Mycorrhization and Warming Modulate Soil Organic Matter Stability

Soil organic matter (SOM) is the primary source of plant-available nutrients, as well as a substantial carbon (C) reservoir in terrestrial ecosystems. Maintenance of SOM levels is therefore critical for ecosystem sustainability. SOM stocks mainly depend on the balance between uptake (by photosynthesis) and release (via SOM decomposition). Mycorrhizal colonization increases net photosynthesis within the host plant for 4-30%, thus stimulates microbial activity and accelerate or retard SOM decomposition, consequently leading to SOM destabilization and losses. Furthermore, this SOM destabilization is also depends strongly on temperature, which are predicted to rise by 1.0 to 4.8 °C at the end of twenty-first century, with high risk to activate microorganisms and accelerate their turnover, thus promoting terrestrial C cycle. Therefore, this thesis aims to evaluate the effects of mycorrhization and warming on SOM stability and its underlying microbial mechanisms. In Study 1, we used continuous 13CO2 labeling to quantify the C allocation and rhizosphere priming effect (RPE) of a mycorrhizal wild type progenitor and its mycorrhiza defective mutant (reduced mycorrhizal colonization) of tomato. Arbuscular mycorrhizal fungi (AMF) increased the net rhizodeposition by 25-72% in soils, and lowered the RPE on SOM decomposition by 24-38%. This indicated a higher potential for C sequestration by MYC plants because the reduced nutrient availability restricted the activity of free-living decomposers. The RPE and N-cycling enzyme activities decreased by N fertilization 8 and 12 weeks after transplanting, suggesting a lower microbial N demand from SOM mining. Based on the 13C profile of microbial phospholipid fatty acids (PLFAs) (Study 2), the 13C incorporation into fungal biomarker (PLFA and NLFA 16:1ω5c) increased with sampling time, indicated that AMF was prominent in the plant-soil system. The preferential C allocation to AMF was at the expense of C flow to other microbial groups, thus resulting in a lower 13C incorporation into bacteria and saprotrophic fungi. Even more, high N availability negatively impacted on AMF growth and further rhizodeposited C recovered in the AMF, which resulted from higher C immobilization in the aboveground and higher rhizosphere respiration. Overall, AMF facilitates soil C sequestration by retaining more plant rhizodeposits in soils and by reducing the RPE on SOM decomposition, which is mainly dependent on the N availability. Together with AMF, ectomycorrhizal fungi (ECM) are the two most widespread mycorrhizal types on Earth. Therefore, 14C imaging coupled with zymography was used to investigate the spatial distribution of rhizodeposite C and enzyme activities in response to ECM and another major soil fungal guilds in temperature forests- non-mycorrhizal rhizosphere fungi (NMRF) in Study 3. Plants inoculated with ECM and NMRF allocated more C to soils compared to uninoculated control. When NMRF is co-existence with ECM (MIX), ECM competed with NMRF and thus the growth of ECM was suppressed, as a consequence less assimilated C was allocated to the rhizohyphosphere for MIX compared to ECM. Furthermore, we observed 57% higher chitinase and 49% higher leucine-aminopeptidase in the rhizohyphosphere with ECM compared with the control, whereas NMRF showed a higher production of β-glucosidase. Therefore, Picea abies colonized with ECM and NMRF both induced an increased root exudation and promote enhanced enzyme activities, but ECM focused on nutrient mobilization, whereas NMRF presence stimulates enzymes of the C cycle. Besides rhizodeposits via mycorrhizal pathway, temperature is a another crucial factor enhancing soil microbial activity, and thus threatening SOM stability. Based on microbial and enzymatic functional traits under 8-year long-term warming agricultural field (Study 4), soil organic C (SOC) and total nitrogen (TN) remained stable at warming below 2 °C, while higher warming (by 2-4 °C) did not affect SOC but it increased TN content. Possible explanation of increased TN was linked to unbalanced process of necromass formation and enzymatic decomposition. 2-4 °C warming induced faster microbial growth and turnover, whereas it reduced catalytic efficiency and slowed down the enzyme-mediated turnover of oligosaccharides and polypeptides. Lower enzymatic efficiency and slower turnover of organic residues under 2-4 °C warming thus may cause accumulation of N-related necromass. Consequently, the responses of microbial functional traits to climate warming were dependent on warming magnitudes, above 2 °C warming would exceed a threshold that changes the predicted temperature effect on soil C and N pools in the future, which might in its feedback reaction rather a further future CO2 source feeding into the atmosphere globally Furthermore, the response of soil C cycle to climate warming is also dependent on the ecosystem types. Given that montane grasslands are expected to be exposed to intensive warming, the response of microbial functions may be different from agroecosystems. Therefore, intact plant-soil mesocosms were translocated downslope spanning a temperature increase of 7 °C (from 13, 15, 17 to 20 °C) in the European Alps (Study 5). Microbial community in lower elevation shifted toward to slow-growing K-strategists due to the decreased availability of C substrates. Further, the increase of C-degrading enzymes, accompanied by the decrease of substrate turnover time of β-glucosidase, implied a stronger microbial C turnover because of the C limitation in the lower versus higher elevation soils. This, in turn, presumably leads to potential C losses under climate warming due to the significantly increased C and nutrients cycling of montane grassland soils. Since enzymes are closely linked to SOM decomposition, knowledge on temperature sensitivity (Q10) of enzyme activities is required to predict the future soil C release to the atmosphere. Soil samples from eight-years warming field sites (ambient, +1.6 °C, +3.2 °C) were incubated at a short-term constant temperature (from 5 to 25 °C with 5 °C intervals) under microbial steady-state and activated mode (Study 6). We found a legacy effect of eight-year field warming which facilitated the consumption of labile organics due to faster microbial growth and turnover. Thus, it caused a lower Q10 of enzyme activities in warmed soils. Additional labile C inputs caused a higher Q10-Vmax in warmed versus ambient soil, which demonstrated a reduced microbial memory effect due to thermophilic nature of activated microorganisms. Consequently, the microbial memory is strongly dependent on microbial physiological state, which can be quickly altered by substrate supply. Overall, this thesis suggests that temperature effect on soil C and N pools are mainly dependent on warming magnitudes and ecosystem types. Specifically, if future climate warming beyond the aim of Paris Climate Agreement (> 2 ℃), it would accelerates SOM mineralization and threaten SOM stability. For example, is may induce a severe alteration of N cycle with several potential negative feedbacks-from unhealthy net primary productivity increase in natural ecosystems via groundwater NO3- accumulation up to increased N2O emission with feedback on related climate change. However, mycorrhizae is ubiquitous in terrestrial ecosystems because it can stimulate belowground C inputs and inhibit the growth of saprotrophic fungi, consequently facilitate soil C sequestration. Therefore, mycorrhization may act as a positive mitigation strategy buffer against the predicted increases in SOM decomposition in the future warmer world.2021-06-3