloral environment. Disturbances of soil ecosystems that impact on the normal functioning of microbial communities are potentially detrimental to soil formation, energy transfers, nutrient cycling, and long-term stability. In this regard, an overview of soil properties and processes indicated that the use of microbiological and biochemical soil properties, such as microbial biomass, the analysis of microbial functional diversity and microbial structural diversity by the quantification of community level physiological profiles and signature lipid biomarkers are useful as indicators of soil ecological stress or restoration properties because they are more responsive to small changes than physical and chemical characteristics. In this study, the relationship between physico-chemical characteristics, and different biological indicators of soil quality of agricultural soils conducive, suppressive, and neutral with respect to take-all disease of wheat as caused by the soilborne fungus Gaeumannomyces graminis var. tritici (Ggt), were investigated using various techniques. The effect of crop rotation on the functional and structural diversity of soils conducive to take-all disease was also investigated. Through the integration of quantitative and qualitative biological data as well as the physico-chemical characteristics of the various soils, the functional and structural diversity of microbial communities in the soils during different stadia of take-all disease of wheat were characterised. All results were evaluated statistically and the predominant physical and chemical characteristics that influenced the microbiological and biochemical properties of the agricultural soils during different stadia of take-all disease of wheat were identified using multivariate analyses. Although no significant difference @ > 0.05) could be observed between the various soils using conventional microbiological enumeration techniques, the incidence of Gliocladium spp. in suppressive soils was increased. Significant differences @ < 0.05) were observed between agricultural soils during different stadia of take-all disease of wheat. Although no clear distinction could be made between soils suppressive and neutral to take-all disease of wheat, soils suppressive and conducive to take-all disease of wheat differed substantially in their community level physiological profiles (CLPPs). Soils suppressive / neutral to take-all disease were characterised by enhanced utilisation of carboxylic acids, amino acids, and carbohydrates, while conducive soils were characterised by enhanced utilisation of carbohydrates. Shifts in the functional diversity of the associated microbial communities were possibly caused by the presence of Ggt and associated antagonistic fungal and bacterial populations in the various soils. It was evident that the relationships amongst the functionality of the microbial communities within the various soils had undergone changes through the different stages of development of take-all disease of wheat, thus implying different substrate utilisation capabilities of present soil microbial communities. Diversity indices were calculated as Shannon's diversity index (H') and substrate equitability (J) and were overall within the higher diversity range of 3.6 and 0.8, respectively, indicating the achievement of very high substrate diversity values in the various soils. A substantial percentage of the carbon sources were utilised, which contributed to the very high Shannon-Weaver substrate utilisation indices. Obtained substrate evenness (equitability) (J) indices indicated an existing high functional diversity. The functional diversity as observed during crop rotation, differed significantly (p < 0.05) from each other, implying different substrate utilisation capabilities of present soil microbial communities, which could possibly be ascribed to the excretion of root exudates by sunflowers and soybeans. Using the Sorenson's index, a clear distinction could be made between the degrees of substrate utilisation between microbial populations in soils conducive, suppressive, and neutral to take-all disease of wheat, as well as during crop rotation. Furthermore, the various soils could also be differentiated on the basis of the microbial community structure as determined by phospholipid fatty acid (PLFA) analysis. Soil suppressive to take-all disease of wheat differed significantly (p < 0.05) from soils conducive, and neutral to take-all disease of wheat, implying a shift in relationships amongst the structural diversity of microbial communities within the various soils. A positive association was observed between the microbial phospholipid fatty acid profiles, and dominant environmental variables of soils conducive, suppressive, and neutral to take-all disease of wheat. Soils conducive and neutral to take-all disease of wheat were characterised by high concentrations of manganese, as well as elevated concentrations of monounsaturated fatty acids, terminally branched saturated fatty acids, and polyunsaturated fatty acids which were indicative of Gram-negative bacteria, Gram-positive bacteria and micro eukaryotes (primarily fungi), respectively. These soils were also characterised by low concentrations of phosphorous, potassium, percentage organic carbon, and percentage organic nitrogen, as well as low soil pH. Soil suppressive to take-all disease of wheat was characterised by the elevated levels of estimated of biomass and elevated concentrations of normal saturated fatty acids, which is ubiquitous to micro-organisms. The concentration of normal saturated fatty acids in suppressive soils is indicative of a low structural diversity. This soil was also characterised by high concentrations of phosphorous, potassium, percentage organic carbon, and percentage organic nitrogen, as well as elevated soil pH. The relationship between PLFAs and agricultural soils was investigated using principal component analysis (PCA), redundancy analysis (RDA) and discriminant analysis (DA). Soil suppressive to take-all disease of wheat differed significantly (p < 0.05) from soils conducive, and neutral to take-all disease of wheat, implying a shift in relationships amongst the structural diversity of microbial communities within the various soils. A positive association was observed between the microbial phospholipid fatty acid profiles, and dominant environmental variables of soils conducive, suppressive, and neutral to take-all disease of wheat. Hierarchical cluster analysis of the major phospholipid fatty acid groups indicated that the structural diversity differed significantly between soils conducive, suppressive, and neutral to take-all disease of wheat caused by Gaeumannomyces graminis var. tritici. The results indicate that the microbial community functionality as well as the microbial community structure was significantly influenced by the presence of take-all disease of wheat caused by Gaeumannomyces graminis var. tritici, and that the characterisation of microbial functional and structural diversity by analysis of community level physiological profiles and phospholipid fatty acid analysis, respectively, could be successfully used as an assessment criteria for the evaluation of agricultural soils conducive, suppressive, and neutral to take-all disease of wheat, as well as in crop rotation systems. This methodology might be of significant value in assisting in the management and evaluation of agricultural soils subject to the prevalence of other soilborne diseases.

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