globalchange  > 气候变化事实与影响
DOI: doi:10.1038/nclimate2580
论文题名:
Mineral protection of soil carbon counteracted by root exudates
作者: Marco Keiluweit
刊名: Nature Climate Change
ISSN: 1758-959X
EISSN: 1758-7079
出版年: 2015-03-30
卷: Volume:5, 页码:Pages:588;595 (2015)
语种: 英语
英文关键词: Biogeochemistry ; Climate-change impacts ; Ecosystem ecology ; Geochemistry
英文摘要:

Multiple lines of existing evidence suggest that climate change enhances root exudation of organic compounds into soils. Recent experimental studies show that increased exudate inputs may cause a net loss of soil carbon. This stimulation of microbial carbon mineralization (‘priming) is commonly rationalized by the assumption that exudates provide a readily bioavailable supply of energy for the decomposition of native soil carbon (co-metabolism). Here we show that an alternate mechanism can cause carbon loss of equal or greater magnitude. We find that a common root exudate, oxalic acid, promotes carbon loss by liberating organic compounds from protective associations with minerals. By enhancing microbial access to previously mineral-protected compounds, this indirect mechanism accelerated carbon loss more than simply increasing the supply of energetically more favourable substrates. Our results provide insights into the coupled biotic–abiotic mechanisms underlying the ‘priming phenomenon and challenge the assumption that mineral-associated carbon is protected from microbial cycling over millennial timescales.

Plants direct between 40–60% of photosynthetically fixed carbon (C) to roots and associated microorganisms via sloughed-off root cells, tissues, mucilage and a variety of exuded organic compounds1, 2. Elevated CO2 concentrations in the atmosphere are projected to increase the quantity3, 4 and alter the composition5, 6 of root exudates released into the soil. It seems less clear to what extent changing inputs will cause a net loss of native (or ‘old) organic C (ref. 7). A better understanding of the mechanism underlying soil C loss is pivotal in predicting how the large soil C stocks may respond to global change.

Exudate-induced soil C loss is commonly attributed to a ‘priming effect—that is, a short-term increase in microbial mineralization of native soil C as a result of fresh carbon inputs to the soil8. Although the process of ‘priming has received great attention in ecosystem sciences in recent years8, 9, our knowledge of the underlying mechanism is limited. It is often supposed that bioavailable exudate compounds induce greater microbial activity and enzyme production because they serve as ‘co-metabolites8, 10. Co-metabolism is defined as the mineralization of a non-growth substrate (for example, certain forms of native soil organic C) during growth of a microorganism on a bioavailable carbon and energy source (for example, exudate compounds)11. This mechanism is often invoked to increase the physiological potential of decomposers for the mineralization of native soil C (refs 8, 10) (Fig. 1a). However, as noted by Kuzyakov and co-workers12, direct experimental evidence in support of this mechanism is scarce because most studies have aimed at identifying ‘priming effects rather than the underlying mechanism.

Figure 1: Proposed mechanisms for the exudate-induced acceleration of the microbial mineralization of native carbon (‘priming effects) in the rhizosphere.
Proposed mechanisms for the exudate-induced acceleration of the microbial mineralization of native carbon (/`priming effects[rsquor]) in the rhizosphere.

a, The traditional view is that reduced exudate compounds (for example, simple sugars) stimulate microbial growth and activity via co-metabolism, and so increase the overall physiological potential of the decomposer community for carbon mineralization. Other factors such as the increased microbial demand for nitrogen or successional shifts in the community structure may also contribute to increased mineralization rates8, 12. b, The alternative mechanism proposed here takes into account that large quantities of soil C are inaccessible to microbes owing to associations with mineral phases. Root exudates that can act as ligands (for example, organic acids) effectively liberate C through complexation and dissolution reactions with protective mineral phases, thereby promoting its accessibility to microbes and accelerating its loss from the system through microbial mineralization. Microbial O2 consumption may further increase the accessibility of protected C by lowering the redox potential, Eh, and promoting reductive dissolution of SRO minerals.

