Close coupling of plant functional types with soil microbial community composition drives soil carbon and nutrient cycling in tundra heath.

Aims: This study aimed at elucidating divergent effects of two dominant plant functional types (PFTs) in tundra heath, dwarf shrubs and mosses, on soil microbial processes and soil carbon (C) and nutrient availability, and thereby to enhance our understanding of the complex interactions between PFTs, soil microbes and soil functioning. Methods: Samples of organic soil were collected under three dwarf shrub species (of distinct mycorrhizal association and life form) and three moss species in early and late growing season. We analysed soil C and nutrient pools, extracellular enzyme activities and phospholipid fatty acid profiles, together with a range of plant traits, soil and abiotic site characteristics. Results: Shrub soils were characterised by high microbial biomass C and phosphorus and phosphatase activity, which was linked with a fungal-dominated microbial community, while moss soils were characterised by high soil nitrogen availability, peptidase and peroxidase activity associated with a bacterial-dominated microbial community. The variation in soil microbial community structure was explained by mycorrhizal association, root morphology, litter and soil organic matter quality and soil pH-value. Furthermore, we found that the seasonal variation in microbial biomass and enzyme activities over the growing season, likely driven by plant belowground C allocation, was most pronounced under the tallest shrub Betula nana. Conclusion: Our study demonstrates a close coupling of PFTs with soil microbial communities, microbial decomposition processes and soil nutrient availability in tundra heath, which suggests potential strong impacts of global change-induced shifts in plant community composition on carbon and nutrient cycling in high-latitude ecosystems. Supplementary Information: The online version contains supplementary material available at 10.1007/s11104-023-05993-w.

Mosses reduce soil nitrogen availability in a subarctic birch forest via effects on soil thermal regime and sequestration of deposited nitrogen.

In high-latitude ecosystems bryophytes are important drivers of ecosystem functions. Alterations in abundance of mosses due to global change may thus strongly influence carbon (C) and nitrogen (N) cycling and hence cause feedback on climate. The effects of mosses on soil microbial activity are, however, still poorly understood. Our study aims at elucidating how and by which mechanisms bryophytes influence microbial decomposition processes of soil organic matter and thus soil nutrient availability.We present results from a field experiment in a subarctic birch forest in northern Sweden, where we partly removed the moss cover and replaced it with an artificial soil cover for simulating moss effects on soil temperature and moisture. We combined this with a fertilization experiment with 15N-labelled N for analysing the effects of moss N sequestration on soil processes.Our results demonstrate the capacity of mosses to reduce soil N availability and retard N cycling. The comparison with artificial soil cover plots suggests that the effect of mosses on N cycling is linked to the thermal insulation capacity of mosses causing low average soil temperature in summer and strongly reduced soil temperature fluctuations, the latter also leading to a decreased frequency of freeze-thaw events in autumn and spring. Our results also showed, however, that the negative temperature effect of mosses on soil microbial activity was in part compensated by stimulatory effects of the moss layer, possibly linked to leaching of labile substrates from the moss. Furthermore, our results revealed that bryophytes efficiently sequester added N from wet deposition and thus prevent effects of increased atmospheric N deposition on soil N availability and soil processes. Synthesis. Our study emphasizes the important role of mosses in carbon and nutrient cycling in high-latitude ecosystems and the potential strong impacts of reductions in moss abundance on microbial decomposition processes and nutrient availability in subarctic and boreal forests.

Microbes as Engines of Ecosystem Function: When Does Community Structure Enhance Predictions of Ecosystem Processes?

