Next Article in Journal
Insight into Hormonal Homeostasis and the Accumulation of Selected Heat Shock Proteins in Cold Acclimated and Deacclimated Winter Oilseed Rape (Brassica napus L.)
Previous Article in Journal
Irrigation Depth and Potassium Doses Affect Fruit Yield and Quality of Figs (Ficus carica L.)
 
 
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Article

Legacy Effect of Long-Term Elevated CO2 and Warming on Soil Properties Controls Soil Organic Matter Decomposition

1
Institute of Resource, Ecosystem and Environment of Agriculture, Nanjing Agricultural University, 1 Weigang, Nanjing 210095, China
2
Center of Agricultural Climate Change, Nanjing Agricultural University, 1 Weigang, Nanjing 210095, China
*
Author to whom correspondence should be addressed.
These authors contributed equally to this work.
Agriculture 2023, 13(3), 639; https://doi.org/10.3390/agriculture13030639
Submission received: 10 February 2023 / Revised: 3 March 2023 / Accepted: 5 March 2023 / Published: 8 March 2023
(This article belongs to the Section Agricultural Soils)

Abstract

:

Highlights

  • Litter quality change does not affect SOM decomposition under elevated CO2 and warming.
  • The legacy effect of elevated CO2 and warming on soil properties controls SOM decomposition.
  • Elevated CO2 may promote SOC sequestration by suppressing SOM decomposition.

Abstract

Plant litter quality is one of the key factors that control soil organic matter (SOM) decomposition. Under climate change, although significant change in litter quality has been intensively reported, the effect of litter quality change on SOM decomposition is poorly understood. This limits our ability to model the dynamics of soil carbon under climate change. To determine the effect of litter quality and soil property change on SOM decomposition, we performed a controlled, reciprocal transplant and litter decomposition experiments. The soils and plant litters were collected from a long-term field experiment, where four treatments were designed, including: (1) the control without warming at ambient CO2; (2) elevated atmospheric CO2 up to 500 ppm (C); (3) warming plant canopy by 2 °C (T); (4) elevated CO2 plus warming (CT). We found that elevated CO2 and warming altered the litter quality significantly in terms of macronutrients’ content and their stoichiometry. Elevated CO2 decreased the concentration of N in rice and wheat straw, while warming decreased the concentration of N and K in wheat straw. However, the change in plant litter quality did not lead to a shift in SOM decomposition. On the contrary, the legacy effect of long-term elevated CO2 and warming on soil properties dominated the decomposition rate of SOM. Elevated atmospheric CO2 suppressed SOM decomposition mainly by increasing phosphorous availability and lowering the soil C/N, fungi/bacteria ratio, and N-acetyl-glucosaminidase activity, while warming or elevated CO2 plus warming had no effect on SOM decomposition. Our results demonstrated that the changes in soil property other than litter quality control the decomposition of SOM under climate change, and soil property change in respond to climate change should be considered in model developing to predict terrestrial soil carbon dynamics under elevated atmospheric CO2 and warming.

