Minerals in the rhizosphere Jilling, Andrea; Keiluweit, Marco; Contosta, Alexandra R. ...
Biogeochemistry,
07/2018, Volume:
139, Issue:
2
Journal Article
Peer reviewed
Open access
Despite decades of research progress, ecologists are still debating which pools and fluxes provide nitrogen (N) to plants and soil microbes across different ecosystems. Depolymerization of soil ...organic N is recognized as the rate-limiting step in the production of bioavailable N, and it is generally assumed that detrital N is the main source. However, in many mineral soils, detrital polymers constitute a minor fraction of total soil organic N. The majority of organic N is associated with clay-sized particles where physicochemical interactions may limit the accessibility of N-containing compounds. Although mineral-associated organic matter (MAOM) has historically been considered a critical, but relatively passive, reservoir of soil N, a growing body of research now points to the dynamic nature of mineral-organic associations and their potential for destabilization. Here we synthesize evidence from biogeoscience and soil ecology to demonstrate how MAOM is an important, yet overlooked, mediator of bioavailable N, especially in the rhizosphere. We highlight several biochemical strategies that enable plants and microbes to disrupt mineral-organic interactions and access MAOM. In particular, root-deposited low-molecular-weight exudates may enhance the mobilization and solubilization of MAOM, increasing its bioavailability. However, the competitive balance between the possible fates of N monomers—bound to mineral surfaces versus dissolved and available for assimilation—will depend on the specific interaction between mineral properties, soil solution, mineral-bound organic matter, and microbes. Building off our emerging understanding of MAOM as a source of bioavailable N, we propose a revision of the Schimel and Bennett (Ecology 85:591–602, 2004) model (which emphasizes N depolymerization), by incorporating MAOM as a potential proximal mediator of bioavailable N.
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DOBA, EMUNI, FZAB, GEOZS, IJS, IMTLJ, IZUM, KILJ, KISLJ, MFDPS, NUK, OBVAL, OILJ, PILJ, PNG, SAZU, SBCE, SBJE, SBMB, SBNM, UILJ, UKNU, UL, UM, UPUK, VKSCE, ZAGLJ
Rising temperatures enhance microbial decomposition of soil organic matter (SOM) and thereby increase the soil CO2 efflux. Elevated decomposition rates might differently affect distinct SOM pools, ...depending on their stability and accessibility. Soil fractions derived from density fractionation have been suggested to represent SOM pools with different turnover times and stability against microbial decomposition.
To investigate the effect of soil warming on functionally different soil organic matter pools, we here investigated the chemical and isotopic composition of bulk soil and three density fractions (free particulate organic matter, fPOM; occluded particulate organic matter, oPOM; and mineral associated organic matter, MaOM) of a C-rich soil from a long-term warming experiment in a spruce forest in the Austrian Alps. At the time of sampling, the soil in this experiment had been warmed during the snow-free period for seven consecutive years. During that time no thermal adaptation of the microbial community could be identified and CO2 release from the soil continued to be elevated by the warming treatment. Our results, which included organic carbon content, total nitrogen content, δ13C, Δ14C, δ15N and the chemical composition, identified by pyrolysis-GC/MS, showed no significant differences in bulk soil between warming treatment and control. Surprisingly, the differences in the three density fractions were mostly small and the direction of warming induced change was variable with fraction and soil depth. Warming led to reduced N content in topsoil oPOM and subsoil fPOM and to reduced relative abundance of N-bearing compounds in subsoil MaOM. Further, warming increased the δ13C of MaOM at both sampling depths, reduced the relative abundance of carbohydrates while it increased the relative abundance of lignins in subsoil oPOM. As the size of the functionally different SOM pools did not significantly change, we assume that the few and small modifications in SOM chemistry result from an interplay of enhanced microbial decomposition of SOM and increased root litter input in the warmed plots. Overall, stable functional SOM pool sizes indicate that soil warming had similarly affected easily decomposable and stabilized SOM of this C-rich forest soil.
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•Soil warming had little effect on organic matter chemistry of all density fractions.•Changes in chemistry depended on sampling depth and fraction.•All density fractions might have been similarly affected by soil warming.•Increased root turnover might have masked enhanced microbial decomposition.
