Fungal Perspective of Pine and Oak Colonization in Mediterranean Degraded Ecosystems

Forest restoration has become one of the most important challenges for restoration ecology in the recent years. In this regard, soil fungi are fundamental drivers of forest ecosystem processes, with significant implications for plant growth and survival. However, the post-disturbance recovery of belowground communities has been rarely assessed, especially in highly degraded systems such as mines. Our aim was to compare forests and mined systems for biomass and structure of fungal communities in soil during early stages of tree establishment after disturbance. We performed ergosterol analysis and PacBio and Illumina sequencing of internal transcribed spacer 2 amplicons across soil layers in P. sylvestris, Q. robur and Q. ilex (holm oak) forests and naturally revegetated mined sites. In pine forests, total fungal biomass was significantly higher in litter and humus compared to mineral layers, with dominance of the mycorrhizal genera Tomentella, Inocybe and Tricholoma. Conversely, in oak forests the most abundant mycorrhizal genera were Tomentella, Cortinarius and Sebacina, but the biomass of saprotrophic fungi was greater in the litter layer compared to mycorrhizal fungi, with the genus Preussia being the most abundant. In the revegetated mined sites, ectomycorrhizal fungi dominated in the humus and mineral layers, with the mycorrhizal genus Oidiodendron being dominant. In contrast, in holm oak forests saprotrophic fungi dominated both soil humus and mineral layers, with the genera of Alternaria, Bovista and Mycena dominating the soil humus forest layer, while the genus Cadophora dominated the mineral layer. The habitat-specific differences in soil fungal community composition and putative functions suggest that an understanding of soil–plant–microbial interactions for different tree species and use of specific soil/litter inoculum upon planting/seeding might help to increase the effectiveness of tree restoration strategies in Mediterranean degraded sites.

Inoculum Sources Modulate Mycorrhizal Inoculation Effect on Tamarix articulata Development and Its Associated Rhizosphere Microbiota

(1) Background: Soil degradation is an increasingly important problem in many parts of the world, particularly in arid and semiarid areas. Arbuscular mycorrhizal fungi (AMF) isolated from arid soils are recognized to be better adapted to these edaphoclimatic conditions than exogenous ones. Nevertheless, little is known about the importance of AMF inoculum sources on Tamarix articulata development in natural saline soils. Therefore, the current study aims at investigating the efficiency of two AMF-mixed inoculums on T. articulata growth, with consideration of its rhizosphere microbiota. (2) Methods: indigenous inoculum made of strains originating from saline soils and a commercial one were used to inoculate T. articulata in four saline soils with different salinity levels under microcosm conditions with evaluation of rhizosphere microbial biomasses. (3) Results: Our findings showed that indigenous inoculum outperforms the commercial one by 80% for the mycorrhizal rate and 40% for plant biomasses, which are correlated with increasing shoot phosphorus content. Soil microbial biomasses increased significantly with indigenous mycorrhizal inoculum in the most saline soil with 46% for AMF, 25% for saprotrophic fungi and 15% for bacterial biomasses. (4) Conclusion: Present results open the way towards the preferential use of mycorrhizal inoculum, based on native AMF, to perform revegetation and to restore the saline soil microbiota.

Heterospecific Neighbor Plants Impact Root Microbiome Diversity and Molecular Function of Root Fungi

Within the forest community, competition and facilitation between adjacent-growing conspecific and heterospecific plants are mediated by interactions involving common mycorrhizal networks. The ability of plants to alter their neighbor’s microbiome is well documented, but the molecular biology of plant-fungal interactions during competition and facilitation has not been previously examined. We used a common soil-plant bioassay experiment to study molecular plant-microbial interactions among rhizosphere communities associated with Pinus taeda (native host) and Populus trichocarpa (non-native host). Gene expression of interacting fungal and bacterial rhizosphere communities was compared among three plant-pairs: Populus growing with Populus, Populus with Pinus, and Pinus with Pinus. Our results demonstrate that heterospecific plant partners affect the assembly of root microbiomes, including the changes in the structure of host specific community. Comparative metatranscriptomics reveals that several species of ectomycorrhizal fungi (EMF) and saprotrophic fungi exhibit different patterns of functional and regulatory gene expression with these two plant hosts. Heterospecific plants affect the transcriptional expression pattern of EMF host-specialists (e.g., Pinus-associated Suillus spp.) on both plant species, mainly including the genes involved in the transportation of amino acids, carbohydrates, and inorganic ions. Alteration of root microbiome by neighboring plants may help regulate basic plant physiological processes via modulation of molecular functions in the root microbiome.

Fungal Interactions Matter: Tricholoma matsutake Domination Affect Fungal Diversity and Function in Temperate Deciduous Forest Soils

Tricholoma matsutake forms a symbiotic association with coniferous trees, developing mycelial aggregations, called ‘shiro’, which are characterized by distinct chemical and physical properties from nearby forest bulk soil. The fungal diversity living in shiro soil play key roles in nutrient cycles for this economically important mushroom, but have not been profiled across large spatial and environmental gradients. Samples of shiro and non-shiro (nearby bulk soil) were taken from five field sites where sporocarps naturally formed. Phospholipid fatty acids (PLFA) and Illumina MiSeq sequencing were combined to identify fungal biomass and community structure. Matsutake dominated in the shiro, which had a significantly reduced saprotrophic fungi biomass compared to non-shiro soil. Fungal diversity was negatively correlated with the relative abundance of T. matsutake in the shiro soil. The fungal community in the shiro was characterized by similar fungal species composition in most samples regardless of forest types. Matsutake coexisted with a specific fungal community due to competition or nutrient interactions. Oidiodendron was positively correlated with the abundance of T. matsutake, commonly cohabitant in the shiro. In contrast, Helotiales and Mortierella were negatively correlated with T. matsutake, both of which commonly inhabit the non-shiro soil but do not occur in shiro soils. We conclude that T. matsutake generate a dominance effect to shape the fungal community and diversity in shiro soil across distinctive forest types.