1. Introduction

Climate change, mainly characterized by the rapid increase in the atmospheric CO2 concentration and the elevation of global surface temperature, is challenging the sustainable development of global agriculture. The concentration of CO2 in the atmosphere has been increasing since the 1840s, and it has exceeded 400 ppm in 2013 [1]. In the meantime, the global temperature is continuously rising. It is predicted that the atmospheric CO2 concentration will exceed 700 ppm [2], and the global temperature will increase by 1.1–6.4 °C by the end of this century [3].
Soil organic matter (SOM) in terrestrial ecosystems plays an important role in the global carbon cycle. Approximately 2000 petagrams of carbon are stored in the top two meters of global soils as SOM, and more than twice as much carbon is stored in the soil as in the world’s vegetation and atmosphere combined. Therefore, a slight change in SOM will have a profound impact on atmospheric CO2 concentration, which in turn influences the global climate. Although a great number of research studies have been conducted to investigate the effect of climate change on soil carbon cycling, it remains an open question whether elevated CO2 and global warming will promote soil carbon sequestration [4]. Several studies reported that elevated atmospheric CO2 could increase soil organic carbon (SOC) storage by increasing net CO2 uptake [5,6]. Liu et al. (2018) and Luo et al. (2006) predicted that the SOC stock would increase by approximately 5%, although it is quite small compared to the increase in the rate of plant biomass carbon under elevated CO2 [7,8]. However, Koyama et al. (2018) found that elevated atmospheric CO2 did not affect the SOC pool in a Mojave Desert ecosystem [9]. Similar findings were reported in cropland and temperate grassland ecosystems [10,11]. Furthermore, increased soil CO2 flux under elevated CO2 has been frequently reported [7]. Kuzyakov et al. (2019) argued that elevated atmospheric CO2 has no (or little) effect on the soil carbon pool but strongly increases the CO2 fluxes and accelerates carbon cycles [12]. Similarly to elevated CO2, recent meta-analyses have shown that global warming generally has no [13,14,15,16,17] or negative [13,15] effects on the SOC pool. Long-term warming decreased the SOC pool by stimulating microbial utilization of the recalcitrant C pool [13]. However, most of the studies involved in these meta-analyses were conducted in forest or grassland ecosystems. It remains unclear whether global warming will affect the pools and fluxes of SOC in cropland ecosystems. This uncertainty limits our accurate prediction of soil carbon stock change under elevated CO2 and warming.
The concentration of CO2 in soil is much higher than that in the atmosphere (10–50 times), and elevated atmospheric CO2 (+200 ppm) will probably not affect soil carbon cycling directly [18]. Its effect on soil carbon cycling is indirect, through the plant growth changes. Elevated CO2 and warming affect plant growth by altering leaf stomatal conductance and the photosynthesis rate [19]. Elevated CO2 can increase crop yield by photosynthesis rate and soil nutrients use efficiency increase [5]. As the atmospheric CO2 concentration increases, the nutrient conditions of grains and the shoot biomass will change accordingly. Therefore, some studies have predicted that plants would be exposed to a global nutrient imbalance with lower N contents or higher ratios of C:N and C:P in plant litters under elevated CO2 [20,21]. In addition to macronutrients, the micronutrients in plant litter will also decrease under elevated CO2 [22]. He et al. (2015) even found that elevated CO2 and warming reduced the content of crude protein and the in vitro digestibility of wheat straw [23]. Plant litter with different chemical properties would likely affect the decomposition rate of SOM. For example, Elias et al. (2020) found that plant litter with higher P content and lower lignin to N ratios decompose faster in a forest soil [24]. Fanin et al. (2011) also found that the content of C, N and P and their stoichiometry in plant litters were important factors that regulate soil microbial respiration [25]. However, under elevated CO2 and warming, the effect of litter quality change on SOM decomposition has never been tested.
In addition to plant litter quality, the soil microbial community also regulates the decomposition of SOM. Under elevated CO2 or warming, significant changes in soil microbial communities have been reported intensively [26,27,28]. Several studies found that elevated CO2 altered the soil microbial composition [29,30,31,32,33,34,35,36]. Soils exposed to elevated CO2 had higher relative abundances of fungi and higher enzyme activity [29,37], which led to more soil carbon loss [30,31,36,38]. Lipson et al. (2005) observed that elevated CO2 had no effect on bacterial diversity but increased fungal biomass in a Chaparral Ecosystem [33]. Sun et al. (2021) found that the soil microbial community evolves from dominating K-strategists to r-strategists under elevated CO2, with decreasing ratios of fungi to bacteria, Gram-positive to Gram-negative bacteria and Acidobacteria to Proteobacteria [28]. Warming generally increases the abundance of microorganisms related to soil carbon and nitrogen cycling, leading to soil carbon loss and greater N2O emissions [39,40]. Some studies showed that warming reduced bacterial and fungal abundance in forest ecosystems [41,42]. The soil microbial community structure was also altered by warming [43]. Deslippe et al. (2012) found that warming decreased bacterial communities evenness while it increased fungal communities evenness [44]. Cheng et al. (2017) showed that warming increased the relative abundance of key functional genes involved in soil carbon degradation [39]. Sheik et al. (2011) found that warming increased the soil microbial population size but decreased diversity under wet conditions, whereas it reduced the microbial population size under drought conditions [45]. Under elevated atmospheric CO2 and warming, the abundance of some dominant phyla was significantly increased, and the effect of combined elevated CO2 and warming on soil functional processes was similar to that of only elevated CO2 [46].
Under elevated CO2 or warming, the changes in the soil microbial community and plant litter quality have been observed as mentioned above. Understanding the effect of plant litter quality and the soil microbial community on soil organic carbon decomposition can help us to model soil carbon dynamics under elevated CO2 and warming. To our knowledge, there was no report investigating the effect of plant litter quality and soil microbial community change on soil organic carbon mineralization under these elevated conditions. Three manipulated incubation experiments were conducted to answer the following questions: (1) Does plant litter quality (C:N and nutrient content) change affect SOM decomposition under elevated CO2 and warming? (2) Does soil microbial community change affect SOM decomposition under elevated CO2 and warming? (3) Does plant litter have a greater effect on SOM decomposition than soil microbial community? We hypothesized that plant litter with decreased quality under elevated CO2 and warming would suppress SOM decomposition, whereas the change in the soil microbial community would promote SOM decomposition. The results of this study can be used in soil carbon cycling model developing to predict terrestrial carbon dynamics under future climate change of elevated CO2 and warming more precisely.

2. Materials and Methods

2.1. Soils and Plants Litter

The soils and plants litter used in this study were collected from the long-term field experiment of Nanjing Agricultural University, which was located in Kangbo Village (31°30′48″ N, 120°33′36″ E), Changshu City, Jiangsu Province of China. The field experiment facility was constructed in 2010, and the objective of this facility was to simulate Free Air CO2 Enrichment and plant canopy warming in an open field (Figure 1). The soil is a Gleyic Stagnic Anthrosol (WRB-FAO) derived from clayey lacustrine deposit and cultivated with summer rice-winter wheat rotation dating back hundreds of years. The basic properties of the topsoil before the experiment onset were: pH (H2O) 7.0, bulk density of 1.2 g cm−3, and concentration of organic C and total N of 16.0 g kg−1 and 1.9 g kg−1, respectively. There were four treatments, including elevated CO2 up to 500 ppm (C), warming plant canopy by 2 °C (T), elevated CO2 plus plant canopy warming (CT), and ambient CO2 without warming as the control (Control). The soils were collected from the top 15 cm in June 2018, after 7 years of treatment. The plant litters (rice and wheat straw) were collected at harvest. Rice straw (Cultivar: Changyou 5) was collected in October 2017, and wheat straw (Cultivar: Yangmai 16) was collected in June 2018.

2.2. Experimental Design

Three incubation experiments were designed (Table 1). In the first experiment (Experiment I), the soils from the control, C, T and CT treatments were incubated with the addition of crop straw from the control, C, T and CT treatments, respectively. In the second experiment (Experiment II), the soils from the control were incubated with the addition of crop straw from the control, C, T and CT treatments. In the third experiment (Experiment III), the soils from the control, C, T and CT treatments were incubated with the addition of crop straw from the control. All the treatments were replicated three times.
Fifty grams of air-dried soils were mixed with 0.06 g of rice straw, and the mixture was placed in a 500 mL flask. All flasks were incubated at 25 °C in the dark. The bottle was sealed with a cap, and two rubber tubes (16 cm and 7 cm in length) were inserted into the bottle cap. A three-way valve was sleeved above the rubber tube for fresh air and gas sample collection. To simulate the soil respiration process during the whole crop growing season in the study area, two soil water conditions were designed. The soils mixed with rice straw were incubated first at aerobic conditions with soil water content maintained at 80% of the soil water holding capacity. Then, they were mixed with wheat straw (0.06 g) and incubated under flooded conditions. During aerobic incubation, gas sampling was performed on Days 1, 1.5, 2, 3, 4, 5, 6, 8, 9, 11, 13, 15, 17, 19, 23, 28, 33, 43 and 64. During anaerobic incubation, gas sampling was performed on Days 65, 65.5, 66, 66.5, 67.5, 69, 71, 73, 82, 89, 98, 115, 123, 131, 139 and 147. Gas samples were collected with a syringe 2 h after ventilation.
The concentration of CO2 in the gas samples was detected in a gas chromatograph (Agilent 7890A). The emission rate of CO2 was calculated using the following equation:
F = ρ × V m × Δ C Δ t × 273 273 + T × α  
where F represents the CO2 emission rate (mg C·kg−1·d−1); ρ represents the density of CO2, which is 1.997 g·L−1; V represents the volume of air above the flask (L); m represents the mass of soil (g); ΔC represents the change in CO2 concentration in the gas sample (μmol·mol−1); Δt represents the sampling time (d) of the closed flask; and T is the temperature of the incubation (25 °C). α represents the conversion coefficient, 12/44 (C/CO2).

