Cover crops support the climate change mitigation potential of agroecosystems.

Cover crops have the potential to mitigate climate change by reducing negative impacts of agriculture on ecosystems. This study is first to quantify the net climate change mitigation impact of cover crops including land-use effects. A systematic literature and data review was conducted to identify major drivers for climate benefits and costs of cover crops in maize (Zea maize L.) production systems. The results indicate that cover crops lead to a net climate change mitigation impact (NCCMI) of 3.30 Mg CO2e ha-1 a-1. We created four scenarios with different impact weights of the drivers and all of them showing a positive NCCMI. Carbon land benefit, the carbon opportunity costs based on maize yield gains following cover crops, is the major contributor to the NCCMI (34.5% of all benefits). Carbon sequestration is the second largest contributor (33.8%). The climate costs of cover crops are mainly dominated by emissions from their seed production and foregone benefits due to land use for cover crops seeds. However, these two costs account for only 15.8% of the benefits. Extrapolating these results, planting cover crops before all maize acreage in the EU results in a climate change mitigation of 49.80 million Mg CO2e a-1, which is equivalent to 13.0% of the EU's agricultural emissions. This study highlights the importance of incorporating cover crops into sustainable cropping systems to minimize the agricultural impact to climate change.

Distinct metabolite classes in root exudates are indicative for field- or hydroponically-grown cover crops.

Introduction: Plants release a large variety of metabolites via their roots to shape physico-chemical soil properties and biological processes in the rhizosphere. While hydroponic growth conditions facilitate accessibility of the root system and recovery of root exudates, the natural soil environment can alter root metabolism and exudate secretion, raising the question to what extent the quantity and composition of root exudates released in hydroponic growth systems reflect those recovered from soil-grown roots. Methods: Using a root washing method, we sampled root exudates from four field-grown cover crop species with wide taxonomic distance, namely white mustard, lacy phacelia, bristle oat, and Egyptian clover. A set of primary metabolites and secondary metabolites were analysed in a targeted and untargeted LC-MS-based approach, respectively, for comparison with exudates obtained from hydroponically cultured plants. Results and discussion: We found that hydroponically cultivated plants released a larger amount of total carbon, but that the recovery of total carbon was not indicative for the diversity of metabolites in root exudates. In the field, root exudates from phacelia and clover contained 2.4 to 3.8 times more secondary metabolites, whereas carbon exudation in hydroponics was 5- to 4-fold higher. The composition of the set of metabolites identified using the untargeted approach was much more distinct among all species and growth conditions than that of quantified primary metabolites. Among secondary metabolite classes, the presence of lipids and lipid-like molecules was highly indicative for field samples, while the release of a large amount of phenylpropanoids, organoheterocyclic compounds or benzenoids was characteristic for clover, mustard or oat, respectively, irrespective of the cultivation condition. However, at the compound level the bulk of released metabolites was specific for cultivation conditions in every species, which implies that hydroponically sampled root exudates poorly reflect the metabolic complexity of root exudates recovered from field-grown plants.

Author Correction: Interspecific competition among catch crops modifies vertical root biomass distribution and nitrate scavenging in soils.

An amendment to this paper has been published and can be accessed via a link at the top of the paper.

Interspecific competition among catch crops modifies vertical root biomass distribution and nitrate scavenging in soils.

The potential of a plant species to acquire nutrients depends on its ability to explore the soil by its root system. Co-cultivation of different species is anticipated to lead to vertical root niche differentiation and thus to higher soil nutrient depletion. Using a qPCR-based method we quantified root biomass distribution of four catch crop species in vertical soil profiles in pure vs. mixed stands. Pure stands of mustard and phacelia robustly reached 70 cm soil depth, while oat preferably colonized upper soil layers, and clover developed the shallowest and smallest root system. Analysis of residual nitrate pools in different soil depths and correlation with root biomass showed that, besides rooting depth also root biomass determines soil nitrogen depletion. While occupying the same vertical niches as in pure stands, mustard and phacelia dominated total root biomass of the mix. In contrast, root biomass of clover and oat was severely suppressed in presence of the other species. Below-ground biomass profiling indicated low niche complementarity among the root systems of the examined species. Nonetheless, the mixture mostly overyielded root biomass of the pure stands and thus shows higher potential for efficient soil exploration by roots.

Microbial and abiotic controls on mineral-associated organic matter in soil profiles along an ecosystem gradient.

