Mycorrhizal type and tree diversity affect foliar elemental pools and stoichiometry.

Species-specific differences in nutrient acquisition strategies allow for complementary use of resources among plants in mixtures, which may be further shaped by mycorrhizal associations. However, empirical evidence of this potential role of mycorrhizae is scarce, particularly for tree communities. We investigated the impact of tree species richness and mycorrhizal types, arbuscular mycorrhizal fungi (AM) and ectomycorrhizal fungi (EM), on above- and belowground carbon (C), nitrogen (N), and phosphorus (P) dynamics. Soil and soil microbial biomass elemental dynamics showed weak responses to tree species richness and none to mycorrhizal type. However, foliar elemental concentrations, stoichiometry, and pools were significantly affected by both treatments. Tree species richness increased foliar C and P pools but not N pools. Additive partitioning analyses showed that net biodiversity effects of foliar C, N, P pools in EM tree communities were driven by selection effects, but in mixtures of both mycorrhizal types by complementarity effects. Furthermore, increased tree species richness reduced soil nitrate availability, over 2 yr. Our results indicate that positive effects of tree diversity on aboveground nutrient storage are mediated by complementary mycorrhizal strategies and highlight the importance of using mixtures composed of tree species with different types of mycorrhizae to achieve more multifunctional afforestation.

Not all soil carbon is created equal: Labile and stable pools under nitrogen input.

Anthropogenic activities have raised nitrogen (N) input worldwide with profound implications for soil carbon (C) cycling in ecosystems. The specific impacts of N input on soil organic matter (SOM) pools differing in microbial availability remain debatable. For the first time, we used a much-improved approach by effectively combining the 13C natural abundance in SOM with 21 years of C3-C4 vegetation conversion and long-term incubation. This allows to distinguish the impact of N input on SOM pools with various turnover times. We found that N input reduced the mineralization of all SOM pools, with labile pools having greater sensitivity to N than stable ones. The suppression in SOM mineralization was notably higher in the very labile pool (18%-52%) than the labile and stable (11%-47%) and the very stable pool (3%-21%) compared to that in the unfertilized control soil. The very labile C pool made a strong contribution (up to 60%) to total CO2 release and also contributed to 74%-96% of suppressed CO2 with N input. This suppression of SOM mineralization by N was initially attributed to the decreased microbial biomass and soil functions. Over the long-term, the shift in bacterial community toward Proteobacteria and reduction in functional genes for labile C degradation were the primary drivers. In conclusion, the higher the availability of the SOM pools, the stronger the suppression of their mineralization by N input. Labile SOM pools are highly sensitive to N availability and may hold a greater potential for C sequestration under N input at global scale.

New perspectives on microbiome and nutrient sequestration in soil aggregates during long-term grazing exclusion.

Grazing exclusion alters grassland soil aggregation, microbiome composition, and biogeochemical processes. However, the long-term effects of grazing exclusion on the microbial communities and nutrient dynamics within soil aggregates remain unclear. We conducted a 36-year exclusion experiment to investigate how grazing exclusion affects the soil microbial community and the associated soil functions within soil aggregates in a semiarid grassland. Long-term (36 years) grazing exclusion induced a shift in microbial communities, especially in the <2 mm aggregates, from high to low diversity compared to the grazing control. The reduced microbial diversity was accompanied by instability of fungal communities, extended distribution of fungal pathogens to >2 mm aggregates, and reduced carbon (C) sequestration potential thus revealing a negative impact of long-term GE. In contrast, 11-26 years of grazing exclusion greatly increased C sequestration and promoted nutrient cycling in soil aggregates and associated microbial functional genes. Moreover, the environmental characteristics of microhabitats (e.g., soil pH) altered the soil microbiome and strongly contributed to C sequestration. Our findings reveal new evidence from soil microbiology for optimizing grazing exclusion duration to maintain multiple belowground ecosystem functions, providing promising suggestions for climate-smart and resource-efficient grasslands.

Compatibility of X-ray computed tomography with plant gene expression, rhizosphere bacterial communities and enzyme activities.