2.3. Plant and Soil Sample Analysis

Plant and soil samples were analyzed following the protocol described by Lu (2000) [47]. The plant samples were digested with sulfuric acid and hydrogen peroxide. The contents of nitrogen, phosphorus and potassium in the digestion were determined by the micro-Kjeldahl determination method, colorimetric method and flame photometer method, respectively. Total organic carbon and total nitrogen were measured by a CNS Macro Elemental Analyzer (Elementar, Germany). Dissolved organic carbon (DOC) was extracted with 0.05 mol·L−1 K2SO4 solution. The mixture was shaken at 180 r·min−1 for 30 min and then passed through a 0.45 μm filter. The concentration of DOC in the liquid was measured in a TOC analyzer. Soil pH was measured in distilled water (soil/water ratio of 1/2.5 w/w) with a pH meter (Seven Easy Mettler Toledo, China, 2008). Soil available K was extracted with 1.0 mol L−1 ammonium acetate (pH 7.0) and determined with a flame photometer (FP6410, Company of Shanghai Jingke, China). Soil available P was extracted with 1.0 mol L−1 sodium bicarbonate and determined using colorimetric method.
Soil microbial biomass carbon (MBC) was determined using the chloroform fumigation-extraction method. Fresh soils were fumigated at 25 °C for 24 h. The fumigated soils were extracted with 0.5 mol·L−1 K2SO4 solution for 30 min in a shaker (180 r·min−1). Then, the mixture was filtered through a 0.45 μm water-based filter membrane. The concentration of carbon in the extract was measured with a TOC analyzer (Multi N/C 3100). MBC = (fumigated C-unfumigated C)/0.45
Microbial metabolic quotient is the ratio of carbon emitted by soil respiration to soil microbial biomass during incubation time. Soil PLFA was determined according to the method of Frostegård and Bååth (1996) [48]. PLFAs were extracted from freeze-dried soil samples (2 g) with a single-phase chloroform/methanol/citric acid buffer (15 mL at a 1:2:0.8 vol ratio). Total concentration of PLFAs (nmol·g−1) was set to account for total microbial biomass. Bacterial/fungal ratio (B/F) was calculated by dividing the bacterial biomass by the fungal biomass. Soil enzyme activity was determined by fluorescence microplate method with MUB (4-methylumbelliferone) and L-DOPa (L-3,4-dihydroxyphenylalanine) substrates. Fresh soil samples equivalent to 2.0 g of dry soil were weighed into a glass beaker, 300 mL buffer was added to make soil suspension, and this was homogenized thoroughly on a magnetic stirrer. Then, 200 µL soil suspension and 50 µL of 200 µmol·L−1 MUB substrate were siphoned off with a pipette gun into a 96-well black polystyrene microplate. At the same time, MUB standard solution was used to make the standard curve of each soil sample to be tested. The fluorescence values were measured by Perkinelmer EnSight (Perkinelmer, MA, USA) with excitation and absorption wavelengths of 365 nm and 450 nm after 3 h of culture at 25 °C under dark conditions.

2.4. Statistical Analysis

Data are expressed as the mean plus/minus one standard deviation of three replicates. One-way ANOVA followed by the least significant difference (LSD) was used to test the difference among the various treatments. Statistical significance was set at p < 0.05. All statistical analyses were carried out in SPSS 20.0, and figures were made by Origin 2021.

3. Results

3.1. Changes in Litter Quality under Elevated CO2 and Warming

Table 2 shows the nutrient concentration of rice and wheat straw under elevated CO2 and warming. Elevated CO2 decreased the N concentration of rice and wheat straw by 16.5% and 39.7%, respectively. Under elevated CO2, the K concentration of wheat also decreased significantly. Warming decreased the N and K concentration of wheat straw by 25.2% and 52.9%, respectively. Under elevated CO2 plus warming, the N and P concentration of rice straw and the N and K concentration of wheat straw decreased significantly compared to the control.

3.2. The Effect of Elevated CO2 and Warming on Soil Respiration (Experiment I)

The average CO2 emission rate during the aerobic stage was 66.39 mg C·kg−1·d−1, which was about 13 times higher than the one during the anaerobic stage (Figure 2A). During the aerobic stage, the emission peak occurred on the first day of incubation, and since then, it decreased dramatically until Day 2. From Day 4 to Day 64, soil CO2 emission rate gradually decreased. During the anaerobic stage, soil CO2 emission rate dramatically increased in the first 15 days and then gradually declined. The emission peak was observed at Day 82.
The cumulative release of CO2 (soil respiration hereafter) from the soil is shown in Figure 3A. Much more CO2 was released during the aerobic stage, which accounted for about 90% of the overall release rate. During the aerobic process, elevated CO2 decreased soil respiration by 27.60% compared to the control, while warming or elevated CO2 plus warming had no effect on it. During the anaerobic process, all the treatments had no effect on soil respiration.

3.3. The Effect of Litter Quality Change on Soil Respiration (Experiment II)

As shown in Figure 2B, the CO2 released dynamics across treatments were very similar to Experiment I. During the anaerobic stage, the CO2 release rate increased dramatically in the first 15 days and was then gradually declined. The emission peak was observed at Day 82. Adding litters from different climate change treatments to the control soil had no effect on the soil respiration rate (Figure 3B).