We tested these hypotheses by delivering a continuous supply of individual exudate solutions through an artificial root (length = 10 cm, diameter = 2.5 mm) into unperturbed soil, recreating a rhizosphere environment (Supplementary Fig. 1). Exudates were supplied to a grassland soil (Supplementary Table 1) at root surface-normalized rates mimicking natural exudation rates of root tips (15 μmol C cm−2 d−1; refs 25, 26). For comparison, selected analyses were replicated with a forest soil. To distinguish exudate C from native soil C, individual exudate solutions were isotopically labelled with 13C (δ13C = 8,800‰). Exudate solutions or an inorganic nutrient solution (control) were provided over an incubation period of 35 days to replicate a burst in root growth at the onset of the growing season when the highest exudation rates are expected26. Compared to the control, all three exudate compounds induced visible physical gradients surrounding the artificial root after 7–10 days, which remained stable until the end of the experiment. In the oxalic acid treatment, these pronounced effects developed around the entire root and extended up to 5–10 mm into the soil (Fig. 2a), but in soils receiving glucose and acetic acid additions were limited to small patches around the root.

Figure 2: Exudate effects on artificial rhizosphere soil.
Exudate effects on artificial rhizosphere soil.

a, Photographs of the rhizosphere effect caused by oxalic acid addition and the control for comparison. White arrows indicate positions of the artificial root providing exudate solutions. b, O2 concentrations as a function of distance to the root for the different exudate treatments. Points represent mean ± s.e.m. (n = 2). Asterisks denote locations with mean O2 concentrations significantly lower than the control (one-way ANOVA, Tukeys ad hoc HSD test, p < 0.05). Solid lines represent model fits used to calculate microbial respiration based on Ficks first law of diffusion53. The inset shows volume-specific respiration rates in the rhizosphere for each exudate treatment. See Supplementary Information for details on fitting parameters and rate calculations.

To determine the effect of root exudates on microbial respiration rates in rhizosphere microsites, we used microsensors to record O2 profiles in the soil surrounding the root (Fig. 2b). These profiles showed that addition of oxalic acid significantly depleted O2 availability up to 5 mm into the surrounding soil (p < 0.05; Fig. 2b), whereas the effects of glucose and acetic acid additions were restricted to the first 1.5 mm. Across the entire rhizosphere zone (0–15 mm), microbial respiration rates followed a consistent pattern: oxalic acid > glucose > acetic acid (Fig. 2b, inset). To test whether this was a response specific to the grassland soil (silt-loam), we repeated the experiment with a forest soil (clay-loam) differing in texture and mineralogy (Supplementary Table 1) and observed the same result (Supplementary Fig. 1). Overall, microbial respiration in the oxalic acid treatment exceeded that of glucose by factors of ~1.6 (silt-loam) and ~2.8 (clay; Table 1).

We compared the stoichiometry of microbial carbon-use efficiency (CUE) and biochemical oxygen demand (BOD) of oxalic acid versus glucose mineralization pathways and found that oxalic acid addition accelerated the mineralization of native soil C more than glucose addition. Reported CUEs (the ratio of C assimilated into new biomass relative to the amount of C used in cellular respiration) for oxalic acid (5–25%) and glucose (40–70%) in soils27, 28, 29 indicate that the fraction of oxalic acid C released as CO2 (75–95%) is about twice that of glucose C (30–60%). Mineralization (that is, complete oxidation) of oxalic acid to CO2 requires 0.25 moles of O2 per unit C compared to 1 mole of O2 per unit C for glucose (Table 1). The BOD expected for the mineralization of each substrate is equal to:

The CUE and stoichiometric BOD values used are shown in Table 1. These calculations demonstrate that the BOD expected for microbial mineralization of oxalic acid should be only half the value associated with glucose mineralization (Table 1). Because our measured respiration rates show the opposite trend, we conclude that mineralization of other, more reduced (non-exudate) soil C must have accounted for at least 50% of the respiration observed in the oxalate treatment.