Non-invasive X-ray computed tomography (XRCT) is increasingly used in rhizosphere research to visualize development of soil-root interfaces in situ. However, exposing living systems to X-rays can potentially impact their processes and metabolites. In order to evaluate these effects, we assessed the responses of rhizosphere processes 1 and 24 h after a low X-ray exposure (0.81 Gy). Changes in root gene expression patterns occurred 1 h after exposure with down-regulation of cell wall-, lipid metabolism-, and cell stress-related genes, but no differences remained after 24 h. At either time point, XRCT did not affect either root antioxidative enzyme activities or the composition of the rhizosphere bacterial microbiome and microbial growth parameters. The potential activities of leucine aminopeptidase and phosphomonoesterase were lower at 1 h, but did not differ from the control 24 h after exposure. A time delay of 24 h after a low X-ray exposure (0.81 Gy) was sufficient to reverse any effects on the observed rhizosphere systems. Our data suggest that before implementing novel experimental designs involving XRCT, a study on its impact on the investigated processes should be conducted.

Labile carbon retention compensates for CO2 released by priming in forest soils.

Increase of belowground C allocation by plants under global warming or elevated CO2 may promote decomposition of soil organic carbon (SOC) by priming and strongly affects SOC dynamics. The specific effects by priming of SOC depend on the amount and frequency of C inputs. Most previous priming studies have investigated single C additions, but they are not very representative for litterfall and root exudation in many terrestrial ecosystems. We evaluated effects of (13)C-labeled glucose added to soil in three temporal patterns: single, repeated, and continuous on dynamics of CO2 and priming of SOC decomposition over 6 months. Total and (13)C labeled CO2 were monitored to analyze priming dynamics and net C balance between SOC loss caused by priming and the retention of added glucose-C. Cumulative priming ranged from 1.3 to 5.5 mg C g(-1) SOC in the subtropical, and from -0.6 to 5.5 mg C g(-1) SOC in the tropical soils. Single addition induced more priming than repeated and continuous inputs. Therefore, single additions of high substrate amounts may overestimate priming effects over the short term. The amount of added glucose C remaining in soil after 6 months (subtropical: 8.1-11.2 mg C g(-1) SOC or 41-56% of added glucose; tropical: 8.7-15.0 mg C g(-1) SOC or 43-75% of glucose) was substantially higher than the net C loss due to SOC decomposition including priming effect. This overcompensation of C losses was highest with continuous inputs and lowest with single inputs. Therefore, raised labile organic C input to soils by higher plant productivity will increase SOC content even though priming accelerates decomposition of native SOC. Consequently, higher continuous input of C belowground by plants under warming or elevated CO2 can increase C stocks in soil despite accelerated C cycling by priming in soils.

Soil C and N availability determine the priming effect: microbial N mining and stoichiometric decomposition theories.

The increasing input of anthropogenically derived nitrogen (N) to ecosystems raises a crucial question: how does available N modify the decomposer community and thus affects the mineralization of soil organic matter (SOM). Moreover, N input modifies the priming effect (PE), that is, the effect of fresh organics on the microbial decomposition of SOM. We studied the interactive effects of C and N on SOM mineralization (by natural (13) C labelling adding C4 -sucrose or C4 -maize straw to C3 -soil) in relation to microbial growth kinetics and to the activities of five hydrolytic enzymes. This encompasses the groups of parameters governing two mechanisms of priming effects - microbial N mining and stoichiometric decomposition theories. In sole C treatments, positive PE was accompanied by a decrease in specific microbial growth rates, confirming a greater contribution of K-strategists to the decomposition of native SOM. Sucrose addition with N significantly accelerated mineralization of native SOM, whereas mineral N added with plant residues accelerated decomposition of plant residues. This supports the microbial mining theory in terms of N limitation. Sucrose addition with N was accompanied by accelerated microbial growth, increased activities of ß-glucosidase and cellobiohydrolase, and decreased activities of xylanase and leucine amino peptidase. This indicated an increased contribution of r-strategists to the PE and to decomposition of cellulose but the decreased hemicellulolytic and proteolytic activities. Thus, the acceleration of the C cycle was primed by exogenous organic C and was controlled by N. This confirms the stoichiometric decomposition theory. Both K- and r-strategists were beneficial for priming effects, with an increasing contribution of K-selected species under N limitation. Thus, the priming phenomenon described in 'microbial N mining' theory can be ascribed to K-strategists. In contrast, 'stoichiometric decomposition' theory, that is, accelerated OM mineralization due to balanced microbial growth, is explained by domination of r-strategists.