3.4. The Effect of Soil Property Change on Soil Respiration (Experiment III)

As shown in Figure 2C, the CO2 release dynamics across treatments were very similar to Experiment I and Experiment II. However, soil respiration varied greatly across treatments during the aerobic incubation stage. Compared to the ambient control, soils treated with elevated CO2 plus warming emitted higher amounts of CO2. The accumulated CO2 emission of soils treated with elevated CO2 was 2874 mg C·kg−1, which was significantly lower than the values from soils under warming and elevated CO2 plus warming. During the anaerobic stage, there were no significant treatment effects (Figure 3C).

3.5. Correlation between Soil Respiration and Soil Characteristics

In Experiment I, soil respiration rate was positively correlated with microbial metabolic quotient, soil C:N, fungi to bacteria ratio and N-acetyl-glucosaminidase activity, but was negatively correlated with soil available P (Table 3). In Experiment III, soil respiration rate was positively correlated with SOC, dissolved organic carbon, microbial metabolic quotient, soil available K and β-Glucosidase activity, but it was negatively correlated with soil microbial biomass carbon and available P content.

4. Discussion

Under future climate change of elevated CO2 and warming, the changes in soil condition and litter quality have been observed, and they were supposed to alter the decomposition of SOM. Then, a new balance between organic carbon inputs and soil carbon losses, which can be used to predict the dynamics of SOC under climate change conditions, might be reached. However, this hypothesis was not fully supported by the current study. We found that the legacy effect of long-term elevated CO2 and warming on soil conditions dominated the decomposition of SOM. Plant litter quality change had no effect on SOM mineralization, although significant changes in plant litter quality were observed in this study and among others [21,49]. Hillstrom et al. (2010) also found that elevated CO2 had a minimal effect on microbial respiration in a forest system, although it affected litter quality significantly [50], whereas Cornwell et al. (2008) found that the decomposition rate of litter caused by litter quality is three times that of climate factors [51]. This may be true for ecosystems on a large scale, but for small areas of field, like that in the current study, this might not be true.
The response of soil respiration to elevated CO2 varied across studies [7,52,53,54,55]. A recent study had shown that elevated CO2 increased soil respiration by 25% on average [7]; however, this study showed that elevated CO2 suppressed soil respiration compared with the ambient control, although neutral or negative effects have also been reported. Two reasons accounted for the higher soil respiration rate found under elevated CO2 levels. Firstly, elevated CO2 stimulated soil respiration by increasing the labile carbon pools. This carbon derived mainly from fine roots development and their exudates; most of it was decomposed by soil microbes and released to the atmosphere directly without forming aggregates with soil minerals [56,57]. Therefore, no net carbon gains were observed in soils under elevated CO2. Secondly, elevated CO2 stimulated soil respiration via the water saving effect. Under elevated CO2, leaf stoma closure reduced plant transpiration, and more water could be stored in soil, which facilitated soil microbial respiration [53]. However, the water saving effect can only be observed in dry soil conditions; under wet soil conditions, it will decrease soil respiration because of low soil aeration. Therefore, Bader and Körner (2010) argued that there was no overall simulation of soil respiration under elevated CO2 in a mature deciduous forest ecosystem [53]. Furthermore, the magnitude of the soil respiration stimulating effect does not persist forever, and it will decline over the years with atmospheric CO2 enrichment [58]. This suggests that soil microbial community can adapt to long-term elevated CO2, and a new balance between carbon inputs and outputs can be reached. In the current study, there was no water saving effect as described in previous studies, because the soils were incubated at the same water condition, and there were no carbon additions via root exudates. Therefore, no stimulation effect was observed. The soils under long-term elevated CO2 had higher phosphorous availability and lower soil C:N, fungi-to-bacteria ratio, and N-acetyl-glucosaminidase activity, which collectively led to the lower soil respiration rates (Table 3).
This study also demonstrated that soil respiration under elevated CO2 plus warming responded differently to litter addition (Figure 3; Experiment I, Experiment III). The soil incorporated with litter from the control had a significant higher CO2 emission rate than the soil with litter from the treatment of elevated CO2 plus warming. In experiment III, the soil respiration rate of soil under elevated CO2 plus warming was even higher than the rate of soil under the control and elevated CO2 alone, which was different from the results in experiment I. We attributed this to the adaptation of the soil microbial community to long-term elevated CO2 and warming [59]. The soil microbes in this study under 7 years of elevated CO2, warming or both elevated CO2 and warming have to obtaining nutrients and energy from SOM and litter in a more efficient way, and CO2 was emitted. In contrast, a sudden change in food resource (adding litter from other environments, such as the litter from the control in this study) led to a lower carbon use efficiency, which caused a high soil respiration rate, especially for the warming treatment soils. Therefore, the soil microbes need to decompose more organic matter to obtain similar amounts of nutrients after food change.

5. Conclusions

The study showed that under elevated CO2 and warming, the change in plant litter has no effect on the decomposition of soil organic matter, even though significant changes in litter quality have been observed. The decomposition of soil organic matter is controlled by the legacy effect of soil properties changes under climate change conditions. Changes in soil phosphorous availability and C/N, fungi/bacteria ratio and N-acetyl-glucosaminidase activity may be attributed to the alternation of SOM decomposition under elevated CO2. Elevated atmospheric CO2 may promote soil carbon sequestration by suppressing soil microbial respiration under no temperature elevation conditions.

Author Contributions

J.L. and B.S.: writing—original draft and data analyzing; B.S. and C.L.: methodology, formal analysis and investigation; X.L.: conceptualization, data analyzing, writing the original draft and funding acquisition; M.D., X.Z., L.L. and G.P.: review and editing the manuscript. All authors have read and agreed to the published version of the manuscript.

Funding

This study was financially supported by the National Key R & D Program of China (2017YFD0300202) and the Sino-German Mobility Program (M-0105).

Data Availability Statement

The data that support the findings of this study are available from the corresponding author upon reasonable request.

