Role of plant rhizosphere across multiple species, grassland management and temperature on microbial communities and long term soil organic matter dynamics

par Tanvir Shahzad

Thèse de doctorat en Ecologie, Biogéochimie, Agronomie

Sous la direction de Claire Chenu.

Le président du jury était Sylvie Recous.

Le jury était composé de Claire Chenu, Pierre Barré, Sébastien Fontaine.

Les rapporteurs étaient Evgenia Blagodatskaya, Sébastien Barot.


  • Résumé

    It is increasingly being recognized that the soil microbes can mineralize recalcitrant soil organic matter (SOM) by using the fresh carbon (C) as a source of energy, a process called priming effect (PE). It has been shown mostly in lab incubations that PE can have important consequences for sequestration of organic C in soils. However, the importance of PE in C and N dynamics of ecosystems remains little known. The soil-plant interactions and rhizospheric processes can modulate the rates of PE and its consequences on C and N dynamics in an ecosystem. The objective of this thesis was to determine the role of PE in the C and N dynamics of permanent grasslands and the modulation of this role in response to management (plant clipping, fertilization) and global warming. Moreover, it was aimed to identify the microbial groups involved in PE and to unravel the way, e.g. absorption of N, root exudations and litter deposition, by which plant can induce PE. The thesis was based on a new approach allowing continuous dual labelling of multiple grassland plants with 13C- and 14C-CO2. The dual labelling permitted the separation of soil-derived CO2 from plant-derived CO2, the calculation of PE and the determination of mean age of soil-derived CO2-C. Moreover, phospholipids fatty-acids analysis (PLFA) permitted to correlate the variation of PE with changes in microbial community composition. Our work showed that the increased SOM mineralization under grasses was consistently two to three times more than that in bare soils (i.e. PE) over long term (511 days). This reveals that the PE plays key role in ecosystem CO2-C flux and indicates that a very large pool of SOM is under the control of PE. Moreover, we report that 15,000 years old organic C from an undisturbed deep soil can be mineralized after the supply of fresh C by living plants to soil microbes. This result supports the idea that the SOM in deep soils is stable due to the energy-limitation of microbes and the ‘inert' pool of organic C defined in current models is not so ‘inert' finally. The supply of N in soil-plant system through the use of fertilizer or legume decreased the PE suggesting that the C storage in soils is limited by nutrient supply. Similarly, plant clipping reduced the plant N uptake thereby PE. Collectively these results suggest synchronization between plant N uptake and SOM mineralization supporting the idea that soils under permanent plant cover function as a bank of nutrients for the plant, maximizing plant productivity and nutrient retention. An innovative method clearly showed that the root exudation is the major way by which grassland plants induce PE. Moreover, saprophytic fungi are suggested as the key actors in the mineralization of recalcitrant SOM & PE. Lastly, we developed a new theory on temperature response of SOM mineralization by taking into account the energy-limitation of microbes and the temperature-dependent inactivation of enzymes. This theory predicts a negative relationship between temperature and mineralization of recalcitrant SOM, which was supported by experimental results. This finding challenges the classical paradigm of positive relationship between temperature and recalcitrant SOM mineralization. Overall, these investigations on plant-soil systems reinforce the idea that PE and underlying mechanisms play a key role in ecosystem C and N dynamics and even suggest that this role was underestimated in lab experiments.

  • Titre traduit

    Role of plant rhizosphere across multiple species, grassland management and temperature on microbial communities and long term soil organic matter dynamics


  • Résumé

    It is increasingly being recognized that the soil microbes can mineralize recalcitrant soil organic matter (SOM) by using the fresh carbon (C) as a source of energy, a process called priming effect (PE). It has been shown mostly in lab incubations that PE can have important consequences for sequestration of organic C in soils. However, the importance of PE in C and N dynamics of ecosystems remains little known. The soil-plant interactions and rhizospheric processes can modulate the rates of PE and its consequences on C and N dynamics in an ecosystem. The objective of this thesis was to determine the role of PE in the C and N dynamics of permanent grasslands and the modulation of this role in response to management (plant clipping, fertilization) and global warming. Moreover, it was aimed to identify the microbial groups involved in PE and to unravel the way, e.g. absorption of N, root exudations and litter deposition, by which plant can induce PE. The thesis was based on a new approach allowing continuous dual labelling of multiple grassland plants with 13C- and 14C-CO2. The dual labelling permitted the separation of soil-derived CO2 from plant-derived CO2, the calculation of PE and the determination of mean age of soil-derived CO2-C. Moreover, phospholipids fatty-acids analysis (PLFA) permitted to correlate the variation of PE with changes in microbial community composition. Our work showed that the increased SOM mineralization under grasses was consistently two to three times more than that in bare soils (i.e. PE) over long term (511 days). This reveals that the PE plays key role in ecosystem CO2-C flux and indicates that a very large pool of SOM is under the control of PE. Moreover, we report that 15,000 years old organic C from an undisturbed deep soil can be mineralized after the supply of fresh C by living plants to soil microbes. This result supports the idea that the SOM in deep soils is stable due to the energy-limitation of microbes and the ‘inert' pool of organic C defined in current models is not so ‘inert' finally. The supply of N in soil-plant system through the use of fertilizer or legume decreased the PE suggesting that the C storage in soils is limited by nutrient supply. Similarly, plant clipping reduced the plant N uptake thereby PE. Collectively these results suggest synchronization between plant N uptake and SOM mineralization supporting the idea that soils under permanent plant cover function as a bank of nutrients for the plant, maximizing plant productivity and nutrient retention. An innovative method clearly showed that the root exudation is the major way by which grassland plants induce PE. Moreover, saprophytic fungi are suggested as the key actors in the mineralization of recalcitrant SOM & PE. Lastly, we developed a new theory on temperature response of SOM mineralization by taking into account the energy-limitation of microbes and the temperature-dependent inactivation of enzymes. This theory predicts a negative relationship between temperature and mineralization of recalcitrant SOM, which was supported by experimental results. This finding challenges the classical paradigm of positive relationship between temperature and recalcitrant SOM mineralization. Overall, these investigations on plant-soil systems reinforce the idea that PE and underlying mechanisms play a key role in ecosystem C and N dynamics and even suggest that this role was underestimated in lab experiments.


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