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University of Bayreuth (2016)

Adaptions of saprotrophic filamentous fungi to drought stress in soils : Hydraulic redistribution through mycelia networks and transcriptional responses

Guhr, Alexander

Titre : Adaptions of saprotrophic filamentous fungi to drought stress in soils : Hydraulic redistribution through mycelia networks and transcriptional responses

Auteur : Guhr, Alexander

Université de soutenance : University of Bayreuth,

Grade : Doctoral thesis, 2016

Résumé
The desiccation of upper soil horizons is a common phenomenon leading to a decrease in microbial activity. Recent studies have shown that fungal communities are often less sensitive and better adapted to soil desiccation than bacterial communities. Mechanisms behind this observation and general drought responses of filamentous saprotrophic fungi are only scarcely analysed. One reason for better fungal adaptation to desiccation may be hydraulic redistribution (HR) of water from moist to dry soil zones along water potential gradients by mycelia networks. The general goal of this thesis was to investigate the potential of saprotrophic fungi for HR in the non-differentiated mycelium of Agaricus bisporus and in the mycelial cord former Schizophyllum commune. In addition, the impact of HR on mineralisation of organic matter as well as N translocation within mycelia networks was determined. Further, this study aimed to analyse transcriptional and respiratory responses of A. bisporus exposed to drought stress and how they are impacted by the antioxidant riboflavin. Fungal potential for HR, in comparison to capillary transport, and the impact of HR on C mineralisation and N translocation were assessed in mesocosms using labelling experiments. The mesocosms consisted of 2 chambers, filled with sandy soil and separated by a 2 mm air gap to prevent bulk flow of water. After 6 weeks of growth, chambers were desiccated to a water potential of about -9.5 MPa. Afterwards, chamber I was rewetted to field capacity while chamber II remained dry. One set of mesocosms was rewetted with deuterium labelled water and soil from chamber II was sampled over 3 d and analysed for 2H abundance to quantify HR. A separate set of mesocosms was treated with labelled plant material in chamber II. In this case, CO2 samples were extracted over 7 d and analysed for 13C abundance to study the impact of HR on C mineralisation. Furthermore, enzyme activity on the soil surface of chamber II was analysed. N translocation was determined based on δ15N values in soil of chamber I after 7 d. Respiratory and transcriptional response of A. bisporus to drought stress and riboflavin were assessed in separate mesocosm experiments under drought or no drought conditions and with or without 50 µM riboflavin addition. Transcriptomic changes and hyphal riboflavin contents were assessed by high-density microarray hybridization and high performance liquid chromatography, respectively. A. bisporus and S. commune redistributed water at a flow velocity of about 0.3 and 0.43 cm min-1, respectively, per hyphae, resulting in a water potential increase of the bulk soil. The amount of transferred water was similar to capillary transport in sterile sandy soil. Fungal hyphae have the potential to overcome capillary barriers between dry and wet soil compartments via HR. HR seems to partly compensate water deficiency, if water is available in other zones of the mycelia network. And HR is likely a mechanism behind higher drought resistance of soil fungi compared to bacteria. Further, HR is an underrated pathway of water transport in soils and may lead to a transfer of water to zones of high fungal activity. While HR by A. bisporus strongly enhanced C mineralisation by 2800% and enzymatic activity by 250-350% in the dry soil compartment, HR by S. commune only slightly increased C mineralisation and enzyme activity within 7 d. In addition, S. commune translocated N towards the substrate for hyphal growth thereon, whereas A. bisporus translocated N within the mycelial network towards the wet soil. The impact of fungal HR on C mineralisation and N translocation in dry soils seems to be species specific and related to the resource usage strategy. The transcriptional response of A. bisporus to drought or riboflavin was mainly based on factors regulating transcription, translation and growth. This was even stronger in combined treatments. Further, riboflavin induced several protective mechanisms, methylglyoxal (cytotoxic byproduct of glycolysis) detoxifying lactoylglutathione lyase being most pronounced. Drought increased riboflavin content in hyphae about 5 times, with or without riboflavin addition. Without riboflavin addition, fungal respiration decreased by more than 50% at a water potential of about -20 MPa. Respiration remained about 2-3 times higher with riboflavin addition. These data indicate a stress priming function and a prominent role of riboflavin in drought responses of A. bisporus. In conclusion, saprotrophic fungi have the potential for HR. Yet, the impact of fungal HR on C mineralisation and N translocation in dry soils seems to be species specific. The relevance of HR on ecosystem scales may therefore strongly depend on fungal community structure. Drought stress seems to mainly trigger enhanced protein biosynthesis and growth in A. bisporus which may in turn stimulate network extension and water redistribution. Further, riboflavin supports drought tolerance in A. bisporus.

Mots clés  : saprotrophic filamentous fungi ; hydraulic redistribution ; carbon mineralisation ; drought stress ; differential gene expression

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Page publiée le 3 novembre 2017, mise à jour le 30 décembre 2018