Acknowledgments

We would like to thank Zheng Jufeng, Liu Xiuxia, Liu Zhiwei and Xiong Li for providing the data on soil properties.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Climate Change 2014: Synthesis Repor; Pachauri, R.K.; Mayer, L.; Intergovernmental Panel on Climate Change (Eds.) Intergovernmental Panel on Climate Change: Geneva, Switzerland, 2015; ISBN 978-92-9169-143-2. [Google Scholar]
  2. Prentice, I.C.; Farquhar, G.D.; Fasham, M.J.R.; Goulden, M.L.; Heimann, M.; Jaramillo, V.J.; Kheshgi, H.S.; Le Quéré, C.; Scholes, R.J.; Wallace, D.W.R. The Carbon Cycle and Atmospheric Carbon Dioxide. In Climate Change 2001: The Scientific Basis; Cambridge University Press: Cambridge, UK, 2001; pp. 183–237. [Google Scholar]
  3. Climate Change 2007: The Physical Science Basis; Intergovernmental Panel on Climate Change (Ed.) Cambridge University Press: Cambridge, UK, 2007; ISBN 978-0-521-88009-1. [Google Scholar]
  4. Terrer, C.; Phillips, R.P.; Hungate, B.A.; Rosende, J.; Pett-Ridge, J.; Craig, M.E.; van Groenigen, K.J.; Keenan, T.F.; Sulman, B.N.; Stocker, B.D.; et al. A Trade-off between Plant and Soil Carbon Storage under Elevated CO2. Nature 2021, 591, 599–603. [Google Scholar] [CrossRef] [PubMed]
  5. Hyvönen, R.; Ågren, G.I.; Linder, S.; Persson, T.; Cotrufo, M.F.; Ekblad, A.; Freeman, M.; Grelle, A.; Janssens, I.A.; Jarvis, P.G.; et al. The Likely Impact of Elevated CO2, Nitrogen Deposition, Increased Temperature and Management on Carbon Sequestration in Temperate and Boreal Forest Ecosystems: A Literature Review: Tansley Review. New Phytol. 2007, 173, 463–480. [Google Scholar] [CrossRef] [PubMed]
  6. Jastrow, J.D.; Michael Miller, R.; Matamala, R.; Norby, R.J.; Boutton, T.W.; Rice, C.W.; Owensby, C.E. Elevated Atmospheric Carbon Dioxide Increases Soil Carbon. Glob. Chang. Biol. 2005, 11, 2057–2064. [Google Scholar] [CrossRef]
  7. Liu, S.; Ji, C.; Wang, C.; Chen, J.; Jin, Y.; Zou, Z.; Li, S.; Niu, S.; Zou, J. Climatic role of terrestrial ecosystem under elevated CO2: A bottom-up greenhouse gases budget. Ecol. Lett. 2018, 21, 1108–1118. [Google Scholar] [CrossRef] [Green Version]
  8. Luo, Y.; Hui, D.; Zhang, D. Elevated CO2 stimulates net accumulations of carbon and nitrogen in land ecosystems: A meta-analysis. Ecology 2006, 87, 53–63. [Google Scholar] [CrossRef] [Green Version]
  9. Koyama, A.; Harlow, B.; Kuske, C.R.; Belnap, J.; Evans, R.D. Plant and microbial biomarkers suggest mechanisms of soil organic carbon accumulation in a mojave desert ecosystem under elevated CO2. Soil Biol. Biochem. 2018, 120, 48–57. [Google Scholar] [CrossRef]
  10. Keidel, L.; Lenhart, K.; Moser, G.; Müller, C. Depth-dependent response of soil aggregates and soil organic carbon content to long-term elevated CO2 in a temperate grassland soil. Soil Biol. Biochem. 2018, 123, 145–154. [Google Scholar] [CrossRef]
  11. Van Kessel, C.; Nitschelm, J.; Horwath, W.R.; Harris, D.; Walley, F.; Lüscher, A.; Hartwig, U. Carbon-13 input and turn-over in a pasture soil exposed to long-term elevated atmospheric CO2: Pasture soil C-cycling. Glob. Chang. Biol. 2000, 6, 123–135. [Google Scholar] [CrossRef]
  12. Kuzyakov, Y.; Horwath, W.R.; Dorodnikov, M.; Blagodatskaya, E. Review and synthesis of the effects of elevated atmospheric CO2 on soil processes: No changes in pools, but Increased Fluxes and Accelerated Cycles. Soil Biol. Biochem. 2019, 128, 66–78. [Google Scholar] [CrossRef]
  13. Chen, J.; Elsgaard, L.; Groenigen, K.J.; Olesen, J.E.; Liang, Z.; Jiang, Y.; Lærke, P.E.; Zhang, Y.; Luo, Y.; Hungate, B.A.; et al. Soil carbon loss with warming: New evidence from carbon-degrading enzymes. Glob. Chang. Biol. 2020, 26, 1944–1952. [Google Scholar] [CrossRef]
  14. Gao, W.; Yan, D. Warming suppresses microbial biomass but enhances N recycling. Soil Biol. Biochem. 2019, 131, 111–118. [Google Scholar] [CrossRef]
  15. Lu, M.; Zhou, X.; Yang, Q.; Li, H.; Luo, Y.; Fang, C.; Chen, J.; Yang, X.; Li, B. Responses of ecosystem carbon cycle to experimental warming: A meta-analysis. Ecology 2013, 94, 726–738. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  16. Xu, W.; Yuan, W. Responses of microbial biomass carbon and nitrogen to experimental warming: A meta-analysis. Soil Biol. Biochem. 2017, 115, 265–274. [Google Scholar] [CrossRef]
  17. Zhang, X.Z.; Shen, Z.X.; Fu, G. A meta-analysis of the effects of experimental warming on soil carbon and nitrogen dynamics on the Tibetan Plateau. Appl. Soil Ecol. 2015, 87, 32–38. [Google Scholar] [CrossRef]
  18. van de Geijn, S.C.; Veen, J.A. Implications of increased carbon dioxide levels for carbon input and turnover in soils. Vegetatio 1993, 104/105, 282–292. [Google Scholar] [CrossRef]
  19. Long, S.P.; Ainsworth, E.A.; Rogers, A.; Ort, D.R. Rising atmospheric carbon dioxide: Plants FACE the future. Annu. Rev. Plant Biol. 2004, 55, 591–628. [Google Scholar] [CrossRef]
  20. Sardans, J. The C:N:P stoichiometry of organisms and ecosystems in a changing world: A review and perspectives. Perspect. Plant Ecol. Evol. Syst. 2012, 14, 33–47. [Google Scholar] [CrossRef]
