Root exudation is a key plant function with a large influence on soil organic matter dynamics and plant–soil feedbacks in forest ecosystems. Yet despite its importance, the main ecological drivers of ...root exudation in mature forest trees remain to be identified.
During two growing seasons, we analyzed the dependence of in situ collected root exudates on root morphology, soil chemistry and nutrient availability in six mature European beech (Fagus sylvatica L.) forests on a broad range of bedrock types.
Root morphology was a major driver of root exudation across the nutrient availability gradient. A doubling of specific root length exponentially increased exudation rates of mature trees by c. 5-fold. Root exudation was also closely negatively related to soil pH and nitrogen (N) availability. At acidic and N-poor sites, where fungal biomass was reduced, exudation rates were c. 3-fold higher than at N- and base-richer sites and correlated negatively with the activity of enzymes degrading less bioavailable carbon (C) and N in the bulk soil.
We conclude that root exudation increases on highly acidic, N-poor soils, in which fungal activity is reduced and a greater portion of the assimilated plant C is shifted to the external ecosystem C cycle.
Plant mitochondria have a fully operational tricarboxylic acid (TCA) cycle that plays a central role in generating ATP and providing carbon skeletons for a range of biosynthetic processes in both ...heterotrophic and photosynthetic tissues. The cycle enzyme-encoding genes have been well characterized in terms of transcriptional and effector-mediated regulation and have also been subjected to reverse genetic analysis. However, despite this wealth of attention, a central question remains unanswered: “What regulates flux through this pathway in vivo?” Previous proteomic experiments with Arabidopsis discussed below have revealed that a number of mitochondrial enzymes, including members of the TCA cycle and affiliated pathways, harbor thioredoxin (TRX)-binding sites and are potentially redox-regulated. We have followed up on this possibility and found TRX to be a redox-sensitive mediator of TCA cycle flux. In this investigation, we first characterized, at the enzyme and metabolite levels, mutants of the mitochondrial TRX pathway in Arabidopsis : the NADP-TRX reductase a and b double mutant ( ntra ntrb ) and the mitochondrially located thioredoxin o1 ( trxo1 ) mutant. These studies were followed by a comparative evaluation of the redistribution of isotopes when ¹³C-glucose, ¹³C-malate, or ¹³C-pyruvate was provided as a substrate to leaves of mutant or WT plants. In a complementary approach, we evaluated the in vitro activities of a range of TCA cycle and associated enzymes under varying redox states. The combined dataset suggests that TRX may deactivate both mitochondrial succinate dehydrogenase and fumarase and activate the cytosolic ATP-citrate lyase in vivo, acting as a direct regulator of carbon flow through the TCA cycle and providing a mechanism for the coordination of cellular function.
Significance The present work extends redox-based change in enzyme activity to the TCA cycle of plant mitochondria. Thioredoxin (TRX) was found to regulate the activity of enzymes of the mitochondrial cycle (succinate dehydrogenase and fumarase) and of an enzyme associated with it (ATP-citrate lyase) by modulating thiol redox status. A combination of experiments based on mutant and carbon isotope labeling analyses provides evidence that flux through this pathway is coordinately modulated by TRX at the enzyme level of both mitochondria and cytosol. The results provide in vivo confirmation of earlier in vitro results and further show that mitochondria resemble plastids in using TRX and redox status to regulate the main carbon flux pathway of the organelle.
Soil food web structure and function is primarily determined by the major basal resources, which are living plant tissue, root exudates and dead organic matter. A field experiment was performed to ...disentangle the interlinkage of the root-and detritus-based soil food chains. An arable site was cropped either with maize, amended with maize shoot litter or remained bare soil, representing food webs depending on roots, aboveground litter and soil organic matter as predominant resource, respectively. The soil micro-food web, i.e. microorganisms and nematodes, was investigated in two successive years along a depth transect. The community composition of nematodes was used as model to determine the changes in the rhizosphere, detritusphere and bulk soil food web. In the first growing season the impact of treatments on the soil micro-food web was minor. In the second year plant-feeding nematodes increased under maize, whereas after harvest the Channel Index assigned promotion of the detritivore food chain, reflecting decomposition of root residues. The amendment with litter did not foster microorganisms, instead biomass of Gram-positive and Gram-negative bacteria as well as that of fungi declined in the rooted zone. Likely higher grazing pressure by nematodes reduced microbial standing crop as bacterial and fungal feeders increased. However, populations at higher trophic levels were not promoted, indicating limited flux of litter resources along the food chain. After two years of bare soil microbial biomass and nematode density remained stable, pointing to soil organic matter-based resources that allow bridging periods with deprivation. Nematode communities were dominated by opportunistic taxa that are competitive at moderate resource supply. In sum, removal of plants from the system had less severe effects than expected, suggesting considerable food web resilience to the disruption of both the root and detrital carbon channel, pointing to a legacy of organic matter resources in arable soils.