Microorganisms are vital in mediating the earth's biogeochemical cycles; yet, despite our rapidly increasing ability to explore complex environmental microbial communities, the relationship between microbial community structure and ecosystem processes remains poorly understood. Here, we address a fundamental and unanswered question in microbial ecology: 'When do we need to understand microbial community structure to accurately predict function?' We present a statistical analysis investigating the value of environmental data and microbial community structure independently and in combination for explaining rates of carbon and nitrogen cycling processes within 82 global datasets. Environmental variables were the strongest predictors of process rates but left 44% of variation unexplained on average, suggesting the potential for microbial data to increase model accuracy. Although only 29% of our datasets were significantly improved by adding information on microbial community structure, we observed improvement in models of processes mediated by narrow phylogenetic guilds via functional gene data, and conversely, improvement in models of facultative microbial processes via community diversity metrics. Our results also suggest that microbial diversity can strengthen predictions of respiration rates beyond microbial biomass parameters, as 53% of models were improved by incorporating both sets of predictors compared to 35% by microbial biomass alone. Our analysis represents the first comprehensive analysis of research examining links between microbial community structure and ecosystem function. Taken together, our results indicate that a greater understanding of microbial communities informed by ecological principles may enhance our ability to predict ecosystem process rates relative to assessments based on environmental variables and microbial physiology.

Exploring the transfer of recent plant photosynthates to soil microbes: mycorrhizal pathway vs direct root exudation.

Plants rapidly release photoassimilated carbon (C) to the soil via direct root exudation and associated mycorrhizal fungi, with both pathways promoting plant nutrient availability. This study aimed to explore these pathways from the root's vascular bundle to soil microbial communities. Using nanoscale secondary ion mass spectrometry (NanoSIMS) imaging and (13) C-phospho- and neutral lipid fatty acids, we traced in-situ flows of recently photoassimilated C of (13) CO2 -exposed wheat (Triticum aestivum) through arbuscular mycorrhiza (AM) into root- and hyphae-associated soil microbial communities. Intraradical hyphae of AM fungi were significantly (13) C-enriched compared to other root-cortex areas after 8 h of labelling. Immature fine root areas close to the root tip, where AM features were absent, showed signs of passive C loss and co-location of photoassimilates with nitrogen taken up from the soil solution. A significant and exclusively fresh proportion of (13) C-photosynthates was delivered through the AM pathway and was utilised by different microbial groups compared to C directly released by roots. Our results indicate that a major release of recent photosynthates into soil leave plant roots via AM intraradical hyphae already upstream of passive root exudations. AM fungi may act as a rapid hub for translocating fresh plant C to soil microbes.

Fungal and bacterial utilization of organic substrates depends on substrate complexity and N availability.

There is growing evidence of a direct relationship between microbial community composition and function, which implies that distinct microbial communities vary in their functional properties. The aim of this study was to determine whether differences in initial substrate utilization between distinct microbial communities are due to the activities of certain microbial groups. We performed a short-term experiment with beech forest soils characterized by three different microbial communities (winter and summer community, and a community from a tree-girdling plot). We incubated these soils with different (13) C-labelled substrates with or without inorganic N addition and analyzed microbial substrate utilization by (13) C-phospholipid fatty acid (PLFA) analysis. Our results revealed that the fate of labile C (glucose) was similar in the three microbial communities, despite differences in absolute substrate incorporation between the summer and winter community. The active microbial community involved in degradation of complex C substrates (cellulose, plant cell walls), however, differed between girdling and control plots and was strongly affected by inorganic N addition. Enhanced N availability strongly increased fungal degradation of cellulose and plant cell walls. Our results indicate that fungi, at least in the presence of a high N supply, are the main decomposers of polymeric C substrates.

Seasonal variation in functional properties of microbial communities in beech forest soil.