  21. Wang, J.; Liu, X.; Zhang, X.; Li, L.; Lam, S.K.; Pan, G. Changes in plant C, N and P ratios under elevated CO2 and canopy warming in a rice-winter wheat rotation system. Sci. Rep. 2019, 9, 5424. [Google Scholar] [CrossRef] [Green Version]
  22. Wang, J.; Li, L.; Lam, S.K.; Liu, X.; Pan, G. Responses of wheat and rice grain mineral quality to elevated carbon dioxide and canopy warming. Field Crops Res. 2020, 249, 107753. [Google Scholar] [CrossRef]
  23. He, X.; Wu, Y.; Cai, M.; Mu, C.; Luo, W.; Cheng, Y.; Zhu, W. The Effect of increased atmospheric temperature and CO2 concentration during crop growth on the chemical composition and in vitro rumen fermentation characteristics of wheat straw. J. Animal Sci. Biotechnol. 2015, 6, 46. [Google Scholar] [CrossRef] [Green Version]
  24. Elias, D.M.O.; Robinson, S.; Both, S.; Goodall, T.; Majalap-Lee, N.; Ostle, N.J.; McNamara, N.P. Soil microbial community and litter quality controls on decomposition across a tropical forest disturbance gradient. Front. For. Glob. Chang. 2020, 3, 81. [Google Scholar] [CrossRef]
  25. Fanin, N.; Hättenschwiler, S.; Barantal, S.; Schimann, H.; Fromin, N. Does variability in litter quality determine soil microbial respiration in an amazonian rainforest? Soil Biol. Biochem. 2011, 43, 1014–1022. [Google Scholar] [CrossRef]
  26. Butterly, C.R.; Phillips, L.A.; Wiltshire, J.L.; Franks, A.E.; Armstrong, R.D.; Chen, D.; Mele, P.M.; Tang, C. Long-term effects of elevated CO2 on carbon and nitrogen functional capacity of microbial communities in three contrasting soils. Soil Biol. Biochem. 2016, 97, 157–167. [Google Scholar] [CrossRef] [Green Version]
  27. He, Z.; Xiong, J.; Kent, A.D.; Deng, Y.; Xue, K.; Wang, G.; Wu, L.; Van Nostrand, J.D.; Zhou, J. Distinct responses of soil microbial communities to elevated CO2 and O3 in a soybean agro-ecosystem. ISME J. 2014, 8, 714–726. [Google Scholar] [CrossRef] [Green Version]
  28. Sun, Y.; Wang, C.; Yang, J.; Liao, J.; Chen, H.Y.H.; Ruan, H. Elevated CO2 shifts soil microbial communities from K- to r-Strategists. Glob. Ecol. Biogeogr. 2021, 30, 961–972. [Google Scholar] [CrossRef]
  29. Carney, K.M.; Hungate, B.A.; Drake, B.G.; Megonigal, J.P. Altered soil microbial community at elevated CO2 leads to loss of soil carbon. Proc. Natl. Acad. Sci. USA 2007, 104, 4990–4995. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  30. Chung, H.; Zak, D.R.; Reich, P.B.; Ellsworth, D.S. Plant Species Richness, Elevated CO2, and atmospheric nitrogen deposition alter soil microbial community composition and function. Glob. Chang. Biol. 2007, 13, 980–989. [Google Scholar] [CrossRef] [Green Version]
  31. He, Z.; Xu, M.; Deng, Y.; Kang, S.; Kellogg, L.; Wu, L.; Van Nostrand, J.D.; Hobbie, S.E.; Reich, P.B.; Zhou, J. Metagenomic analysis reveals a marked divergence in the structure of belowground microbial communities at elevated CO2: Changes in the soil microbial community at elevated CO2. Ecol. Lett. 2010, 13, 564–575. [Google Scholar]
  32. Jin, J.; Wood, J.; Franks, A.; Armstrong, R.; Tang, C. Long-term CO2 enrichment alters the diversity and function of the microbial community in soils with high organic carbon. Soil Biol. Biochem. 2020, 144, 107780. [Google Scholar] [CrossRef]
  33. Lipson, D.A.; Wilson, R.F.; Oechel, W.C. Effects of elevated atmospheric CO2 on soil microbial biomass, activity, and diversity in a chaparral ecosystem. Appl. Environ. Microbiol. 2005, 71, 8573–8580. [Google Scholar] [CrossRef] [Green Version]
  34. Yang, S.; Zheng, Q.; Yuan, M.; Shi, Z.; Chiariello, N.R.; Docherty, K.M.; Dong, S.; Field, C.B.; Gu, Y.; Gutknecht, J.; et al. Long-term elevated CO2 shifts composition of soil microbial communities in a californian annual grassland, reducing growth and N utilization potentials. Sci. Total Environ. 2019, 652, 1474–1481. [Google Scholar] [CrossRef] [PubMed]
  35. Yu, H.; Deng, Y.; He, Z.; Pendall, E.; Carrillo, Y.; Wang, S.; Jin, D.; Wu, L.; Wang, A.; Xu, Y.; et al. Stimulation of soil microbial functioning by elevated CO2 may surpass effects mediated by irrigation in a semiarid grassland. Geoderma 2021, 401, 115162. [Google Scholar] [CrossRef]
  36. Zhou, J.; Deng, Y.; Luo, F.; He, Z.; Yang, Y. Phylogenetic molecular ecological network of soil microbial communities in response to elevated CO2. mBio 2011, 2, e00122-11. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  37. Drigo, B.; Pijl, A.S.; Duyts, H.; Kielak, A.M.; Gamper, H.A.; Houtekamer, M.J.; Boschker, H.T.S.; Bodelier, P.L.E.; Whiteley, A.S.; Veen, J.A.; et al. Shifting carbon flow from roots into associated microbial communities in response to elevated atmospheric CO2. Proc. Natl. Acad. Sci. USA 2010, 107, 10938–10942. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  38. Cotton, T.E.A.; Fitter, A.H.; Miller, R.M.; Dumbrell, A.J.; Helgason, T. Fungi in the future: Interannual variation and effects of atmospheric change on arbuscular mycorrhizal fungal communities. New Phytol. 2015, 205, 1598–1607. [Google Scholar] [CrossRef] [Green Version]
  39. Cheng, L.; Zhang, N.; Yuan, M.; Xiao, J.; Qin, Y.; Deng, Y.; Tu, Q.; Xue, K.; Van Nostrand, J.D.; Wu, L.; et al. Warming enhances old organic carbon decomposition through altering functional microbial communities. ISME J. 2017, 11, 1825–1835. [Google Scholar] [CrossRef] [Green Version]