Composition and metabolism of microbial communities in soil pores.

Delineation of microbial habitats within the soil matrix and characterization of their environments and metabolic processes are crucial to understand soil functioning, yet their experimental identification remains persistently limited. We combined single- and triple-energy X-ray computed microtomography with pore specific allocation of 13C labeled glucose and subsequent stable isotope probing to demonstrate how long-term disparities in vegetation history modify spatial distribution patterns of soil pore and particulate organic matter drivers of microbial habitats, and to probe bacterial communities populating such habitats. Here we show striking differences between large (30-150 µm Ø) and small (4-10 µm Ø) soil pores in (i) microbial diversity, composition, and life-strategies, (ii) responses to added substrate, (iii) metabolic pathways, and (iv) the processing and fate of labile C. We propose a microbial habitat classification concept based on biogeochemical mechanisms and localization of soil processes and also suggests interventions to mitigate the environmental consequences of agricultural management.

Sustainable land management enhances ecological and economic multifunctionality under ambient and future climate.

The currently dominant types of land management are threatening the multifunctionality of ecosystems, which is vital for human well-being. Here, we present a novel ecological-economic assessment of how multifunctionality of agroecosystems in Central Germany depends on land-use type and climate. Our analysis includes 14 ecosystem variables in a large-scale field experiment with five different land-use types under two different climate scenarios (ambient and future climate). We consider ecological multifunctionality measures using averaging approaches with different weights, reflecting preferences of four relevant stakeholders based on adapted survey data. Additionally, we propose an economic multifunctionality measure based on the aggregate economic value of ecosystem services. Results show that intensive management and future climate decrease ecological multifunctionality for most scenarios in both grassland and cropland. Only under a weighting based on farmers' preferences, intensively-managed grassland shows higher multifunctionality than sustainably-managed grassland. The economic multifunctionality measure is about ~1.7 to 1.9 times higher for sustainable, compared to intensive, management for both grassland and cropland. Soil biodiversity correlates positively with ecological multifunctionality and is expected to be one of its drivers. As the currently prevailing land management provides high multifunctionality for farmers, but not for society at large, we suggest to promote and economically incentivise sustainable land management that enhances both ecological and economic multifunctionality, also under future climatic conditions.

Degradation of Bio-Based and Biodegradable Plastic and Its Contribution to Soil Organic Carbon Stock.

Expanding the use of environmentally friendly materials to protect the environment is one of the key factors in maintaining a sustainable ecological balance. Poly(butylene succinate-co-adipate) (PBSA) is considered among the most promising bio-based and biodegradable plastics for the future with a high number of applications in soil and agriculture. Therefore, the decomposition process of PBSA and its consequences for the carbon stored in soil require careful monitoring. For the first time, the stable isotope technique was applied in the current study to partitioning plastic- and soil-originated C in the CO2 released during 80 days of PBSA decomposition in a Haplic Chernozem soil as dependent on nitrogen availability. The decomposition of the plastic was accompanied by the C loss from soil organic matter (SOM) through priming, which in turn was dependent on added N. Nitrogen facilitated PBSA decomposition and reduced the priming effect during the first 6 weeks of the experiment. During the 80 days of plastic decomposition, 30% and 49% of the released CO2 were PBSA-derived, while the amount of SOM-derived CO2 exceeded the corresponding controls by 100.2 and 132.3% in PBSA-amended soil without and with N fertilization, respectively. Finally, only 4.1% and 5.4% of the PBSA added into the soil was mineralized to CO2, in the treatments without and with N amendment, respectively.

Is plant biomass input driving soil organic matter formation processes in grassland soil under contrasting management?

Grassland management practices vary in stocking rates and plant removal strategies (grazing versus mowing). They influence organic matter (OM) inputs, which were postulated as main controls of soil organic carbon (SOC) sequestration and might therefore control SOC stabilization. The aim of this study was to test this hypothesis by investigating the impacts of grassland harvesting regimes on parameters related to soil microbial functioning and soil organic matter (SOM) formation processes. We used a thirteen-year experiment in Central France under contrasting management (unmanaged, grazing with two intensities, mowing, bare fallow) to establish a carbon input gradient based on biomass leftovers after harvest. We investigated microbial biomass, basal respiration and enzyme activities as indicators of microbial functioning, and amino sugar content and composition as indicator of persistent SOM formation and origin through necromass accumulation. Responses of these parameters to carbon input along the gradient were contrasting and in most cases unrelated. Only the microbial C/N ratio and amino sugar contents showed a linear response indicating that they are influenced by plant-derived OM input. Other parameters were most probably more influenced by root activity, presence of herbivores, and/or physicochemical changes following management activities impacting soil microbial functioning. Grassland harvesting strategies influence SOC sequestration not only by changing carbon input quantity, but also through their effects on belowground processes possibly related to changing carbon input types and physiochemical soil properties.

