Transformation and mineralization of nitrogenous soil components in the gut of soil-feeding termites

This thesis consists of several studies that focused on the role of soil-feeding termites and termite gut microbiota in the transformation and mineralization of nitrogenous soil components. The results can be summarized into four subject matters, namely: 1. N mineralization and transformation du...

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Bibliographic Details
Main Author: Ngugi, David Kamanda
Contributors: Brune, Andreas (Prof. Dr.) (Thesis advisor)
Format: Dissertation
Language:English
Published: Philipps-Universität Marburg 2008
Biologie
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Summary:This thesis consists of several studies that focused on the role of soil-feeding termites and termite gut microbiota in the transformation and mineralization of nitrogenous soil components. The results can be summarized into four subject matters, namely: 1. N mineralization and transformation during soil gut passage In order to better understand the role of soil-feeding termites in the dynamics of N in tropical soils, soil microcosms that received 15N tracers were incubated with termites. Here, our results demonstrated the importance of nitrogenous soil components (peptides) in the diet of soilfeeding termites, providing close to 50% of the termite’s carbon flux. The mineralization process, also results in the formation of enormous amounts of ammonia both in the gut (~150 mM) and the nest material. Additionally, we provided the first evidence for a termite-associated nitrification activity during the feeding activities of termites, which is coupled to denitrification and dissimilatory nitrate reduction to ammonia. At the ecosystem level, soil-feeding termites are estimated to contribute more towards N retention than to N loss in tropical soils. 2. Roles of termite gut microbiota in peptide breakdown and amino acids turnover Using gut homogenates, our studies revealed that termite gut microbiota play major roles in the hydrolysis and mineralization of peptidic components of soil organic matter. Both proteolytic and lysozyme activities were associated with termite tissues (i.e., salivary glands) and also the particulate fraction of the gut content. Together with the high alkalinity of the gut, soil peptides and microbial biomass are sequentially subjected to hydrolysis, solubilization, and extraction in the intestinal tract. Amino acids, which accumulate, are either directly absorbed by the insect or turned over by the dense hindgut microbiota, preferably by anaerobic amino-acid-fermenting bacteria. This underscores theimportant role of termite gut microbiota and the in situ physiological gut conditions, in enhancing the mineralization and utilization of peptidic components of soil organic matter by the termite. 3. Intestinal nitrate reduction leads to N2O and N2 emission Nitrate, a product of the nitrification activities in the gut, is reduced by the intestinal microbiota either to N2O and N2, or to ammonia. The reduction of nitrate to ammonia takes place mainly in the anterior gut region whereas denitrification occurs in the posterior hindgut. Virtually, no nitrate-reducing activities were present in the alkaline gut sections. Living termites emit both N2O and N2, but the emission of N2 rather than N2O seems to be the prevalent nitrogenous gas produced by soil-feeding termites. Nitrate reduction via denitrification represents ~26% of the total electrons flowing through methanogenesis in the intestinal tracts of soil-feeding termites. This study documents the first report on intestinal nitrate reduction to N2 and also provides the first evidence of soilfeeding termites as a source of the greenhouse gas N2O. 4. Excretion of ammonia via an “acid-trap” mechanism Soil-feeding termites preferentially utilize the peptidic components of soil organic matter. Consequently, ammonia levels in the hemolymph (~300 μM) and in the gut fluid accumulate to enormous concentrations. Using 15N tracers, we demonstrate that the alkalinity of the gut plays an important role removing ammonia by volatilizing NH4 + to NH3, which then diffuses into the hemolymph. Subsequently, NH3 is entrapped in the posterior hindgut with a circumneutral pH, most likely via an active transport mechanism. Finally, ammonia is egested through feces into the nest material. Also, preliminary evidence alludes to the role of Malpighian tubules in the excretion of ammonia as uric acid, a hitherto unknown function in soil-feeding termites.
DOI:https://doi.org/10.17192/z2008.0780