Soil Layers Matter: Vertical Stratification of Root-Associated Fungal Assemblages in Temperate Forests Reveals Differences in Habitat Colonization

Ectomycorrhizal and saprotrophic fungi play pivotal roles in ecosystem functioning. Here, we studied the vertical differentiation of root-associated fungi (RAF) in temperate forests. We analysed RAF assemblages in the organic and mineral soil from 150 experimental forest plots across three biogeographic regions spanning a distance of about 800 km. Saprotrophic RAF showed the highest richness in organic and symbiotrophic RAF in mineral soil. Symbiotrophic RAF exhibited higher relative abundances than saprotrophic fungi in both soil layers. Beta-diversity of RAF was mainly due to turnover between organic and mineral soil and showed regional differences for symbiotrophic and saprotrophic fungi. Regional differences were also found for different phylogenetic levels, i.e., fungal orders and indicator species in the organic and mineral soil, supporting that habitat conditions strongly influence differentiation of RAF assemblages. Important exceptions were fungal orders that occurred irrespective of the habitat conditions in distinct soil layers across the biogeographic gradient: Russulales and Cantharellales (ectomycorrhizal fungi) were enriched in RAF assemblages in mineral soil, whereas saprotrophic Polyporales and Sordariales and ectomycorrhizal Boletales were enriched in RAF assemblages in the organic layer. These results underpin a phylogenetic signature for niche partitioning at the rank of fungal orders and suggest that RAF assembly entails two strategies encompassing flexible and territorial habitat colonization by different fungal taxa.

Impact of nitrogen and phosphorus addition on resident soil and root mycobiomes in beech forests

N and P are essential macronutrients for all organisms. How shifts in the availability of N or P affect fungal communities in temperate forests is not well understood. Here, we conducted a factorial P × N fertilization experiment to disentangle the effects of nutrient availability on soil-residing, root-associated, and ectomycorrhizal fungi in beech (Fagus sylvatica) forests differing in P availability. We tested the hypotheses that in P-poor forests, P fertilization leads to enhanced fungal diversity in soil and roots, resulting in enhanced P nutrition of beech, and that N fertilization aggravates P shortages, shifting the fungal communities toward nitrophilic species. In response to fertilizer treatments (1 × 50 kg ha−1 P and 5 × 30 kg ha−1 N within 2 years), the labile P fractions increased in soil and roots, regardless of plant-available P in soil. Root total P decreased in response to N fertilization and root total P increased in response to P addition at the low P site. Ectomycorrhizal species richness was unaffected by fertilizer treatments, but the relative abundances of ectomycorrhizal fungi increased in response to P or N addition. At the taxon level, fungal assemblages were unaffected by fertilizer treatments, but at the order level, different response patterns for saprotrophic fungi among soil and ectomycorrhizal fungi on roots were found. Boletales increased in response to P, and Russulales decreased under N + P addition. Our results suggest that trait conservatism in related species afforded resistance of the resident mycobiome composition to nutritional imbalances.

Limited resilience of the soil microbiome to mechanical compaction within four growing seasons of agricultural management

Soil compaction affects many soil functions, but we have little information on the resistance and resilience of soil microorganisms to this disturbance. Here, we present data on the response of soil microbial diversity to a single compaction event and its temporal evolution under different agricultural management systems during four growing seasons. Crop yield was reduced (up to −90%) in the first two seasons after compaction, but mostly recovered in subsequent seasons. Soil compaction increased soil bulk density (+15%), and decreased air permeability (−94%) and gas diffusion (−59%), and those properties did not fully recover within four growing seasons. Soil compaction induced cropping system-dependent shifts in microbial community structures with little resilience over the four growing seasons. Microbial taxa sensitive to soil compaction were detected in all major phyla. Overall, anaerobic prokaryotes and saprotrophic fungi increased in compacted soils, whereas aerobic prokaryotes and plant-associated fungi were mostly negatively affected. Most measured properties showed large spatial variability across the replicated blocks, demonstrating the dependence of compaction effects on initial conditions. This study demonstrates that soil compaction is a disturbance that can have long-lasting effects on soil properties and soil microorganisms, but those effects are not necessarily aligned with changes in crop yield.

Evolution of the Mode of Nutrition in Symbiotic and Saprotrophic Fungi in Forest Ecosystems

In this review, we highlight the main insights that have been gathered from recent developments using large-scale genomics of fungal saprotrophs and symbiotrophs (including ectomycorrhizal and orchid and ericoid mycorrhizal fungi) inhabiting forest ecosystems. After assessing the goals and motivations underlying our approach, we explore our current understanding of the limits and future potential of using genomics to understand the ecological roles of these forest fungi. Comparative genomics unraveled the molecular machineries involved in lignocellulose decomposition in wood decayers, soil and litter saprotrophs, and mycorrhizal symbionts. They also showed that transitions from saprotrophy to mutualism entailed widespread losses of lignocellulose-degrading enzymes; diversification of novel, lineage-specific symbiosis-induced genes; and convergent evolution of genetic innovations that facilitate the accommodation of mutualistic symbionts within their plant hosts. We also identify the major questions that remain unanswered and propose new avenues of genome-based research to understand the role of soil fungi in sustainable forest ecosystems. Expected final online publication date for the Annual Review of Ecology, Evolution, and Systematics, Volume 52 is November 2021. Please see http://www.annualreviews.org/page/journal/pubdates for revised estimates.