Examining the Shift in the Decomposition Channel Structure of the Soil Decomposer Food Web: A Methods Comparison.

Selecting the appropriate indicators and measuring time point numbers is important for accurately examining the shift in soil gross decomposition channel structure. Through a selected case study on a natural forest vs. rainfed arable system over a two-month-long experiment, the utility of three commonly employed indicators (fungi to bacteria ratio (F:B), fungivore to bacterivore ratio (FF:BF), and glucosamine to muramic acid ratio (GlcN:MurN)) were compared to reflect the shift in soil gross decomposition channel structure. The requirement of measuring the time point numbers for the three indicators was also assessed, and we suggest a potential methodology. Our results revealed that the GlcN:MurN ratio was more reliable for assessing the shifts in gross decomposition channel structure for long-term land use changes, while it was less sensitive to short-term drought compared with the other two indicators. The F:B ratio was more applicable than the FF:BF ratio for reflecting both long- and short-term changes. Furthermore, the reliability of the GlcN:MurN ratio was the least dependent on measuring time point numbers. We suggest the use of multiple indicators and the adoption of multiple measuring time points for the overall methodology.

Two-Phase Conceptual Framework of Phosphatase Activity and Phosphorus Bioavailability.

The activity of extracellular phosphatases is a dynamic process controlled by both plant roots and microorganisms, which is responsible for the mineralization of soil phosphorus (P). Plants regulate the availability of soil P through the release of root mucilage and the exudation of low-molecular weight organic acids (LMWOAs). Mucilage increases soil hydraulic conductivity as well as pore connectivity, both of which are associated with increased phosphatase activity. The LMWOAs, in turn, stimulate the mineralization of soil P through their synergistic effects of acidification, chelation, and exchange reactions. This article reviews the catalytic properties of extracellular phosphatases and their interactions with the rhizosphere interfaces. We observed a biphasic effect of root metabolic products on extracellular phosphatases, which notably altered their catalytic mechanism. In accordance with the proposed conceptual framework, soil P is acquired by both plants and microorganisms in a coupled manner that is characterized by the exudation of their metabolic products. Due to inactive or reduced root exudation, plants recycle P through adsorption on the soil matrix, thereby reducing the rhizosphere phosphatase activity. The two-phase conceptual framework might assist in understanding P-acquisition (substrate turnover) and P-restoration (phosphatase adsorption by soil) in various terrestrial ecosystems.

Keep oxygen in check: An improved in-situ zymography approach for mapping anoxic hydrolytic enzyme activities in a paddy soil.

Paddy soils regularly experience redox oscillations during the wetting and draining stages, yet the effects of short-term presence of oxygen (O2) on in-situ microbial hotspots and enzyme activities in anoxic ecosystems remain unclear. To fill this knowledge gap, we applied soil zymography to localize hotspots and activities of phosphomonoesterase (PME), ß-glucosidase (BG), and leucine aminopeptidase (LAP) in three compartments of rice-planted rhizoboxes (top bulk, rooted, and bottom bulk paddy soil) under oxic (+O2) and anoxic (O2) conditions. Short-term (35 min) aeration decreased PME activity by 13-49 %, BG by 4-52 %, and LAP by 12-61 % as compared with O2 in three soil compartments. The percentage of hotspot area was higher by 3-110 % for PME, by 10-60 % for BG, and by 12-158 % for LAP under +O2 vs. O2 conditions depending on a rice growth stage. Irrespective of the aeration conditions, the rhizosphere extent of rice plants for three enzymes was generally greater under higher moisture conditions and at earlier growth stage. Higher O2 sensitivity for the tested enzymes at bottom bulk soil versus other compartments suggested that short-term aeration during conventional zymography may lead to underestimation of nutrient mobilization in subsoil compared to top bulk soil. The intolerance of anaerobic microorganisms against the toxicity of O2 in the cells and the shift of microbial metabolic pathways may explain such a short-term suppression by O2. Our findings, therefore, show that anoxic conditions and soil moisture should be kept during zymography and probably other in-situ soil imaging methods when studying anoxic systems.

