Soil organic matter decomposition driven by microbial growth: A simple model for a complex network of interactions

Priming effects are expressions of complex interactions within soil microbial communities. Thus, we aimed at building a microbial population growth model which could deal with different substrates, resources and populations. Our model divides the decomposition/growth process at the population level in two stages, mimicking mechanisms taking place at molecular and cellular scales: (1) the first stage is a reversible process whereby microbial biomass capture their substrate to form a complex within definite proportions; (2) the second stage is the irreversible rate-limiting utilization of substrate per se. It is supposed to be a first order process with respect to the quantity of complex. We put these assumptions into equations using an analogy with chemical reactions at equilibrium. We show that this model (1) provides a mathematical formalism that bridges the gap between first order decay of substrates and Monod kinetics; (2) sets constraints on the possible combinations of microbial functional traits, yielding microbial strategies in agreement with observations; (3) allows to model both positive and negative priming effects, and more generally complex interactions between the various components of a soil system. This model is designed to be used as a kernel in any soil organic matter model.     

Priming effects: Interactions between living and dead organic matter

In this re-evaluation of our 10-year old paper on priming effects, I have considered the latest studies and tried to identify the most important needs for future research. Recent publications have shown that the increase or decrease in soil organic matter mineralization (measured as changes of CO₂ efflux and N mineralization) actually results from interactions between living (microbial biomass) and dead organic matter. The priming effect (PE) is not an artifact of incubation studies, as sometimes supposed, but is a natural process sequence in the rhizosphere and detritusphere that is induced by pulses or continuous inputs of fresh organics. The intensity of turnover processes in such hotspots is at least one order of magnitude higher than in the bulk soil. Various prerequisites for high-quality, informative PE studies are outlined: calculating the budget of labeled and total C; investigating the dynamics of released CO₂ and its sources; linking C and N dynamics with microbial biomass changes and enzyme activities; evaluating apparent and real PEs; and assessing PE sources as related to soil organic matter stabilization mechanisms. Different approaches for identifying priming, based on the assessment of more than two C sources in CO₂ and microbial biomass, are proposed and methodological and statistical uncertainties in PE estimation and approaches to eliminating them are discussed. Future studies should evaluate directions and magnitude of PEs according to expected climate and land-use changes and the increased rhizodeposition under elevated CO₂ as well as clarifying the ecological significance of PEs in natural and agricultural ecosystems. The conclusion is that PEs - the interactions between living and dead organic matter - should be incorporated in models of C and N dynamics, and that microbial biomass should regarded not only as a C pool but also as an active driver of C and N turnover.     

Moisture modulates rhizosphere effects on C decomposition in two different soil types

While it is well known that soil moisture directly affects microbial activity and soil organic matter (SOM) decomposition, it is unclear if the presence of plants alters these effects through rhizosphere processes. We studied soil moisture effects on SOM decomposition with and without sunflower and soybean. Plants were grown in two different soil types with soil moisture contents of 45% and 85% of field capacity in a greenhouse experiment. We continuously labeled plants with depleted ¹³C, which allowed us to separate plant-derived CO₂-C from original soil-derived CO₂-C in soil respiration measurements. We observed an overall increase in soil-derived CO₂-C efflux in the presence of plants (priming effect) in both soils. On average a greater priming effect was found in the high soil moisture treatment (up to 76% increase in soil-derived CO₂-C compared to control) than in the low soil moisture treatment (up to 52% increase). Greater plant-derived CO₂-C and plant biomass in the high soil moisture treatment contributed to greater priming effects, but priming effects remained significantly higher in the high moisture treatment than in the low moisture treatment after correcting for the effects of plant-derived CO₂-C and plant biomass. The response to soil moisture particularly occurred in the sandy loam soil by the end of the experiment. Possibly, production of root exudates increased with increased soil moisture content. Root exudation of labile C may also have become more effective in stimulating microbial decomposition in the higher soil moisture treatment and sandy loam soil. Our results indicate that moisture conditions significantly modulate rhizosphere effects on SOM decomposition.     

Model of apparent and real priming effects: Linking microbial activity with soil organic matter decomposition

The most frequently used models simulating soil organic matter (SOM) dynamics are based on first-order kinetics. These models fail to describe and predict such interactions as priming effects (PEs), which are short-term changes in SOM decomposition induced by easily available C or N sources. We hypothesized that if decomposition rate depends not only on size of the SOM pool, but also on microbial biomass and its activity, then PE can be simulated. A simple model that included these interactions and that consisted of three C pools - SOM, microbial biomass, and easily available C - was developed. The model was parameterized and evaluated using results of ¹²C-CO₂ and ¹⁴C-CO₂ efflux after adding ¹⁴C-labeled glucose to a loamy Haplic Luvisol. Experimentally measured PE, i.e., changes in SOM decomposition induced by glucose, was compared with simulated PE. The best agreement between measured and simulated CO₂ efflux was achieved by considering both the total amount of microbial biomass and its activity. Because it separately described microbial turnover and SOM decomposition, the model successfully simulated apparent and real PE.The proposed PE model was compared with three alternative approaches with similar complexity but lacking interactions between the pools and neglecting the activity of microbial biomass. The comparison showed that proposed new model best described typical PE dynamics in which the first peak of apparent PE lasted for 1 day and the subsequent real PE gradually increased during 60 days. This sequential decomposition scheme of the new model, with immediate microbial consumption only of soluble substrate, was superior to the parallel decomposition scheme with simultaneous microbial consumption of two substrates with different decomposability. Incorporating microbial activity function in the model improved the fit of simulation results with experimental data, by providing the flexibility necessary to properly describe PE dynamics. We conclude that microbial biomass should be considered in models of C and N dynamics in soil not only as a pool but also as an active driver of C and N turnover.     

Invertebrates increase the sensitivity of non-labile soil carbon to climate change

The fate of global soil carbon stores in response to predicted climate change is a ‘hotly’ debated topic. Considerable uncertainties remain as to the temperature sensitivity of non-labile soil organic matter (SOM) to decomposition. Currently, models assume that organic matter decomposition is solely controlled by the interaction between climatic conditions and soil mineral characteristics. Consequently, little attention has been paid to adaptive responses of soil decomposer organisms to climate change and their impacts on the turnover of long-standing terrestrial carbon reservoirs. Using a radiocarbon approach we found that warming increased soil invertebrate populations (Enchytraeid worms) leading to a greater turnover of older soil carbon pools. The implication of this finding is that until soil physiology and biology are meaningfully represented in ecosystem carbon models, predictions will underestimate soil carbon turnover.     

Plant biomass influences rhizosphere priming effects on soil organic matter decomposition in two differently managed soils

We used a continuous labeling method of naturally ¹³C-depleted CO₂ in a growth chamber to test for rhizosphere effects on soil organic matter (SOM) decomposition. Two C3 plant species, soybean (Glycine max) and sunflower (Helianthus annus), were grown in two previously differently managed soils, an organically farmed soil and a soil from an annual grassland. We maintained a constant atmospheric CO₂ concentration at 400±5 ppm and δ¹³C signature at −24.4‰ by regulating the flow of naturally ¹³C-depleted CO₂ and CO₂-free air into the growth chamber, which allowed us to separate new plant-derived CO₂-C from original soil-derived CO₂-C in soil respiration. Rhizosphere priming effects on SOM decomposition, i.e., differences in soil-derived CO₂-C between planted and non-planted treatments, were significantly different between the two soils, but not between the two plant species. Soil-derived CO₂-C efflux in the organically farmed soil increased up to 61% compared to the no-plant control, while the annual grassland soil showed a negligible increase (up to 5% increase), despite an overall larger efflux of soil-derived CO₂-C and total soil C content. Differences in rhizosphere priming effects on SOM decomposition between the two soils could be largely explained by differences in plant biomass, and in particular leaf biomass, explaining 49% and 74% of the variation in primed soil C among soils and plant species, respectively. Nitrogen uptake rates by soybean and sunflower was relatively high compared to soil C respiration and associated N mineralization, while inorganic N pools were significantly depleted in the organic farm soil by the end of the experiment. Despite relatively large increases in SOM decomposition caused by rhizosphere effects in the organic farm soil, the fast-growing soybean and sunflower plants gained little extra N from the increase in SOM decomposition caused by rhizosphere effects. We conclude that rhizosphere priming effects of annual plants on SOM decomposition are largely driven by plant biomass, especially in soils of high fertility that can sustain high plant productivity.     

