Soil microbes are essential to maintain terrestrial ecosystem functionality. However, their diversity is threatened by land-use change, such as agricultural expansion and intensification. One important microbial group mediating the exchange of nutrients between plants and soil is arbuscular mycorrhizal (AM) fungi. The response of microorganism diversity to present and past habitat amount has been poorly studied. Here, we evaluate the potential role of current and historical natural habitat availability in explaining the diversity of AM fungi in arable fields. We conducted a spatially intensive sampling of three agricultural fields in Estonia. Soil AM fungal diversity was determined by soil DNA metabarcoding. We related AM fungal species richness, along with beta diversity components (turnover and nestedness), to abiotic conditions and natural habitat area availability at different spatial scales and time periods. Our findings showed a positive relationship between AM fungal richness and the amount of natural habitat area. Specifically, current AM fungal species richness was best explained by the amount of natural habitat from 130 years earlier, indicating a legacy effect of past land use on current soil biodiversity. The amount of past natural areas was negatively related to the beta diversity turnover component, indicating a replacement of AM fungal species in disturbed sites. While biodiversity-friendly farming is useful in promoting diverse soil biota, historical legacies can be persistent. Maintaining natural habitats around agricultural fields can further promote soil AM fungal diversity for future generations.
Soil microorganisms play a key role in the provision of plant-bioavailable nutrients, which is crucial for ecosystem functioning and plant productivity. Fairy rings are widespread features in grasslands accompanied by lush dark-green vegetation bands. This enigmatic feature is caused by increased soil bioavailable nitrogen (N) due to the expansion of fairy ring fungi (FRF). However, little is known about how FRF enhance soil bioavailable N concentrations. Here, we conducted a survey of 35 fairy rings in temperate grasslands to reveal the role of FRF in regulating soil microorganisms and N cycling using amplicon and metagenomic sequencing. The presence of FRF accelerated organic N mineralization via promoting extracellular enzyme (β-1,4-N-acetylglucosaminidase) activity, leading to a 455% increase in ammonium-N. This further stimulated nitrification to enhance nitrate-N concentration by favoring ammonia-oxidizing archaea. Concomitantly, the increased nitrate-N did not promote denitrification or affect the potential risk of N loss. Furthermore, the relative abundance of other saprotrophic and symbiotrophic fungi was significantly reduced by FRF but the changes in these fungi did not affect the activity of extracellular enzymes involved in N mineralization. Our results suggest that FRF can act as ecosystem engineer species shaping fairy rings by driving soil N cycling without the involvement of other microbial functional groups of saprotroph and symbiotroph to boost plant productivity. Thus, due to the stronger N mobilizing ability, FRF show great potential to be exploited as beneficial microorganisms in plant production and sustainable agricultural development.
We searched for patterns supporting the hypothesis of compositional and functional linkage between forest floor nematode communities and dominant tree canopies, while controlling for some relevant soil and climate variables. Twenty-one forest sampling sites scattered throughout the South-Eastern Carpathian basin were selected under spruce, beech, and hornbeam-oak canopies. The relative contribution of forest canopy type to nematode assemblage differentiation was estimated through nematode taxonomic composition and feeding guild structure. The forest canopy type had a significant effect on nematode taxon/feeding guild composition and diversity at stand level. Several (diagnostic) nematode taxa and feeding guilds were positively associated with and accurately predicted the forest canopy types considered. Apart from the herbivorous nematodes, all the other trophic guilds were significantly related, in terms of their relative abundance, to the forest canopy type. Both nematode taxonomic and trophic diversity were significantly higher under beech canopy compared with its two counterparts. The highest total nematode beta diversity, either taxonomic or trophic, was attained between hornbeam-oak and spruce canopies. Nematode taxonomic and trophic beta diversity between forest canopy types were largely determined by taxon replacement and respectively, by a nested trophic structure. Overall, four concordant and two discordant patterns were revealed between nematode taxon and feeding guild composition with respect to overlying forest canopy, all underpinning the addressed ecological linkage. The present results bring evidence regarding the important contribution of the forest canopy, along with climatic variables, in driving the taxonomic and functional composition/diversity of nematode communities from the soil organic horizon.
Fire is a dominant ecosystem process in many Mediterranean climate type ecosystems, and is predicted to increase in severity and frequency, shifting away from previous regimes in many regions. Responses of flora and fauna to fire are relatively well studied, but less is known about the responses of belowground microbiota. We quantified soil fungal dynamics over the first 12–15 months after fire, focusing on attributes of the fire regime (season, interval, severity). Soil samples were collected from three sites in a threatened woodland ecosystem in southwestern Australia, a Mediterranean-type climate region. Fungal taxa were identified via high throughput sequencing of the ITS subregion and taxonomy assigned using reference databases. Richness, diversity, abundance, community composition, and functional groups were quantified. Over the post-fire sampling period, richness and diversity declined and soil fungal community composition changed significantly throughout the sampling period, with family level taxa and functional groupings experiencing the most change. Through the sampling period, an increase in saprotrophic and endophytic fungi was observed, along with a decrease in all pathogenic fungi. We found that the post-fire fungal community is quite dynamic in the first 12–15 months after fire. We found little effect of fire interval or fire season, though our inference was limited. Our work contributes to putting belowground biota into the same conceptual frameworks as aboveground taxa and serves to inform fire managers in fire-prone Mediterranean climate type regions.