  40. Dai, Z.; Yu, M.; Chen, H.; Zhao, H.; Huang, Y.; Su, W.; Xia, F.; Chang, S.X.; Brookes, P.C.; Dahlgren, R.A.; et al. Elevated temperature shifts soil N cycling from microbial immobilization to enhanced mineralization, nitrification and denitrification across global terrestrial ecosystems. Glob. Chang. Biol. 2020, 26, 5267–5276. [Google Scholar] [CrossRef]
  41. Allison, S.D.; Treseder, K.K. Warming and Drying Suppress Microbial activity and carbon cycling in boreal forest soils: Warming suppresses microbial activity. Glob. Chang. Biol. 2008, 14, 2898–2909. [Google Scholar] [CrossRef] [Green Version]
  42. Frey, S.D.; Drijber, R.; Smith, H.; Melillo, J. Microbial biomass, functional capacity, and community structure after 12 years of soil warming. Soil Biol. 2008, 4, 2904–2907. [Google Scholar] [CrossRef]
  43. Guo, X.; Feng, J.; Shi, Z.; Zhou, X.; Yuan, M.; Tao, X.; Hale, L.; Yuan, T.; Wang, J.; Qin, Y.; et al. Climate warming leads to divergent succession of grassland microbial communities. Nature Clim. Chang. 2018, 8, 813–818. [Google Scholar] [CrossRef] [Green Version]
  44. Deslippe, J.R.; Hartmann, M.; Simard, S.W.; Mohn, W.W. Long-term warming alters the composition of arctic soil microbial communities. FEMS Microbiol Ecol. 2012, 82, 303–315. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  45. Sheik, C.S.; Beasley, W.H.; Elshahed, M.S.; Zhou, X.; Luo, Y.; Krumholz, L.R. Effect of warming and drought on grassland microbial communities. ISME J. 2011, 5, 1692–1700. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  46. Yu, H.; Deng, Y.; He, Z.; Van Nostrand, J.D.; Wang, S.; Jin, D.; Wang, A.; Wu, L.; Wang, D.; Tai, X.; et al. Elevated CO2 and warming altered grassland microbial communities in soil top-layers. Front. Microbiol. 2018, 9, 1790. [Google Scholar] [CrossRef] [PubMed]
  47. Lu, R. Analytical Methods for Soil Agricultural Chemistry; China Agricultural Science and Technology Press: Beijing, China, 2000. (In Chinese) [Google Scholar]
  48. FrostegArd, A.; BAAth, E. The use of phospholipid fatty acid analysis to estimate bacterial and fungal biomass in Soil. Biol. Fertil. Soils 1996, 22, 59–65. [Google Scholar]
  49. Lieffering, M.; Kim, H.-Y.; Kobayashi, K.; Okada, M. The impact of elevated CO2 on the elemental concentrations of field-grown rice grains. Field Crops Res. 2004, 88, 279–286. [Google Scholar] [CrossRef]
  50. Hillstrom, M.; Meehan, T.D.; Kelly, K.; Lindroth, R.L. Soil carbon and nitrogen mineralization following deposition of insect frass and greenfall from forests under elevated CO2 and O3. Plant Soil. 2010, 336, 75–85. [Google Scholar] [CrossRef]
  51. Cornwell, W.K.; Cornelissen, J.H.C.; Amatangelo, K.; Dorrepaal, E.; Eviner, V.T.; Godoy, O.; Hobbie, S.E.; Hoorens, B.; Kurokawa, H.; Pérez-Harguindeguy, N.; et al. Plant species traits are the predominant control on litter decomposition rates within biomes worldwide. Ecol. Lett. 2008, 11, 1065–1071. [Google Scholar] [CrossRef]
  52. King, J.S.; Hanson, P.J.; Bernhardt, E.; DeAngelis, P.; Norby, R.J.; Pregitzer, K.S. A multiyear synthesis of soil respiration responses to elevated atmospheric CO2 from four forest FACE experiments: Elevated CO2 increases forest soil respiration. Glob. Chang. Biol. 2004, 10, 1027–1042. [Google Scholar] [CrossRef]
  53. Bader, M.K.-F.; Körner, C. No overall stimulation of soil respiration under mature deciduous forest trees after 7 years of CO2 enrichment: Forest soil respiration under elevated CO2. Glob. Chang. Biol. 2010, 16, 2830–2843. [Google Scholar] [CrossRef]
  54. Clark, K.L.; Skowronski, N.; Hom, J. Invasive insects impact forest carbon dynamics: Defoliation and forest carbon dynamics. Glob. Chang. Biol. 2010, 16, 88–101. [Google Scholar] [CrossRef] [Green Version]
  55. Keidel, L.; Kammann, C.; Grünhage, L.; Moser, G.; Müller, C. Positive feedback of elevated CO2 on soil respiration in late autumn and winter. Biogeosciences 2015, 12, 1257–1269. [Google Scholar] [CrossRef] [Green Version]
  56. Andrews, J.A.; Schlesinger, W.H. Soil CO2 dynamics, acidification, and chemical weathering in a temperate forest with experimental CO2 enrichment. Glob. Biogeochem. Cycles 2001, 15, 149–162. [Google Scholar] [CrossRef]
  57. Lagomarsino, A.; Lukac, M.; Godbold, D.L.; Marinari, S.; De Angelis, P. Drivers of increased soil respiration in a poplar coppice exposed to elevated CO2. Plant Soil. 2013, 362, 93–106. [Google Scholar] [CrossRef]
  58. Bernhardt, E.S.; Barber, J.J.; Pippen, J.S.; Taneva, L.; Andrews, J.A.; Schlesinger, W.H. Long-term effects of free air CO2 enrichment (FACE) on soil respiration. Biogeochemistry 2006, 77, 91–116. [Google Scholar] [CrossRef]
  59. Bradford, M.A. Thermal adaptation of decomposer communities in warming soils. Front. Microbiol. 2013, 4, 333. [Google Scholar] [CrossRef] [PubMed] [Green Version]
Figure 1. A photograph of the experimental set-up from the air.
Figure 1. A photograph of the experimental set-up from the air.
Agriculture 13 00639 g001