Phosphorus (P) is an essential nutrient, but European forest ecosystems are experiencing widespread declines in soil P concentrations. To clarify the roles of ectomycorrhizal (EM) and saprotrophic ...(SAP) fungi in P cycling in forest soils that differ in inorganic and organic P availability, we conducted an ingrowth tube (IGT) experiment over 18 months of exposure in five beech (Fagus sylvatica L.) forests in Germany. To separate the contributions of both fungal guilds in situ, two different types of IGTs were used: (i) open IGTs with micromesh windows to allow EM fungi to regrow into the tubes, and (ii) closed IGTs (without mesh windows) in which recolonization by EM hyphae was restricted. We then measured phosphomonoesterase, phosphodiesterase, peroxidase, and phenoloxidase activities in EM (open IGTs) and SAP (closed IGTs) dominated fungal assemblages. Shifts in fungal assemblages occurred over time, but the speed and extent of those shifts differed between the five forest sites. In three forest sites fungal community composition shifted toward greater dominance of EM fungi in open IGTs than in closed IGTs after a period of 18 months, but these changes were not apparent in two other sites. Although shifts in fungal community composition were noticeable between treatments, we found no effect on phosphomonoesterase activity. Since phosphomonoesterase is present in both fungal guilds, this indicates functional redundancy of fungi. Phosphodiesterase activity was slightly reduced in SAP dominated IGTs, indicating that SAP fungi contribute to phosphodiesterase activity to a lesser extent than do EM fungi. P cycling enzymes did not appear to have been influenced by the total P stocks of the forest sites but may have been affected by additional abiotic factors. Contrary to our expectation, phenoloxidase activity was unaffected by fungal community composition, and only peroxidase activity was higher in SAP dominated IGTs, indicating that the contribution of EM fungi to degradation of complex organic material is driven by the need to obtain nutrients in addition to C. Overall, the results of this study contribute to a better understanding of the roles of EM and SAP fungi in P cycling in forest soils.
Resource quality and availability modify the microbial contribution to soil organic matter turnover and formation. We created a microbial hotspot at the soil-litter interface in a microcosm ...experiment to better understand and integrate specific microbial habitats into C turnover models. Reciprocal transplantation of 13C and 12C litter on top of soil cores allowed us to follow C flow into specific members of the microbial food web (bacteria and fungi) and to calculate the turnover times of litter-derived C in these microorganisms at three different stages of maize litter decomposition; early stage (0–4 days), intermediate stage (5–12 days) and later stage (29–36 days).
Litter age influenced the incorporation rate of C into bacteria and fungi and subsequent turnover in phospholipid fatty acid (PLFA) biomarkers. When fresh litter was applied, both fungi and bacteria were able to assimilate labile litter C in the early stage of decomposition, while lower substrate quality in the intermediate stage of decomposition promoted fungal utilization. Utilization of complex litter C sources was minor in both fungi and bacteria in the later stage of decomposition. Different bacterial substrate utilization strategies were reflected by either a decline of the isotopic signal after exchange of 13C by 12C litter or by storage and/or reuse of previously released microbial 13C. The mean residence time of C in the fungal PLFA 18:2ω6,9 was estimated from 46 to 32 days, which is the same or shorter time than that of bacterial PLFAs. This highlights the role of fungi in rapid turnover processes of plant residues, with implications for implementation of bacterial and fungal processes into C turnover models.
•We studied C flow through soil microorganisms in a microbial hotspot.•Maize C input into soil microbial and C pools changed during litter decomposition.•No clear resource partitioning between detritusphere bacteria and fungi occurred.•Mean residence time of C was equal to or shorter in fungi than in bacteria.•C input into PLFAs reflected various strategies of microbial substrate utilization.
Summary
Nutrient imbalances cause the deterioration of tree health in European forests, but the underlying physiological mechanisms are unknown. Here, we investigated the consequences of decreasing ...root carbohydrate reserves for phosphorus (P) mobilisation and uptake by forest trees.
In P‐rich and P‐poor beech (Fagus sylvatica) forests, naturally grown, young trees were girdled and used to determine root, ectomycorrhizal and microbial activities related to P mobilisation in the organic layer and mineral topsoil in comparison with those in nongirdled trees.
After girdling, root carbohydrate reserves decreased. Root phosphoenolpyruvate carboxylase activities linking carbon and P metabolism increased. Root and ectomycorrhizal phosphatase activities and the abundances of bacterial genes catalysing major steps in P turnover increased, but soil enzymes involved in P mobilisation were unaffected. The physiological responses to girdling were stronger in P‐poor than in P‐rich forests. P uptake was decreased after girdling. The soluble and total P concentrations in roots were stable, but fine root biomass declined after girdling.
Our results support that carbohydrate depletion results in reduced P uptake, enhanced internal P remobilisation and root biomass trade‐off to compensate for the P shortage. As reductions in root biomass render trees more susceptible to drought, our results link tree deterioration with disturbances in the P supply as a consequence of decreased belowground carbohydrate allocation.
Dark, that is, nonphototrophic, microbial CO2 fixation occurs in a large range of soils. However, it is still not known whether dark microbial CO2 fixation substantially contributes to the C balance ...of soils and what factors control this process. Therefore, the objective of this study was to quantitate dark microbial CO2 fixation in temperate forest soils, to determine the relationship between the soil CO2 concentration and dark microbial CO2 fixation, and to estimate the relative contribution of different microbial groups to dark CO2 fixation. For this purpose, we conducted a 13C‐CO2 labeling experiment. We found that the rates of dark microbial CO2 fixation were positively correlated with the CO2 concentration in all soils. Dark microbial CO2 fixation amounted to up to 320 µg C kg−1 soil day−1 in the Ah horizon. The fixation rates were 2.8–8.9 times higher in the Ah horizon than in the Bw1 horizon. Although the rates of dark microbial fixation were small compared to the respiration rate (1.2%–3.9% of the respiration rate), our findings suggest that organic matter formed by microorganisms from CO2 contributes to the soil organic matter pool, especially given that microbial detritus is more stable in soil than plant detritus. Phospholipid fatty acid analyses indicated that CO2 was mostly fixed by gram‐positive bacteria, and not by fungi. In conclusion, our study shows that the dark microbial CO2 fixation rate in temperate forest soils increases in periods of high CO2 concentrations, that dark microbial CO2 fixation is mostly accomplished by gram‐positive bacteria, and that dark microbial CO2 fixation contributes to the formation of soil organic matter.
The contribution of dark, that is, nonphototrophic, microbial CO2 fixation in soil to the carbon cycle is still not well understood. We found that the rates of dark microbial CO2 fixation in temperate forest soils were positively correlated with the CO2 concentration, indicating that more CO2 is fixed in periods of high soil CO2 concentrations and in microsites with high CO2 concentration. In addition, our findings suggest that organic matter formed by microorganisms from CO2 contributes to the soil organic matter pool and that dark CO2 fixation in temperate forest soils is mostly accomplished by gram‐positive bacteria and not by fungi.
The mineralosphere is an important micro habitat in terrestrial ecosystems. How different groups of microorganisms colonise mineral surfaces and whether the level of grassland land-use intensity ...(LUI) modifies this micro-habitat is not well known, however. We exposed mesh containers filled with pristine soil minerals (illite/goethite) mixed with 13C labelled root litter of Dactylis glomerata and Lolium perenne in grassland soils of the “Schwäbische Alb” (Germany) to characterise the succession of different microbial properties in the mineralosphere. The use of sites within the Biodiversity Exploratories made it possible to select five sites of low LUI and five sites of high LUI. After 1, 2, 7, 12 and 31 months of exposure in the grassland soils, we used physiological, microbiological and isotopic methods to elucidate in situ colonisation patterns, carbon use and levels of extracellular enzyme expression by soil microorganisms associated with mineral surfaces. Microorganisms slowly colonised pristine mineral surfaces and established functionally distinct communities over time. Fungi colonised mineral surfaces to a greater extent than bacteria, reaching 13.2% of control soils compared to 3.2% by bacteria after 31 months. Fungi also reached pristine mineral surfaces earlier than bacteria, probably due to their hyphal growth strategies, and made immediate use of the added complex root litter substrate. This result is evident by the incorporation of up to 74% root litter-derived C into the fungus-specific PLFA (18:2ω6,9) compared to 51% root litter-derived C in the bacteria-specific PLFAs. Both bacteria and fungi associated with minerals remained in an active state (high biomass-specific respiration, high bacterial and fungal growth rates) throughout the experimental period. Grassland LUI and physico-chemical properties of the adjacent soil modified both quantity and quality of substrates available to soil microorganisms in the mineralosphere. Since 13C incorporation into microbial biomass was greater under low LUI than under high LUI, we conclude that microorganisms in low LUI sites had to rely on the added root material, while the carbon signal in microorganisms in the high LUI sites was diluted by alternative sources resulting from transport of dissolved organic carbon into the mineralosphere.