Links among Microbial Communities, Soil Properties and Functions: Are Fungi the Sole Players in Decomposition of Bio-Based and Biodegradable Plastic?

The incomplete degradation of bio-based and biodegradable plastics (BBPs) in soils causes multiple threats to soil quality, human health, and food security. Plastic residuals can interact with soil microbial communities. We aimed to link the structure and enzyme-mediated functional traits of a microbial community composition that were present during poly (butylene succinate-co-butylene adipate (PBSA) decomposition in soil with (PSN) and without (PS) the addition of nitrogen fertilizer ((NH4)2SO4). We identified bacterial (Achromobacter, Luteimonas, Rhodanobacter, and Lysobacter) and fungal (Fusarium, Chaetomium, Clonostachys, Fusicolla, and Acremonium) taxa that were linked to the activities of ß-glucosidase, chitinase, phosphatase, and lipase in plastic-amended soils. Fungal biomass increased by 1.7 and 4 times in PS and PSN treatment, respectively, as compared to non-plastic amended soil. PBSA significantly changed the relationships between soil properties (C: N ratio, TN, and pH) and microbial community structure; however, the relationships between fungal biomass and soil enzyme activities remained constant. PBSA significantly altered the relationship between fungal biomass and acid phosphatase. We demonstrated that although the soil functions related to nutrient cycling were not negatively affected in PSN treatment, potential negative effects are reasoned by the enrichment of plant pathogens. We concluded that in comparison to fungi, the bacteria demonstrated a broader functional spectrum in the BBP degradation process.

Nitrogen fixing bacteria facilitate microbial biodegradation of a bio-based and biodegradable plastic in soils under ambient and future climatic conditions.

We discovered a biological mechanism supporting microbial degradation of bio-based poly(butylene succinate-co-adipate) (PBSA) plastic in soils under ambient and future climates. Here, we show that nitrogen-fixing bacteria facilitate the microbial degradation of PBSA by enhancing fungal abundance, accelerating plastic-degrading enzyme activities, and shaping/interacting with plastic-degrading fungal communities.

Bridging Microbial Functional Traits With Localized Process Rates at Soil Interfaces.

In this review, we introduce microbially-mediated soil processes, players, their functional traits, and their links to processes at biogeochemical interfaces [e.g., rhizosphere, detritusphere, (bio)-pores, and aggregate surfaces]. A conceptual view emphasizes the central role of the rhizosphere in interactions with other biogeochemical interfaces, considering biotic and abiotic dynamic drivers. We discuss the applicability of three groups of traits based on microbial physiology, activity state, and genomic functional traits to reflect microbial growth in soil. The sensitivity and credibility of modern molecular approaches to estimate microbial-specific growth rates require further development. A link between functional traits determined by physiological (e.g., respiration, biomarkers) and genomic (e.g., genome size, number of ribosomal gene copies per genome, expression of catabolic versus biosynthetic genes) approaches is strongly affected by environmental conditions such as carbon, nutrient availability, and ecosystem type. Therefore, we address the role of soil physico-chemical conditions and trophic interactions as drivers of microbially-mediated soil processes at relevant scales for process localization. The strengths and weaknesses of current approaches (destructive, non-destructive, and predictive) for assessing process localization and the corresponding estimates of process rates are linked to the challenges for modeling microbially-mediated processes in heterogeneous soil microhabitats. Finally, we introduce a conceptual self-regulatory mechanism based on the flexible structure of active microbial communities. Microbial taxa best suited to each successional stage of substrate decomposition become dominant and alter the community structure. The rates of decomposition of organic compounds, therefore, are dependent on the functional traits of dominant taxa and microbial strategies, which are selected and driven by the local environment.

Spatiotemporal Dynamics of Maize (Zea mays L.) Root Growth and Its Potential Consequences for the Assembly of the Rhizosphere Microbiota.