In line with accelerated mineralization of native soil C, soils receiving oxalic acid additions experienced a net C loss in the zone closest to the root (p < 0.05; Fig. 3a). In contrast, addition of the energetically more favourable substrates glucose and acetic acid resulted in a pronounced increase in total soil C content (Fig. 3a). This net C accumulation, possibly due to an increase in microbial biomass C caused by microbial assimilation of these exudates, was not counterbalanced by concurrent increases in the mineralization of native C.

Figure 3: Exudate-induced effects on total soil C and protective mineral phases.
Exudate-induced effects on total soil C and protective mineral phases.

a, Relative changes in total soil C. b, Fe and Al bound in metal–organic complexes (MOCs) and short-range order (SRO) phases presented as a function of distance to the root. Treatment effects were calculated as the percentage difference between concentrations in treatment and control samples for each distance. Positive values indicate a treatment-induced pool increase, whereas negative values indicate a pool decrease. Asterisks denote pool sizes significantly different from the control (one-way ANOVA, Tukeys ad hoc HSD, p < 0.05). Values are shown as means ± s.e.m. (n = 2). Data shown for silt-loam grassland soils only. Changes in metal pools of the clay-rich forest soil can be found in Supplementary Fig. 6.

To test whether disruptions of protective mineral–organic associations are responsible for the ‘priming effect we observed, sequential extractions targeting MOC and SRO phases were performed (Fig. 3b). Compared to the control, oxalic acid addition significantly decreased concentrations of Fe and Al phases up to 12 mm into the soil (p < 0.05). Specifically, Fe and Al in MOCs decreased with increasing proximity to the root, paralleled by a notable decline of Fe in SRO phases. Acetic acid exudates also significantly reduced the amount of Fe and Al in MOCs in the zone closest to the root (p < 0.05), whereas glucose showed no measurable effect. There were no significant responses of more crystalline pools to the exudate treatments. Complementary batch experiments showed that oxalic acid caused greater mobilization of Fe and Al after a short incubation of 1 h than after a prolonged incubation period (48 h; Supplementary Table 10); glucose showed no such effect. We infer that, in our system, physiological levels of oxalic acid disrupt mineral–organic associations via an immediate, abiotic mechanism rather than slower, microbially mediated processes. This mechanism is more effective for mineral–organic associations formed by amorphous MOCs than for such that are composed of more crystalline SRO phases—a result consistent with observations of stronger ‘priming effects (that is, accelerated mineralization of native soil C) in soils dominated by amorphous MOCs than in soils characterized by more crystalline metal oxides phases19.

We further examined the concentration and speciation of pore water C and metals as a test for the liberation of mineral-bound organic C (Supplementary Table 6). In the near-root zone (0–4 mm), oxalic acid addition increased pore water C concentrations by a factor of ~8 compared to the control, whereas acetic acid and glucose additions affected C concentrations by factors of only ~2.5 and ~1, respectively. This increase in dissolved C in the pore water correlated with increases in dissolved Fe (R2 = 0.98) and Al (R2 = 0.95; Fig. 4a and Supplementary Table 6). The bulk chemical composition of organic C in the pore water was determined by laser desorption post ionization mass spectrometry (LDPI-MS), a method that is particularly sensitive for lignin-derived compounds38. Mass spectra of pore water from the oxalic acid treatment showed a notably greater abundance of high mass-to-charge peaks (m/z = 250 to 500) relative to the other treatments (Supplementary Fig. 4). These mass peaks can be attributed to aromatic dimers based on the relatively low ionization energy of aromatic compounds39 and peak patterns resembling those of lignin in soils38. These results support the hypothesis that oxalic acid addition chemically disrupted MOCs and SRO mineral phases in the rhizosphere (Fig. 3b) and increased pore water concentrations of C and metals more than either glucose or acetic acid (Fig. 4a). Oxalic acid additions seem to increase microbial access to C in the pore water via this mechanism.

Figure 4: Exudate effect on metal–organic associations in the pore water.
Exudate effect on metal-organic associations in the pore water.

a, C mobilization into the pore water in relation to dissolved Fe concentrations. b, Ca and Fe associated with dissolved organic C collected from control and oxalic acid treatments. Maps are generated as difference maps of two image scans collected above and below the respective absorption edge energies. c, Carbon K-edge NEXAFS spectra of pore water C. Spectra of discrete regions of interest are shown as dotted lines, with the blue lines and shaded areas representing mean and standard deviation, respectively. The numbers of regions analysed was glucose, acetic acid and oxalic acid were 8, 9 and 10, respectively, with 9 regions for the control. Data shown for silt-loam grassland soils only. Carbon NEXAFS spectra for clay-rich forest soil (Supplementary Fig. 5) and details on the STXM maps can be found in the Supplementary Information.

As detailed above, we expected that an energetically more favourable root exudate such as glucose should cause a greater ‘priming effect than a less attractive one such as oxalic acid (Fig. 1a). However, the inverse was observed: by improving the accessibility of C previously protected in mineral–organic associations, oxalic acid induced a much stronger ‘priming effect than glucose and acetic acid. Rather than via co-metabolism, organic ligands with metal-complexing abilities accelerate microbial mineralization of C in the rhizosphere via an indirect, multipart mechanism (Fig. 1b). Organic ligands released into the rhizosphere (i) mobilize mineral-bound C through complexation and dissolution of SRO phases and/or (ii) solubilize organic compounds through the removal of crosslinking metal cations from MOCs. Release from SRO or MOC phases promotes the accessibility of organic compounds to microbes. Increased microbial access subsequently (iii) stimulates microbial mineralization and shifts the community structure towards phyla adapted to soil environments with greater accessibility of C. On the basis of these results, we conclude that ‘priming effects are not a purely biotic phenomenon and should be viewed as the sum of direct biotic co-metabolic (Fig. 1a) and indirect C mobilization (Fig. 1b) mechanisms. We suggest that future investigations into the causes of ‘priming effects consider both mechanisms simultaneously and focus on quantifying their relative contributions in different soil ecosystems.

In our study, oxalic acid disrupted mineral–organic associations in both grassland and forest soils. This observation is consistent with root-induced weathering of protective mineral phases during periods of rapid root growth in arable44 and forest soils45, and highlights the general nature of the proposed mechanism. To estimate the importance of the proposed mechanism at the ecosystem-scale, we calculated the potential C loss that may be attributed to this mobilization mechanism in a forest ecosystem. The oxalic acid treatment resulted in an overall C loss of ~4% over our experimental period. If we assume that the total amount of exudate C released into the soil in our experiments is comparable to that released over the course of an annual burst of root growth in times of high primary productivity26, and organic acids comprise up to ~25% of the mixture of compounds exuded over that time frame24, the annual soil C loss is estimated to be ~1% C yr−1. By comparison, Richter et al.46 found that soil C in deep mineral horizons, where C accessibility is probably low owing to mineral–organic associations, is rapidly mineralized on reforestation and expansion of the rooting zone. In that study, the average loss over four decades of reforestation was approximately 1.08% C yr−1—a rate strikingly close to the value in our experiment. Although simple, our calculation highlights the potential impact of the proposed ‘priming mechanism on mineral-protected C at an ecosystem level.

Conceptual frameworks of soil organic matter stabilization have long considered C in mineral–organic associations permanently inaccessible to microbes, and thus protected from loss processes for millennia or longer13, 14, 18. But this paradigm is shifting, and many now recognize that any natural organic compound can be decomposed when the required resources are

URL: http://www.nature.com/nclimate/journal/v5/n6/full/nclimate2580.html
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资源类型: 期刊论文
标识符: http://119.78.100.158/handle/2HF3EXSE/4787
Appears in Collections:气候变化事实与影响
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气候变化与战略

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Marco Keiluweit. Mineral protection of soil carbon counteracted by root exudates[J]. Nature Climate Change,2015-03-30,Volume:5:Pages:588;595 (2015).
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