•Fungi colonise pristine mineral surfaces in grassland soils more rapidly than bacteria.•Fungi incorporated relatively more root-derived C into their biomass than bacteria.•Up to 74% of the C in fungal biomass was root litter-derived.•Mineral-associated microorganisms were more active than in the control soil.
Plant-derived carbon (C) transfer to soil is one of the important factors controlling the size and structure of the belowground microbial community. The present study quantifies this plant-derived C ...incorporation into abiotic and biotic C pools in top- and subsoil in an arable field over five years. Stable isotope analysis was used to determine the incorporation of maize root and shoot litter C into soil organic C (SOC), extractable organic C (EOC), total microbial biomass (Cmic), ergosterol and phospholipid fatty acids (PLFAs). The following treatments were investigated: corn maize (CM), providing root- and shoot-derived C (without corncobs), fodder maize (FM), providing only root-derived C, and wheat plus maize shoot litter amendment (WL), providing only shoot-derived maize C. Wheat plants (W) without maize litter amendment served as control. Soil samples were taken each September directly before harvest from 2009 to 2013. During the experiment, the maize-derived C signal increased in SOC, EOC, Cmic, ergosterol, bacterial and fungal PLFAs in the topsoil (0–10 cm). Although total maize shoot C input was threefold lower than maize root C input, similar relative amounts of maize C derived from shoots and roots were incorporated into the different C pools in the WL and the FM treatments, indicating the importance of shoot-derived C sources for microorganisms in the topsoil. An additive effect of both C sources was found in the CM treatment with almost twice as much maize-derived C in the respective pools. Furthermore, the proportion of maize-derived C varied between the different pools with lower incorporation into the total SOC (17%) and total EOC (24%) pools and higher incorporation ratios of maize C into PLFAs of different microbial groups (29% in Gram-positive (Gr+) bacterial PLFA-C, 44% in Gram-negative (Gr−) bacterial PLFA-C, 69% in fungal PLFA-C and 78% in ergosterol) in the CM treatment in topsoil after five years. After the third and fifth vegetation periods, we also detected maize-derived C in the rooted zone (40–50 cm depth) and the root-free zone (60–70 cm depth). The maize-derived C incorporation was lower in subsoil C pools in comparison to topsoil C pools. In the root-free zone, the maize-derived C was found to be 2% in total SOC, 28% in total EOC, 9% in Gr+ bacterial PLFA-C, 20% in Gr− bacterial PLFA-C and 53% in fungal PLFA-C. Saprotrophic fungi incorporated maize-derived C in all soil depths to a greater degree than Gr+ and Gr− bacteria, indicating the importance of saprotrophic fungi in this agro-ecosystem.
•Root and shoot C was incorporated in an additive way into topsoil C pools.•Maize C input increased in soil C pools in the order SOC < EOC < bacteria < fungi.•Fungi incorporated maize C to a higher extend than bacteria in top- and subsoil.•Subsoil microorganisms depend on quantity rather than quality of C substrates.
Diffuse nitrogen losses from agriculture in Germany continue to cause regionally increased nitrate concentrations in groundwater. Groundwater quality monitoring cannot be a timely indicator of the ...effects of mitigation measures being applied in agriculture, due to frequently long transport routes and high residence times of the leachate. Instead, nitrate leaching potential is often determined at field and farm scale by monitoring soil mineral nitrogen contents at 0–90 cm depth in autumn (SMNa), i.e. before the start of the annual leachate period. In this study, we developed an understanding of the controls on the soil mineral nitrogen content at the start of winter. In an on-farm approach, extensive data was collected from 48 farms in five nitrate-sensitive regions in Germany from 2017 to 2020. From this data set, 25 management and site factors were evaluated with regard to their significance for SMNa by means of a random forest model. With the random forest regression, we identified the role of the factors on SMNa with an acceptable model accuracy with R2 = 0.56. The results show that the cultivated crop is the most important factor influencing SMNa. Potatoes, oilseed rape and maize produced the highest SMNas, whereas SMNas were lowest after spring barley, sugar beet and winter barley. Among site factors, soil type and texture as well as precipitation in October were most decisive. The effects of N fertilisation parameters such as rate and timing were masked by these site factors. The results show that the reduction of nitrogen-intensive crops in crop sequences can be a promising measure for the reduction of nitrate loads. On the other hand, our analysis makes clear that soil-related factors controlling nitrogen release and risk of leaching, as well as weather, can significantly mask the effect of cultivation.
•Prediction of potential nitrate leaching with random forest algorithm.•Grown crop revealed most important factor for nitrate leaching potential.•Site-adapted nitrogen management crucial.
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