Formation of mineral-organic associations is a key process in the global carbon cycle. Recent concepts propose litter quality-controlled microbial assimilation and direct sorption processes as main factors in transferring carbon from plant litter into mineral-organic associations. We explored the pathways of the formation of mineral-associated organic matter (MOM) in soil profiles along a 120-ky ecosystem gradient that developed under humid climate from the retreating Franz Josef Glacier in New Zealand. We determined the stocks of particulate and mineral-associated carbon, the isotope signature and microbial decomposability of organic matter, and plant and microbial biomarkers (lignin phenols, amino sugars and acids) in MOM. Results revealed that litter quality had little effect on the accumulation of mineral-associated carbon and that plant-derived carbon bypassed microbial assimilation at all soil depths. Seemingly, MOM forms by sorption of microbial as well as plant-derived compounds to minerals. The MOM in carbon-saturated topsoil was characterized by the steady exchange of older for recent carbon, while subsoil MOM arises from retention of organic matter transported with percolating water. Overall, MOM formation is not monocausal but involves various mechanisms and processes, with reactive minerals being effective filters capable of erasing chemical differences in organic matter inputs.

A plant-microbe interaction framework explaining nutrient effects on primary production.

In most terrestrial ecosystems, plant growth is limited by nitrogen and phosphorus. Adding either nutrient to soil usually affects primary production, but their effects can be positive or negative. Here we provide a general stoichiometric framework for interpreting these contrasting effects. First, we identify nitrogen and phosphorus limitations on plants and soil microorganisms using their respective nitrogen to phosphorus critical ratios. Second, we use these ratios to show how soil microorganisms mediate the response of primary production to limiting and non-limiting nutrient addition along a wide gradient of soil nutrient availability. Using a meta-analysis of 51 factorial nitrogen-phosphorus fertilization experiments conducted across multiple ecosystems, we demonstrate that the response of primary production to nitrogen and phosphorus additions is accurately predicted by our stoichiometric framework. The only pattern that could not be predicted by our original framework suggests that nitrogen has not only a structural function in growing organisms, but also a key role in promoting plant and microbial nutrient acquisition. We conclude that this stoichiometric framework offers the most parsimonious way to interpret contrasting and, until now, unresolved responses of primary production to nutrient addition in terrestrial ecosystems.

Temperature response of permafrost soil carbon is attenuated by mineral protection.

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 14 C 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.

Plant-derived compounds stimulate the decomposition of organic matter in arctic permafrost soils.

Arctic ecosystems are warming rapidly, which is expected to promote soil organic matter (SOM) decomposition. In addition to the direct warming effect, decomposition can also be indirectly stimulated via increased plant productivity and plant-soil C allocation, and this so called "priming effect" might significantly alter the ecosystem C balance. In this study, we provide first mechanistic insights into the susceptibility of SOM decomposition in arctic permafrost soils to priming. By comparing 119 soils from four locations across the Siberian Arctic that cover all horizons of active layer and upper permafrost, we found that an increased availability of plant-derived organic C particularly stimulated decomposition in subsoil horizons where most of the arctic soil carbon is located. Considering the 1,035 Pg of arctic soil carbon, such an additional stimulation of decomposition beyond the direct temperature effect can accelerate net ecosystem C losses, and amplify the positive feedback to global warming.

Microbial nitrogen dynamics in organic and mineral soil horizons along a latitudinal transect in western Siberia.

Soil N availability is constrained by the breakdown of N-containing polymers such as proteins to oligopeptides and amino acids that can be taken up by plants and microorganisms. Excess N is released from microbial cells as ammonium (N mineralization), which in turn can serve as substrate for nitrification. According to stoichiometric theory, N mineralization and nitrification are expected to increase in relation to protein depolymerization with decreasing N limitation, and thus from higher to lower latitudes and from topsoils to subsoils. To test these hypotheses, we compared gross rates of protein depolymerization, N mineralization and nitrification (determined using 15N pool dilution assays) in organic topsoil, mineral topsoil, and mineral subsoil of seven ecosystems along a latitudinal transect in western Siberia, from tundra (67°N) to steppe (54°N). The investigated ecosystems differed strongly in N transformation rates, with highest protein depolymerization and N mineralization rates in middle and southern taiga. All N transformation rates decreased with soil depth following the decrease in organic matter content. Related to protein depolymerization, N mineralization and nitrification were significantly higher in mineral than in organic horizons, supporting a decrease in microbial N limitation with depth. In contrast, we did not find indications for a decrease in microbial N limitation from arctic to temperate ecosystems along the transect. Our findings thus challenge the perception of ubiquitous N limitation at high latitudes, but suggest a transition from N to C limitation of microorganisms with soil depth, even in high-latitude systems such as tundra and boreal forest. KEY POINTS: We compared soil N dynamics of seven ecosystems along a latitudinal transectShifts in N dynamics suggest a decrease in microbial N limitation with depthWe found no decrease in microbial N limitation from arctic to temperate zones.

Microbial community composition shapes enzyme patterns in topsoil and subsoil horizons along a latitudinal transect in Western Siberia.