易利用态有机物质对水稻土甲烷排放的激发作用

为探讨外源有机物质对淹水稻田土壤CH4排放的激发作用,对比不同外源有机物质对土壤CH4排放的贡献差别,本研究选取3种标记的易利用态有机物(葡萄糖、乙酸和草酸)分别加入水稻土,进行了为期1个月的培养。结果表明:培养30 d后不同处理CH4的累计排放量差异显著(P0.05),其中,乙酸葡萄糖草酸对照;双因素方差分析结果显示,外源有机物质的添加加速了土壤易利用态有机质的矿化(即产生正激发效应);不同处理条件下激发作用产生的CH4分别占各处理CH4总累计排放量的73.3%(葡萄糖处理)、71.5%(乙酸处理)和40.9%(草酸处理),且CH4排放量与CH4激发效应之间极显著正相关关系说明土壤CH4排放主要要来自于土壤原有机质的分解,外源有机物质可能主要对土壤微生物活性及代谢途径有影响。     

Sources and mechanisms of priming effect induced in two grassland soils amended with slurry and sugar

The mechanisms and specific sources of priming effects, i.e. short term changes of soil organic matter (SOM) decomposition after substance addition, are still not fully understood. These uncertainties are partly method related, i.e. until now only two C sources in released CO₂ could be identified. We used a novel approach separating three carbon (C) sources in CO₂ efflux from soil. The approach is based on combination of different substances originated from C₃ or C₄ plants in different treatments and identical transformation of substances like C₃ sugar (from sugar beet) and C₄ sugar (from sugar cane). We investigated the influence of the addition of two substances having different microbial utilizability, i.e. slurry and sugar on the SOM or/and slurry decomposition in two grassland soils with different levels of C_org (2.3 vs. 5.1% C). Application of slurry to the soil slightly accelerated the SOM decomposition. Addition of sugar lead to changes of SOM and slurry decomposition clearly characterized by two phases: immediately after sugar addition, the microorganisms switched from the decomposition of hardly utilizable SOM to the decomposition of easily utilizable sugar. This first phase was very short (2-3 days), hence was frequently missed in other experiments. The second phase showed a slightly increased slurry and SOM decomposition (compared to the soil without sugar). The separation of three sources in CO₂ efflux from grassland soils allowed us to conclude that the C will be utilized according to its utilizability: sugar>slurry>SOM. Additionally, decomposition of more inert C (here SOM) during the period of intensive sugar decomposition was strongly reduced (negative priming effect). We conclude that, priming effects involve a chain of mechanisms: (i) preferential substrate utilization, (ii) activation of microbial biomass by easily utilizable substrate (iii) subsequent increased utilization of following substrates according to their utilizability, and (iv) decline to initial state.     

The priming effect of organic matter: a question of microbial competition?

It is generally accepted that the low quality of soil carbon limits the amount of energy available for soil microorganisms, and in turn the rate of soil carbon mineralization. The priming effect, i.e. the increase in soil organic matter (SOM) decomposition rate after fresh organic matter input to soil, is often supposed to result from a global increase in microbial activity due to the higher availability of energy released from the decomposition of fresh organic matter. Work to date, however, suggests that supply of available energy induces no effect on SOM mineralization. The mechanisms of the priming effect are much more complex than commonly believed. The objective of this review was to build a conceptual model of the priming effect based on the contradictory results available in the literature adopting the concept of nutritional competition. After fresh organic matter input to soils, many specialized microorganisms grow quickly and only decompose the fresh organic matter. We postulated that the priming effect results from the competition for energy and nutrient acquisition between the microorganisms specialized in the decomposition of fresh organic matter and those feeding on polymerised SOM.     

Short and long-term effects of elevated CO2 on Lolium perenne rhizodeposition and its consequences on soil organic matter turnover and plant N yield

It is still unclear whether elevated CO₂ increases plant root exudation and consequently affects the soil microbial biomass. The effects of elevated CO₂ on the fate of the C and nitrogen (N) contained in old soil organic matter pools is also unclear. In this study the short and long-term effects of elevated CO₂ on C and N pools and fluxes were assessed by growing isolated plants of ryegrass (Lolium perenne) in glasshouses at elevated and ambient atmospheric CO₂ and using soil from the New Zealand FACE site that had >4 years exposure to CO₂ enrichment. Using ¹⁴CO₂ pulse labelling, the effects of elevated CO₂ on C allocation within the plant-soil system were studied. Under elevated CO₂ more root derived C was found in the soil and in the microbial biomass 48 h after labelling. The increased availability of substrate significantly stimulated soil microbial growth and acted as priming effect, enhancing native soil organic matter decomposition regardless of the mineral N supply. Despite indications of faster N cycling in soil under elevated CO₂, N availability to plants stayed unchanged. Soil previously exposed to elevated CO₂ exhibited a higher N cycling rate but again there was no effect on plant N uptake. With respect to the difficulties of extrapolating glasshouse experiment results to the field, we concluded that the accumulation of coarse organic matter observed in the field under elevated CO₂ was probably not created by an imbalance between C and N but was likely to be due to more complex phenomena involving soil mesofauna and/or other nutrients limitations.