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GEOZS, IJS, IMTLJ, KILJ, KISLJ, NUK, OILJ, PNG, SAZU, SBCE, SBJE, UL, UM, UPCLJ, UPUK, ZRSKP
A longstanding assumption of glucose tracing experiments is that all glucose is microbially utilized during short incubations of ≤2 days to become microbial biomass or carbon dioxide. Carbon use ...efficiency (CUE) estimates have consequently ignored the formation of residues (non-living microbial products) although such materials could represent an important sink of glucose that is prone to stabilization as soil organic matter. We examined the dynamics of microbial residue formation from a short tracer experiment with frequent samplings over 72 h, and conducted a meta-analysis of previously published glucose tracing studies to assess the generality of these experimental results. Both our experiment and metaanalysis indicated 30–34% of amended glucose-C (¹³Cor ¹⁴C) was in the form of residues within the first 6 h of substrate addition. We expand the conventional efficiency calculation to include residues in both the numerator and denominator of efficiency, thereby deriving a novel metric of the potential persistence of glucose-C in soil as living microbial biomass plus residues (‘carbon stabilization efficiency’). This new metric indicates nearly 40% of amended glucose-C persists in soil 180 days after amendment, the majority as non-biomass residues. Starting microbial biomass and clay content emerge as critical factors that positively promote such long term stabilization of labile C. Rapid residue production supports the conclusion that non-growth maintenance activity can illicit high demands for C in soil, perhaps equaling that directed towards growth, and that residues may have an underestimated role in the cycling and sequestration potential of C in soil.
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DOBA, EMUNI, FZAB, GEOZS, IJS, IMTLJ, IZUM, KILJ, KISLJ, MFDPS, NUK, OBVAL, OILJ, PILJ, PNG, SAZU, SBCE, SBJE, SBMB, SBNM, UILJ, UKNU, UL, UM, UPUK, VKSCE, ZAGLJ
Microbial nitrogen use efficiency (NUE) describes the partitioning of organic N taken up between growth and the release of inorganic N to the environment (that is, N mineralization), and is thus ...central to our understanding of N cycling. Here we report empirical evidence that microbial decomposer communities in soil and plant litter regulate their NUE. We find that microbes retain most immobilized organic N (high NUE), when they are N limited, resulting in low N mineralization. However, when the metabolic control of microbial decomposers switches from N to C limitation, they release an increasing fraction of organic N as ammonium (low NUE). We conclude that the regulation of NUE is an essential strategy of microbial communities to cope with resource imbalances, independent of the regulation of microbial carbon use efficiency, with significant effects on terrestrial N cycling.
Resource stoichiometry (C:N:P) is an important determinant of litter decomposition. However, the effect of elemental stoichiometry on the gross rates of microbial N and P cycling processes during ...litter decomposition is unknown. In a mesocosm experiment, beech (
Fagus sylvatica
L.) litter with natural differences in elemental stoichiometry (C:N:P) was incubated under constant environmental conditions. After three and six months, we measured various aspects of nitrogen and phosphorus cycling. We found that gross protein depolymerization, N mineralization (ammonification), and nitrification rates were negatively related to litter C:N. Rates of P mineralization were negatively correlated with litter C:P. The negative correlations with litter C:N were stronger for inorganic N cycling processes than for gross protein depolymerization, indicating that the effect of resource stoichiometry on intracellular processes was stronger than on processes catalyzed by extracellular enzymes. Consistent with this, extracellular protein depolymerization was mainly limited by substrate availability and less so by the amount of protease. Strong positive correlations between the interconnected N and P pools and the respective production and consumption processes pointed to feed-forward control of microbial litter N and P cycling. A negative relationship between litter C:N and phosphatase activity (and between litter C:P and protease activity) demonstrated that microbes tended to allocate carbon and nutrients in ample supply into the production of extracellular enzymes to mine for the nutrient that is more limiting. Overall, the study demonstrated a strong effect of litter stoichiometry (C:N:P) on gross processes of microbial N and P cycling in decomposing litter; mineralization of N and P were tightly coupled to assist in maintaining cellular homeostasis of litter microbial communities.
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BFBNIB, FZAB, GIS, IJS, INZLJ, KILJ, NLZOH, NMLJ, NUK, OILJ, PNG, SAZU, SBCE, SBMB, UL, UM, UPUK, ZRSKP
Rising temperatures in the Arctic can affect soil organic matter (SOM) decomposition directly and indirectly, by increasing plant primary production and thus the allocation of plant-derived organic ...compounds into the soil. Such compounds, for example root exudates or decaying fine roots, are easily available for microorganisms, and can alter the decomposition of older SOM (“priming effect”). We here report on a SOM priming experiment in the active layer of a permafrost soil from the central Siberian Arctic, comparing responses of organic topsoil, mineral subsoil, and cryoturbated subsoil material (i.e., poorly decomposed topsoil material subducted into the subsoil by freeze–thaw processes) to additions of 13C-labeled glucose, cellulose, a mixture of amino acids, and protein (added at levels corresponding to approximately 1% of soil organic carbon). SOM decomposition in the topsoil was barely affected by higher availability of organic compounds, whereas SOM decomposition in both subsoil horizons responded strongly. In the mineral subsoil, SOM decomposition increased by a factor of two to three after any substrate addition (glucose, cellulose, amino acids, protein), suggesting that the microbial decomposer community was limited in energy to break down more complex components of SOM. In the cryoturbated horizon, SOM decomposition increased by a factor of two after addition of amino acids or protein, but was not significantly affected by glucose or cellulose, indicating nitrogen rather than energy limitation. Since the stimulation of SOM decomposition in cryoturbated material was not connected to microbial growth or to a change in microbial community composition, the additional nitrogen was likely invested in the production of extracellular enzymes required for SOM decomposition. Our findings provide a first mechanistic understanding of priming in permafrost soils and suggest that an increase in the availability of organic carbon or nitrogen, e.g., by increased plant productivity, can change the decomposition of SOM stored in deeper layers of permafrost soils, with possible repercussions on the global climate.
•We tested the response of decomposition in arctic soils to organic matter input.•Decomposition rates in organic topsoil were hardly affected by substrate additions.•Decomposition rates in mineral subsoil doubled after addition of organic C.•Decomposition rates of cryoturbated material doubled after addition of organic N.•Arctic C stocks might be diminished by increased C and N availability with warming.
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GEOZS, IJS, IMTLJ, KILJ, KISLJ, NUK, OILJ, PNG, SAZU, SBCE, SBJE, UL, UM, UPCLJ, UPUK
Climate change in Arctic ecosystems fosters permafrost thaw and makes massive amounts of ancient soil organic carbon (OC) available to microbial breakdown. However, fractions of the organic matter ...(OM) may be protected from rapid decomposition by their association with minerals. Little is known about the effects of mineral‐organic associations (MOA) on the microbial accessibility of OM in permafrost soils and it is not clear which factors control its temperature sensitivity. In order to investigate if and how permafrost soil OC turnover is affected by mineral controls, the heavy fraction (HF) representing mostly MOA was obtained by density fractionation from 27 permafrost soil profiles of the Siberian Arctic. In parallel laboratory incubations, the unfractionated soils (bulk) and their HF were comparatively incubated for 175 days at 5 and 15°C. The HF was equivalent to 70 ± 9% of the bulk CO2 respiration as compared to a share of 63 ± 1% of bulk OC that was stored in the HF. Significant reduction of OC mineralization was found in all treatments with increasing OC content of the HF (HF‐OC), clay‐size minerals and Fe or Al oxyhydroxides. Temperature sensitivity (Q10) decreased with increasing soil depth from 2.4 to 1.4 in the bulk soil and from 2.9 to 1.5 in the HF. A concurrent increase in the metal‐to‐HF‐OC ratios with soil depth suggests a stronger bonding of OM to minerals in the subsoil. There, the younger 14C signature in CO2 than that of the OC indicates a preferential decomposition of the more recent OM and the existence of a MOA fraction with limited access of OM to decomposers. These results indicate strong mineral controls on the decomposability of OM after permafrost thaw and on its temperature sensitivity. Thus, we here provide evidence that OM temperature sensitivity can be attenuated by MOA in permafrost soils.
The study investigated the temperature sensitivity of organic carbon in Siberian permafrost soils. The results showed that although substantial amounts of soil organic carbon are prone to degradation under rising global temperatures, strong mineral controls affect the temperature sensitivity of organic carbon mineralization. We here provide evidence that OM temperature sensitivity can be attenuated by mineral‐organic associations in permafrost soil.
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BFBNIB, FZAB, GIS, IJS, KILJ, NLZOH, NUK, OILJ, SBCE, SBMB, UL, UM, UPUK
One of the biggest environmental challenges facing agriculture is how to both supply and retain nitrogen (N), especially as precipitation becomes more variable with climate change. We used a ...greenhouse experiment to assess how contrasting histories of crop rotational complexity affect plant-soil-microbe interactions that govern N processes, including during water stress. With higher levels of carbon and N cycling hydrolytic enzymes, higher mineral-associated organic matter N concentrations, and an altered microbial community, soils from the most complex rotation enabled 80% more corn N uptake under two moisture regimes, compared to soil from monoculture corn. Higher levels of plant N likely drove the changes in corn leaf gas exchange, particularly increasing intrinsic water use efficiency by 9% in the most complex rotation. The water deficit increased the standing pool of nitrate 44-fold in soils with a history of complex crop rotations, compared to an 11-fold increase in soils from the corn monoculture. The implications of this difference must be considered in a whole cropping systems and field context. Cycling of 15N-labeled fresh clover residue into soil N pools did not depend on the water regime or rotation history, with 2-fold higher recovery in the mineral vs. particulate organic N pool. In contrast, the water deficit reduced recovery of clover 15N in corn shoots by 37%, showing greater impacts of water deficit on plant N uptake compared to organic N cycling in soil. This study provides direct experimental evidence that long-term crop rotational complexity influences microbial N cycling and availability with feedbacks to plant physiology. Collectively, these results could help explain general observations of higher yields in more complex crop rotations, including specifically during dry conditions.
•Complex rotations increased soil hydrolytic enzyme activities, MAOM-N.•PLFA profiles were distinct in soils with history of simplified vs. complex rotations.•Crop N uptake—and N content—increased with soil's history of rotational complexity.•Rotational complexity increased corn's water use efficiency even during water deficit.•Higher nitrate remained in soil with complex rotation history after water deficit.
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GEOZS, IJS, IMTLJ, KILJ, KISLJ, NLZOH, NUK, OILJ, PNG, SAZU, SBCE, SBJE, UILJ, UL, UM, UPCLJ, UPUK, ZAGLJ, ZRSKP
Soil microbial growth, respiration, and carbon (C) use efficiency (CUE) are essential parameters to understand, describe and model the soil carbon cycle. While seasonal dynamics of microbial ...respiration are well studied, little is known about how microbial growth and CUE change over the course of a year, especially outside the plant growing season. In this study, we measured soil microbial respiration, gross growth via 18O incorporation into DNA, and biomass in an agricultural field and a deciduous forest 16 times over the course of two years. We sampled soils to a depth of 5 cm from plots at which harvest residues or leaf litter remained on the plot or was removed. We observed strong seasonal variations of microbial respiration, growth, and biomass. All these microbial parameters were significantly higher at the forest site, which contained 4.3 % organic C compared to the agricultural site with 0.9 % organic C. CUE also varied strongly (0.1 to 0.7) but was overall significantly higher at the agricultural site compared to the forest site. We found that microbial respiration and to a lesser extent microbial growth followed the seasonal dynamics of soil temperature. Microbial growth was further affected by the presence of plants in the agricultural system or foliage in the forest. At low temperatures in winter, both microbial respiration and gross growth showed the lowest rates, whereas CUE (calculated from both respiration and growth) showed amongst the highest values determined during the two years, due to the higher temperature sensitivity of microbial respiration. Microbial biomass C strongly increased in winter. Surprisingly, this winter peak was not connected to high microbial growth or an increase in DNA content. This suggests that microorganisms accumulated C and N, potentially in the form of osmo- or cryoprotectants or increased in cell size but did not divide. This microbial winter bloom and following decline, where C is released from microbial biomass and freely available, might constitute a highly dynamic time in the annual C cycle in temperate soil systems. Highly variable CUE, which was observed in our study, and the fact that CUE is calculated from independently controlled microbial respiration and microbial growth, ask for great caution when CUE is used to describe soil microbial physiology, soil C dynamics or C sequestration. Instead, microbial respiration, microbial growth, and microbial biomass C should be investigated individually in combination to better understand the soil C cycle.
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GEOZS, IJS, IMTLJ, KILJ, KISLJ, NLZOH, NUK, OILJ, PNG, SAZU, SBCE, SBJE, UILJ, UL, UM, UPCLJ, UPUK, ZAGLJ, ZRSKP
Plant seasonal cycles alter carbon (C) and nitrogen (N) availability for soil microbes, which may affect microbial community composition and thus feed back on microbial decomposition of soil organic ...material and plant N availability. The temporal dynamics of these plant-soil interactions are, however, unclear. Here, we experimentally manipulated the C and N availability in a beech forest through N fertilization or tree girdling and conducted a detailed analysis of the seasonal pattern of microbial community composition and decomposition processes over 2 yr. We found a strong relationship between microbial community composition and enzyme activities over the seasonal course. Phenoloxidase and peroxidase activities were highest during late summer, whereas cellulase and protease peaked in late autumn. Girdling, and thus loss of mycorrhiza, resulted in an increase in soil organic matter-degrading enzymes and a decrease in cellulase and protease activity. Temporal changes in enzyme activities suggest a switch of the main substrate for decomposition between summer (soil organic matter) and autumn (plant litter). Our results indicate that ectomycorrhizal fungi are possibly involved in autumn cellulase and protease activity. Our study shows that, through belowground C allocation, trees significantly alter soil microbial communities, which may affect seasonal patterns of decomposition processes.
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BFBNIB, FZAB, GIS, IJS, KILJ, NLZOH, NMLJ, NUK, OILJ, PNG, SAZU, SBCE, SBMB, UL, UM, UPUK
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