Substrate quality and the availability of nutrients are major factors controlling microbial decomposition processes in soils. Seasonal alteration in resource availability, which is driven by plants via belowground C allocation, nutrient uptake and litter fall, also exerts effects on soil microbial community composition. Here we investigate if seasonal and experimentally induced changes in microbial community composition lead to alterations in functional properties of microbial communities and thus microbial processes. Beech forest soils characterized by three distinct microbial communities (winter and summer community, and summer community from a tree girdling plot, in which belowground carbon allocation was interrupted) were incubated with different 13C-labeled substrates with or without inorganic N supply and analyzed for substrate use and various microbial processes. Our results clearly demonstrate that the three investigated microbial communities differed in their functional response to addition of various substrates. The winter communities revealed a higher capacity for degradation of complex C substrates (cellulose, plant cell walls) than the summer communities, indicated by enhanced cellulase activities and reduced mineralization of soil organic matter. In contrast, utilization of labile C sources (glucose) was lower in winter than in summer, demonstrating that summer and winter community were adapted to the availability of different substrates. The saprotrophic community established in girdled plots exhibited a significantly higher utilization of complex C substrates than the more plant root associated community in control plots if additional nitrogen was provided. In this study we were able to demonstrate experimentally that variation in resource availability as well as seasonality in temperate forest soils cause a seasonal variation in functional properties of soil microorganisms, which is due to shifts in community structure and physiological adaptations of microbial communities to altered resource supply.

Responses of belowground carbon allocation dynamics to extended shading in mountain grassland.

Carbon (C) allocation strongly influences plant and soil processes. Short-term C allocation dynamics in ecosystems and their responses to environmental changes are still poorly understood. Using in situ (13) CO(2) pulse labeling, we studied the effects of 1 wk of shading on the transfer of recent photoassimilates between sugars and starch of above- and belowground plant organs and to soil microbial communities of a mountain meadow. C allocation to roots and microbial communities was rapid. Shading strongly reduced sucrose and starch concentrations in shoots, but not roots, and affected tracer dynamics in sucrose and starch of shoots, but not roots: recent C was slowly incorporated into root starch irrespective of the shading treatment. Shading reduced leaf respiration more strongly than root respiration. It caused no reduction in the amount of (13) C incorporated into fungi and Gram-negative bacteria, but increased its residence time. These findings suggest that, under interrupted C supply, belowground C allocation (as reflected by the amount of tracer allocated to root starch, soil microbial communities and belowground respiration) was maintained at the expense of aboveground C status, and that C source strength may affect the turnover of recent plant-derived C in soil microbial communities.

Plants control the seasonal dynamics of microbial N cycling in a beech forest soil by belowground C allocation.

Soil microbes in temperate forest ecosystems are able to cycle several hundreds of kilograms of N per hectare per year and are therefore of paramount importance for N retention. Belowground C allocation by trees is an important driver of seasonal microbial dynamics and may thus directly affect N transformation processes over the course of the year. Our study aimed at unraveling plant controls on soil N cycling in a temperate beech forest at a high temporal resolution over a time period of two years, by investigating the effects of tree girdling on microbial N turnover. In both years of the experiment, we discovered (1) a summer N mineralization phase (between July and August) and (2) a winter N immobilization phase (November-February). The summer mineralization phase was characterized by a high N mineralization activity, low microbial N uptake, and a subsequent high N availability in the soil. During the autumn/winter N immobilization phase, gross N mineralization rates were low, and microbial N uptake exceeded microbial N mineralization, which led to high levels of N in the microbial biomass and low N availability in the soil. The observed immobilization phase during the winter may play a crucial role for ecosystem functioning, since it could protect dissolved N that is produced by autumn litter degradation from being lost from the ecosystem during the phase when plants are mostly inactive. The difference between microbial biomass N levels in winter and spring equals 38 kg N/ha and may thus account for almost one-third of the annual plant N demand. Tree girdling strongly affected annual N cycling: the winter N immobilization phase disappeared in girdled plots (microbial N uptake and microbial biomass N were significantly reduced, while the amount of available N in the soil solution was enhanced). This was correlated to a reduced fungal abundance in autumn in girdled plots. By releasing recently fixed photosynthates to the soil, plants may thus actively control the annual microbial N cycle. Tree belowground C allocation increases N accumulation in microorganisms during the winter which may ultimately feed back on plant N availability in the following growing season.

Microbial processes and community composition in the rhizosphere of European beech - The influence of plant C exudates.