Soil horizons below 30 cm depth contain about 60% of the organic carbon stored in soils. Although insight into the physical and chemical stabilization of soil organic matter (SOM) and into microbial community composition in these horizons is being gained, information on microbial functions of subsoil microbial communities and on associated microbially-mediated processes remains sparse. To identify possible controls on enzyme patterns, we correlated enzyme patterns with biotic and abiotic soil parameters, as well as with microbial community composition, estimated using phospholipid fatty acid profiles. Enzyme patterns (i.e. distance-matrixes calculated from these enzyme activities) were calculated from the activities of six extracellular enzymes (cellobiohydrolase, leucine-amino-peptidase, N-acetylglucosaminidase, chitotriosidase, phosphatase and phenoloxidase), which had been measured in soil samples from organic topsoil horizons, mineral topsoil horizons, and mineral subsoil horizons from seven ecosystems along a 1500 km latitudinal transect in Western Siberia. We found that hydrolytic enzyme activities decreased rapidly with depth, whereas oxidative enzyme activities in mineral horizons were as high as, or higher than in organic topsoil horizons. Enzyme patterns varied more strongly between ecosystems in mineral subsoil horizons than in organic topsoils. The enzyme patterns in topsoil horizons were correlated with SOM content (i.e., C and N content) and microbial community composition. In contrast, the enzyme patterns in mineral subsoil horizons were related to water content, soil pH and microbial community composition. The lack of correlation between enzyme patterns and SOM quantity in the mineral subsoils suggests that SOM chemistry, spatial separation or physical stabilization of SOM rather than SOM content might determine substrate availability for enzymatic breakdown. The correlation of microbial community composition and enzyme patterns in all horizons, suggests that microbial community composition shapes enzyme patterns and might act as a modifier for the usual dependency of decomposition rates on SOM content or C/N ratios.

Input of easily available organic C and N stimulates microbial decomposition of soil organic matter in arctic permafrost soil.

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.

Effects of soil organic matter properties and microbial community composition on enzyme activities in cryoturbated arctic soils.

Enzyme-mediated decomposition of soil organic matter (SOM) is controlled, amongst other factors, by organic matter properties and by the microbial decomposer community present. Since microbial community composition and SOM properties are often interrelated and both change with soil depth, the drivers of enzymatic decomposition are hard to dissect. We investigated soils from three regions in the Siberian Arctic, where carbon rich topsoil material has been incorporated into the subsoil (cryoturbation). We took advantage of this subduction to test if SOM properties shape microbial community composition, and to identify controls of both on enzyme activities. We found that microbial community composition (estimated by phospholipid fatty acid analysis), was similar in cryoturbated material and in surrounding subsoil, although carbon and nitrogen contents were similar in cryoturbated material and topsoils. This suggests that the microbial community in cryoturbated material was not well adapted to SOM properties. We also measured three potential enzyme activities (cellobiohydrolase, leucine-amino-peptidase and phenoloxidase) and used structural equation models (SEMs) to identify direct and indirect drivers of the three enzyme activities. The models included microbial community composition, carbon and nitrogen contents, clay content, water content, and pH. Models for regular horizons, excluding cryoturbated material, showed that all enzyme activities were mainly controlled by carbon or nitrogen. Microbial community composition had no effect. In contrast, models for cryoturbated material showed that enzyme activities were also related to microbial community composition. The additional control of microbial community composition could have restrained enzyme activities and furthermore decomposition in general. The functional decoupling of SOM properties and microbial community composition might thus be one of the reasons for low decomposition rates and the persistence of 400 Gt carbon stored in cryoturbated material.

Distinct microbial communities associated with buried soils in the Siberian tundra.

Cryoturbation, the burial of topsoil material into deeper soil horizons by repeated freeze-thaw events, is an important storage mechanism for soil organic matter (SOM) in permafrost-affected soils. Besides abiotic conditions, microbial community structure and the accessibility of SOM to the decomposer community are hypothesized to control SOM decomposition and thus have a crucial role in SOM accumulation in buried soils. We surveyed the microbial community structure in cryoturbated soils from nine soil profiles in the northeastern Siberian tundra using high-throughput sequencing and quantification of bacterial, archaeal and fungal marker genes. We found that bacterial abundances in buried topsoils were as high as in unburied topsoils. In contrast, fungal abundances decreased with depth and were significantly lower in buried than in unburied topsoils resulting in remarkably low fungal to bacterial ratios in buried topsoils. Fungal community profiling revealed an associated decrease in presumably ectomycorrhizal (ECM) fungi. The abiotic conditions (low to subzero temperatures, anoxia) and the reduced abundance of fungi likely provide a niche for bacterial, facultative anaerobic decomposers of SOM such as members of the Actinobacteria, which were found in significantly higher relative abundances in buried than in unburied topsoils. Our study expands the knowledge on the microbial community structure in soils of Northern latitude permafrost regions, and attributes the delayed decomposition of SOM in buried soils to specific microbial taxa, and particularly to a decrease in abundance and activity of ECM fungi, and to the extent to which bacterial decomposers are able to act as their functional substitutes.