Figure 2. CO2 released rate during the aerobic and anaerobic stage. Control represents the soils or litter that were collected from the ambient atmospheric CO2 without warming; C represents the soils or litter that were collected from elevated CO2; T represents the soils or litter that were collected from plant canopy warming; CT represents the soils or litter that were collected from CO2 plus warming. The letters (AC) represent Experiment I, Experiment II and Experiment III, respectively. The inset represents the period of flooded incubation from Day 65 to Day 147.
Figure 2. CO2 released rate during the aerobic and anaerobic stage. Control represents the soils or litter that were collected from the ambient atmospheric CO2 without warming; C represents the soils or litter that were collected from elevated CO2; T represents the soils or litter that were collected from plant canopy warming; CT represents the soils or litter that were collected from CO2 plus warming. The letters (AC) represent Experiment I, Experiment II and Experiment III, respectively. The inset represents the period of flooded incubation from Day 65 to Day 147.
Agriculture 13 00639 g002
Figure 3. The cumulative CO2 emission during aerobic and anaerobic stage. Please refer to Table 1 for the treatment abbreviations. The letters (AC) represent Experiment I, Experiment II and Experiment III, respectively. Different lower-case letters indicate significant differences among treatments (p < 0.05).
Figure 3. The cumulative CO2 emission during aerobic and anaerobic stage. Please refer to Table 1 for the treatment abbreviations. The letters (AC) represent Experiment I, Experiment II and Experiment III, respectively. Different lower-case letters indicate significant differences among treatments (p < 0.05).
Agriculture 13 00639 g003
Table 1. Experimental design. Control represents the soils or litter that were collected from the ambient atmospheric CO2 without warming; C represents the soils or litter that were collected from elevated CO2; T represents the soils or litter that were collected from plant canopy warming; CT represents the soils or litter that were collected from CO2 plus warming.
Table 1. Experimental design. Control represents the soils or litter that were collected from the ambient atmospheric CO2 without warming; C represents the soils or litter that were collected from elevated CO2; T represents the soils or litter that were collected from plant canopy warming; CT represents the soils or litter that were collected from CO2 plus warming.
SoilsLittersAbbreviation
Experiment IControlControlS + L
CCSC + LC
TTST + LT
CTCTSCT + LCT
Experiment IIControlControlS + L
ControlCS + LC
ControlTS + LT
ControlCTS + LCT
Experiment IIIControlControlS + L
CControlSC + L
TControlST + L
CTControlSCT + L
Table 2. Nutrients concentration of plant litter under elevated CO2 and warming.
Table 2. Nutrients concentration of plant litter under elevated CO2 and warming.
TreatmentRice StrawWheat Straw
N (g·kg−1)P (g·kg−1)K (g·kg−1)N (g·kg−1)P (g·kg−1)K (g·kg−1)
Control10.59 ± 1.59 a1.06 ± 0.18 a16.70 ± 2.28 a9.28 ± 1.20 a1.11 ± 0.30 a15.87 ± 0.05 a
C8.84 ± 0.50 b0.90 ± 0.11 a14.90 ± 0.31 a5.60 ± 0.85 b0.67 ± 0.16 a11.56 ± 1.65 b
T11.42 ± 0.17 a0.97 ± 0.08 a16.69 ± 1.44 a6.94 ± 0.78 b0.89 ± 0.06 a7.47 ± 2.52 c
CT8.05 ± 0.71 b0.66 ± 0.03 b16.48 ± 0.54 a6.09 ± 0.65 b1.09 ± 0.29 a7.16 ± 1.98 c
Different lower-case letters indicate significant differences among treatments (p < 0.05).
Table 3. Person correlation between soil respiration during the aerobic period and soil characteristics.
Table 3. Person correlation between soil respiration during the aerobic period and soil characteristics.
Soil CharacteristicsSoil Respiration
(Experiment I)
Soil Respiration
(Experiment III)
Soil organic carbon0.4030.672 *
Dissolved organic carbon0.2590.586 *
Microbial biomass carbon−0.232−0.780 **
Microbial metabolic quotient0.831 **0.914 **
Soil pH0.175−0.284
Soil C/N0.676 *0.549
Soil available K0.4130.674 *
Soil available P−0.601 *−0.754 **
Total PLFAs0.045−0.125
Bacterial PLFAs−0.062−0.199
Fungal PLFAs0.135−0.037
F/B ratio0.631 *0.429
α-Glucosidase0.1380.311
β-Glucosidase0.2360.664 *
N-acetyl-glucosaminidase0.738 **0.426
Cellobiohydrolase−0.0420.441
β-Xylosidase−0.163−0.016
* indicates significance at 0.05; ** indicates significance at 0.01.
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.

Share and Cite

MDPI and ACS Style

Li, J.; Sun, B.; Liu, C.; Drosos, M.; Zhang, X.; Liu, X.; Li, L.; Pan, G. Legacy Effect of Long-Term Elevated CO2 and Warming on Soil Properties Controls Soil Organic Matter Decomposition. Agriculture 2023, 13, 639. https://doi.org/10.3390/agriculture13030639

AMA Style

Li J, Sun B, Liu C, Drosos M, Zhang X, Liu X, Li L, Pan G. Legacy Effect of Long-Term Elevated CO2 and Warming on Soil Properties Controls Soil Organic Matter Decomposition. Agriculture. 2023; 13(3):639. https://doi.org/10.3390/agriculture13030639

Chicago/Turabian Style

Li, Jie, Baobao Sun, Cheng Liu, Marios Drosos, Xuhui Zhang, Xiaoyu Liu, Lianqing Li, and Genxing Pan. 2023. "Legacy Effect of Long-Term Elevated CO2 and Warming on Soil Properties Controls Soil Organic Matter Decomposition" Agriculture 13, no. 3: 639. https://doi.org/10.3390/agriculture13030639

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop