Stoichiometry constrains microbial response to root exudation- insights from a model and a field experiment in a temperate forest

By J. Drake, B. Darby, M. Giasson, Mark A. Kramer, Richard P Phillips, A. Finzi. 2012

247 citations recorded by the source corpus.

Plant roots release a wide range of chemicals into soils. This process, termed root exudation, is thought to increase the activity of microbes and the exoenzymes they synthesize, leading to accelerated rates of carbon (C) mineralization and nutrient cycling in rhizosphere soils relative to bulk soils. The nitrogen (N) content of microbial biomass and exoenzymes may introduce a stoichiometric constraint on the ability of microbes to effectively utilize the root exudates, particularly if the exudates are rich in C but low in N. We combined a theoretical model of microbial activity with an exudation experiment to test the hypothesis that the ability of soil microbes to utilize root exudates for the synthesis of additional biomass and exoenzymes is constrained by N availability. The field experiment simulated exudation by automatically pumping solutions of chemicals often found in root exudates ("exudate mimics") containing C alone or C in combination with N (C : N ratio of 10) through microlysimeter "root simulators" into intact forest soils in two 50-day experiments. The delivery of C-only exudate mimics increased microbial respiration but had no effect on microbial biomass or exoenzyme activities. By contrast, experimental delivery of exudate mimics containing both C and N significantly increased microbial respiration, microbial biomass, and the activity of exoenzymes that decompose low molecular weight components of soil organic matter (SOM, e.g., cellulose, amino sugars), while decreasing the activity of exoenzymes that degrade high molecular weight SOM (e.g., polyphenols, lignin). The modeling results were consistent with the experiments; simulated delivery of C-only exudates induced microbial N-limitation, which constrained the synthesis of microbial biomass and exoenzymes. Exuding N as well as C alleviated this stoichiometric constraint in the model, allowing for increased exoenzyme production, the priming of decomposition, and a net release of N from SOM (i.e., mineralization). The quantity of N released from SOM in the model simulations was, under most circumstances, in excess of the N in the exudate pulse, suggesting that the exudation of N-containing compounds can be a viable strategy for plant-N acquisition via a priming effect. The experimental and modeling results were consistent with our hypothesis that N-containing compounds in root exudates affect rhizosphere processes by providing substrates for the synthesis of N-rich microbial biomass and exoenzymes. This study suggests that exudate stoichiometry is an important and underappreciated driver of microbial activity in rhizosphere soils.

Subfields: Plant Science, Soil Science

View Paper: https://www.semanticscholar.org/paper/c673596bd864c9bae22e8d8d90286fa214ede9d9

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Citations in the corpus

Extracellular enzymes in terrestrial, freshwater, and marine environments: perspectives on system variability and common research needs (2013, background): “As a result, root carbon inputs to the soil are increasingly investigated as a driver of microbial nutrient acquisition and enzyme production (Drake et al. 2013).”
Stoichiometric imbalances between terrestrial decomposer communities and their resources: mechanisms and implications of microbial adaptations to their resources (2014, methodology): “This manuscript is an outcome of the MICDIF integrated project (Linking microbial diversity and function across scales and ecosystems) funded by the Austrian Science Fund FWF (S 10006-B01, S 10006-B06, S 10006-B07).”
Root-induced changes in nutrient cycling in forests depend on exudation rates (2014, unknown): “Recent exudation addition experiments indicate that rhizosphere priming may be greatest in soils that have a high ratio of labile-to-stable soil C owing to the presence of a larger microbial biomass (de Graaff et al., 2013), or in soils with a N economy dominated by organic N (Drake et al., 2013).”
Optimization of Indole Acetic Acid Production by Pseudomonas putida UB1 and its Effect as Plant Growth-Promoting Rhizobacteria on Mustard (Brassica nigra) (2013, unknown): “Microorganisms inhabiting rhizosphere of plants utilize the rich source of substrates from the roots and are expected to synthesize and release auxins as secondary metabolites [6, 11, 15, 34].”
Soil C and N availability determine the priming effect: microbial N mining and stoichiometric decomposition theories (2014, unknown): “, 2003), microbial activation (Drake et al., 2012), as well as preferential substrate utilization (Cheng, 1999) and competition for mineral nutrients (Cheng & Kuzyakov, 2005) in the rhizosphere.”
Soil extracellular enzyme activities correspond with abiotic factors more than fungal community composition (2013, background): “Indeed, we observed a significantly positive correlation between the relative abundance of arbuscular mycorrhizal fungi (AMF) and AG activity, which may be indicative of priming of saprotrophs by AMF (Cheng et al. 2012; Drake et al. 2012).”
Plant nitrogen uptake drives rhizosphere bacterial community assembly during plant growth (2015, background): “…reduction in soil nutrient availability increases C:N stoichiometry within the rhizosphere, which can initiate microbial extracellular enzyme production to oxidize or hydrolyze soil organic matter to release otherwise unavailable nutrients (Allison et al., 2007; Kuzyakov, 2010; Drake et al., 2013).”
Rhizosphere priming: a nutrient perspective (2013, background): “In modeling and field experiments Drake et al. (2013), simulated exudates and showed that adding C alone enhanced SOM decomposition, but adding C and N together stimulated SOM decomposition and N mineralization significantly more than C alone.”
Contribution of exudates, arbuscular mycorrhizal fungi and litter depositions to the rhizosphere priming effect induced by grassland species (2015, background): “This has led to studies to better understand the magnitude, controls and direction of rhizosphere processes over soil organic matter (SOM) dynamics (Dijkstra et al., 2006a,b; Dijkstra and Cheng, 2007; Cheng et al., 2013; Dijkstra et al., 2013; Drake et al., 2013).”
Root exudates increase N availability by stimulating microbial turnover of fast-cycling N pools (2017, unknown): “…provide strong evidence of links between root-derived C and N-cycling, logy, University of G€ottingen, (I.C. Meier), afinzi@bu.edu the mechanisms that drive these dynamics are poorly understood owing to challenges of experimentallymanipulating exudate inputs in situ (but see Drake et al., 2013a).”