Plants recruit microorganisms from bulk soil by secreting easily available organic carbon into the rhizosphere. Grafting often increases the disease resistance of agricultural plants by modifying this carbon flow from roots into rhizosphere and by recruiting active microorganisms that suppress pathogens. Here, we continuously labeled grafted and ungrafted watermelon plants in a 13CO2 atmosphere to identify the active microorganisms assimilating root exudates. Multi-omics associated technologies (amplicon sequencing, metagenomics and metabolomics) combined with 13C tracing were used to examine the carbon flows, microbial utilization and transformation in the rhizosphere. The number of potentially active bacterial species recruited in the rhizosphere of grafted plants and utilizing root exudates was four times more than in ungrafted plants. These potentially active species matched to metagenome-assembled-genomes (MAGs) mainly belonging to Sphingomonas in the rhizosphere of ungrafted plants, and to Sphingomonas, Chitinophaga, Dyadobacter and Pseudoxanthomonas in the rhizosphere of grafted plants. Sphingomonas possesses the functional potential to metabolize a plant self-toxic substance, namely 4-hydroxybenzoic acid. Furthermore, grafting shaped the complex metabolic interactions and changed the original metabolic dependence between the potentially active bacterial species. Grafting plants diversified belowground carbon flows, activating a greater number of beneficial microbes.
Drought and rainfall events will become more frequent and intense with climate change. At the same time, soil moisture is one of the major factors controlling soil microbial processes such as carbon cycling. When challenged with drought there are two main growth responses microorganisms can use: (1) they can maintain growth rates during drought (i.e., resistance) and (2) they can recover growth rates faster when the drought ends (i.e., resilience). Microbial communities are shaped by multiple other factors in the soil environment, however how those impact drought responses remain unclear. Here we investigate how climate (estimated as aridity index) and soil properties determine microbial growth resistance and resilience to drought across a climate gradient in Europe. To test this, we exposed the different soils to a standardised drought cycle in controlled conditions. We assessed bacterial growth, fungal growth and respiration during soil drying to determine resistance and in high resolution during three days after rewetting to estimate resilience to drought. We found that alpha diversity was the strongest driver of both bacterial drought resistance and resilience, which occurred via changes in soil pH. This shows the importance of diversity for sustaining bacterial functions during drought stress. A secondary driver of bacterial drought resistance and resilience was the aridity index was also an important driver, where bacterial communities from more arid climates had higher resistance and resilience to drought. Fungal communities were both more resistant and resilient compared to bacteria, but this was independent of other measured environmental factors. Bacterial resilience was partly linked with differences in community composition. Our results suggest that if sites are exposed to increased aridity due to climate change or are managed to promote bacterial diversity, they will have higher bacterial growth rates during drought perturbations, which could potentially promote soil carbon storage.
Decoding the fundamental taxa that decompose crop rhizodeposits (rhizo-C) and/or straw residue (straw-C) is crucial for understanding the role of plant-derived carbon (C) in driving microbial community assembly and consequent C decomposition. Here, a parallel 13C-labeling design, DNA-SIP, and metagenomics techniques were combined to separate maize rhizo-C utilizers from straw-C utilizers in agriculture soils containing both C sources. Also, by comparing bacterial utilizers and their C metabolisms in soils amended with a single C source (e.g., straw-13C only) and two C sources (e.g., straw-13C and rhizo-12C), we investigated the shift of composition and metabolisms of soil bacterial utilizers responding to C sources shift (e.g., compositional and metabolic changes of straw-13C utilizers from soil containing straw-13C to soil containing both straw-13C and rhizo-12C). We revealed i) Proteobacteria predominantly utilized rhizo-13C, while Firmicutes dominated the community specializing in straw-13C decomposition in soil containing both straw-C and rhizo-C; ii) the planted maize (i.e. rhizo-C input) changed community composition and metabolisms of straw-C utilizers, which shifted from K-strategists characterized by an enrichment of lignin-degrading genes to r-strategists which exhibited an enrichment of genes related to polysaccharide degradation. This metabolic shift of straw-C utilizer ultimately reduced straw-13C mineralization by 25.6% when maize was planted. This study identified the distinct utilizers of rhizo-C and straw-C in soils containing both C sources, and shed light on the shift of bacterial community and their metabolic activities responding to the changes of maize-derived C sources.
While carbon flow through soil decomposition channels is well studied, the associated energy fluxes are less considered. In particular, how microbial substrate and energy turnover are linked to higher trophic levels has hardly been investigated to date. Soil nematode communities can serve as a model group to address this knowledge gap. As important microbial grazers nematodes hold a central position in soil food webs. The present study relates the structure and function of the micro-food web to microbial carbon and energy use efficiency. Microbial biomass (phospholipid fatty acids), activity (substrate-induced growth) and energy flow (substrate-induced heat release) are linked with the nematode fauna, i.e. population density, ecological indices and metabolic footprints. Soils from four agricultural sites in central Europe were compared, either long-term unfertilized or fertilized with farmyard manure.
Environmental conditions (e.g. soil nutrients, moisture) influenced microbial biomass, nematode population density and decomposition channels more than fertilization. While all arable soils were dominated by bacteria, at sites with moderate nutrient status fungi also contributed to carbon and energy flow. The life strategies of microorganisms and nematodes showed a comparable pattern: nutrient-poor unfertilized soils comprised more K-strategists, characterized by an efficient but slow metabolism. Conversely, nutrient-rich soils represented fast cycle systems, dominated by copiotrophic microorganisms and strong r-strategists among nematodes. Across soils, microbial energy use efficiency was quite balanced compared to carbon use efficiency. Remarkably, nematode functional groups were closely linked to microbial substrate turnover efficiency, suggesting nematode faunal analysis as a useful proxy. The nematode Channel Index, a measure for soil decomposition channel activity, is proposed as a tool for mapping microbial carbon and energy turnover.