Numerous studies have shown that plants selectively recruit microbes from the soil to establish a complex, yet stable and quite predictable microbial community on their roots - their "microbiome." Microbiome assembly is considered as a key process in the self-organization of root systems. A fundamental question for understanding plant-microbe relationships is where a predictable microbiome is formed along the root axis and through which microbial dynamics the stable formation of a microbiome is challenged. Using maize as a model species for which numerous data on dynamic root traits are available, this mini-review aims to give an integrative overview on the dynamic nature of root growth and its consequences for microbiome assembly based on theoretical considerations from microbial community ecology.

Impact of manure on soil biochemical properties: A global synthesis.

Manure application mitigates land degradation and improves soil fertility. Despite many individual studies on manure effects, a comprehensive overview of its consequences for a broad range of soil properties is lacking. Through a meta-analysis of 521 observations spanning the experiments from days after pulse addition up to 113 years with continues manure input, we quantified and generalized the average responses of soil biochemical properties depending on climate factors, management, soil, and manure characteristics. Large increase of pools with fast turnover (microbial carbon (C) and nitrogen (N): +88% and +84%, respectively) compared to stable organic matter pools (+27% for organic C, and +33% for total N) reflects acceleration of C and N cycles and soil fertility improvement. Activities of enzymes acquiring C-, energy-, N-, phosphorus- and sulfur were 1.3-3.3 times larger than those in soil without manure for all study durations included. Soil C/N ratio remained unaffected, indicating the stability of coupled C and N cycles. Microbial C/N ratio decreased, indicating a shift towards bacterial domination, general increase of C and N availability and acceleration of element cycling. Composted manure or manure without mineral fertilizers induced the greatest increase compared to non-composted manure or manure with mineral fertilizers, respectively, in most biochemical properties. The optimal manure application rate for adjusting proper soil pH was 25 Mg ha-1 year-1. Among manure types, swine manure caused the greatest increase of N-cycle-related properties: microbial N (+230%), urease (+258%) and N-acetyl-ß-D-glucosaminidase (+138%) activities. Manure application strategies should avoid P and N losses and pollution via runoff, leaching or gaseous emissions due to fast mineralization and priming of soil organic matter. In conclusion, manure application favors C accumulation and accelerates nutrient cycling by providing available organic substances and nutrients and thus increasing enzyme activities.

Changes in the Size of the Active Microbial Pool Explain Short-Term Soil Respiratory Responses to Temperature and Moisture.

Heterotrophic respiration contributes a substantial fraction of the carbon flux from soil to atmosphere, and responds strongly to environmental conditions. However, the mechanisms through which short-term changes in environmental conditions affect microbial respiration still remain unclear. Microorganisms cope with adverse environmental conditions by transitioning into and out of dormancy, a state in which they minimize rates of metabolism and respiration. These transitions are poorly characterized in soil and are generally omitted from decomposition models. Most current approaches to model microbial control over soil CO2 production relate responses to total microbial biomass (TMB) and do not differentiate between microorganisms in active and dormant physiological states. Indeed, few data for active microbial biomass (AMB) exist with which to compare model output. Here, we tested the hypothesis that differences in soil microbial respiration rates across various environmental conditions are more closely related to differences in AMB (e.g., due to activation of dormant microorganisms) than in TMB. We measured basal respiration (SBR) of soil incubated for a week at two temperatures (24 and 33°C) and two moisture levels (10 and 20% soil dry weight [SDW]), and then determined TMB, AMB, microbial specific growth rate, and the lag time before microbial growth (t lag ) using the Substrate-Induced Growth Response (SIGR) method. As expected, SBR was more strongly correlated with AMB than with TMB. This relationship indicated that each g active biomass C contributed ~0.04 g CO2-C h(-1) of SBR. TMB responded very little to short-term changes in temperature and soil moisture and did not explain differences in SBR among the treatments. Maximum specific growth rate did not respond to environmental conditions, suggesting that the dominant microbial populations remained similar. However, warmer temperatures and increased soil moisture both reduced t lag , indicating that favorable abiotic conditions activated soil microorganisms. We conclude that soil respiratory responses to short-term changes in environmental conditions are better explained by changes in AMB than in TMB. These results suggest that decomposition models that explicitly represent microbial carbon pools should take into account the active microbial pool, and researchers should be cautious in comparing modeled microbial pool sizes with measurements of TMB.