Plant roots strongly influence C and N availability in the rhizosphere via rhizodeposition and uptake of nutrients. This study aimed at investigating the effect of resource availability on microbial processes and community structure in the rhizosphere. We analyzed C and N availability, as well as microbial processes and microbial community composition in rhizosphere soil of European beech and compared it to the bulk soil. Additionally, we performed a girdling experiment in order to disrupt root exudation into the soil. By this novel approach we were able to demonstrate that enhanced resource availability positively affected N mineralization and hydrolytic enzyme activities in the rhizosphere, but negatively affected nitrification rates and oxidative enzyme activities, which are involved in the degradation of soil organic matter. Both rhizosphere effects on N mineralization and oxidative enzyme activities disappeared in the girdling treatment. Microbial community structure in the rhizosphere, assessed by phospholipid fatty acid analysis, differed only slightly from bulk soil but was markedly altered by the girdling treatment, indicating additional effects of the girdling treatment beyond the reduction of root exudation. Differences in oxidative enzyme activities and nitrification rates between rhizosphere soil and bulk soil, however, suggest considerable differences in the (functional) microbial community composition.

Seasonality and resource availability control bacterial and archaeal communities in soils of a temperate beech forest.

It was hypothesized that seasonality and resource availability altered through tree girdling were major determinants of the phylogenetic composition of the archaeal and bacterial community in a temperate beech forest soil. During a 2-year field experiment, involving girdling of beech trees to intercept the transfer of easily available carbon (C) from the canopy to roots, members of the dominant phylogenetic microbial phyla residing in top soils under girdled versus untreated control trees were monitored at bimonthly intervals through 16S rRNA gene-based terminal restriction fragment length polymorphism profiling and quantitative PCR analysis. Effects on nitrifying and denitrifying groups were assessed by measuring the abundances of nirS and nosZ genes as well as bacterial and archaeal amoA genes. Seasonal dynamics displayed by key phylogenetic and nitrogen (N) cycling functional groups were found to be tightly coupled with seasonal alterations in labile C and N pools as well as with variation in soil temperature and soil moisture. In particular, archaea and acidobacteria were highly responsive to soil nutritional and soil climatic changes associated with seasonality, indicating their high metabolic versatility and capability to adapt to environmental changes. For these phyla, significant interrelations with soil chemical and microbial process data were found suggesting their potential, but poorly described contribution to nitrification or denitrification in temperate forest soils. In conclusion, our extensive approach allowed us to get novel insights into effects of seasonality and resource availability on the microbial community, in particular on hitherto poorly studied bacterial phyla and functional groups.

Belowground carbon allocation by trees drives seasonal patterns of extracellular enzyme activities by altering microbial community composition in a beech forest soil.

*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.

Negligible contribution from roots to soil-borne phospholipid fatty acid fungal biomarkers 18:2ω6,9 and 18:1ω9.

The phospholipid fatty acid biomarkers 18:1ω9, 18:2ω6,9 and 18:3ω3,6,9 are commonly used as fungal biomarkers in soils. They have, however, also been found to occur in plant tissues, such as roots. Thus, the use of these PLFAs as fungal biomarkers in sieved soil, which may still contain small remains of roots, has been questioned. We used data from a recent beech tree girdling experiment to calculate the contribution of roots to these biomarkers and were able to demonstrate that not more than 0.61% of 18:1ω9 and 18:2ω6,9 in sieved soil samples originated from roots (but 4% of 18:3ω3,6,9). Additionally, the abundance of the biomarker 18:2ω6,9 in the soil was found to be highly correlated to ectomycorrhizal root colonization, which further corroborates its fungal origin. PLFA biomarkers were substantially reduced in vital roots from girdled trees compared to roots of control trees (by up to 76%), indicating that the major part of PLFAs measured in roots may actually originate from ectomycorrhizal fungi growing inside the roots. We calculated, that even a near to 50% reduction in fine root biomass - as observed in the girdling treatment - accounted for only 0.8% of the measured decrease of 18:2ω6,9. Our results demonstrate that both 18:1ω9 and 18:2ω6,9 are suitable biomarkers for detecting fungal dynamics in soils and that especially 18:2ω6,9 is a reliable biomarker to study mycorrhizal dynamics in beech forests.