Accumulation of pathogens in soil microbiome can explain long-term fluctuations of legumes in a grassland community.

All plant populations fluctuate in time. Apart from the dynamics imposed by external forces such as climate, these fluctuations can be driven by endogenous processes taking place within the community. In this study, we aimed to identify potential role of soil-borne microbial communities in driving endogenous fluctuations of plant populations. We combined a unique, 35-yr long abundance data of 11 common plant species from a species-rich mountain meadow with development of their soil microbiome (pathogenic fungi, arbuscular mycorrhizal fungi and oomycetes) observed during 4 yr of experimental cultivation in monocultures. Plant species which abundance fluctuated highly in the field (particularly legumes) accumulated plant pathogens in their soil mycobiome. We also identified increasing proportion of mycoparasitic fungi under highly fluctuating legume species, which may indicate an adaptation of these species to mitigate the detrimental effects of pathogens. Our study documented that long-term fluctuations in the abundance of plant species in grassland communities can be explained by the accumulation of plant pathogens in plant-soil microbiome. By contrast, we found little evidence of the role of mutualists in plant population fluctuations. These findings offer new insights for understanding mechanisms driving both long-term vegetation dynamics and patterns of species coexistence and richness.

Phosphorus limitation promotes soil carbon storage in a boreal forest exposed to long-term nitrogen fertilization.

Forests play a crucial role in global carbon cycling by absorbing and storing significant amounts of atmospheric carbon dioxide. Although boreal forests contribute to approximately 45% of the total forest carbon sink, tree growth and soil carbon sequestration are constrained by nutrient availability. Here, we examine if long-term nutrient input enhances tree productivity and whether this leads to carbon storage or whether stimulated microbial decomposition of organic matter limits soil carbon accumulation. Over six decades, nitrogen, phosphorus, and calcium were supplied to a Pinus sylvestris-dominated boreal forest. We found that nitrogen fertilization alone or together with calcium and/or phosphorus increased tree biomass production by 50% and soil carbon sequestration by 65% compared to unfertilized plots. However, the nonlinear relationship observed between tree productivity and soil carbon stock across treatments suggests microbial regulation. When phosphorus was co-applied with nitrogen, it acidified the soil, increased fungal biomass, altered microbial community composition, and enhanced biopolymer degradation capabilities. While no evidence of competition between ectomycorrhizal and saprotrophic fungi has been observed, key functional groups with the potential to reduce carbon stocks were identified. In contrast, when nitrogen was added without phosphorus, it increased soil carbon sequestration because microbial activity was likely limited by phosphorus availability. In conclusion, the addition of nitrogen to boreal forests may contribute to global warming mitigation, but this effect is context dependent.

Symbiotic status alters fungal eco-evolutionary offspring trajectories.

Despite host-fungal symbiotic interactions being ubiquitous in all ecosystems, understanding how symbiosis has shaped the ecology and evolution of fungal spores that are involved in dispersal and colonization of their hosts has been ignored in life-history studies. We assembled a spore morphology database covering over 26,000 species of free-living to symbiotic fungi of plants, insects and humans and found more than eight orders of variation in spore size. Evolutionary transitions in symbiotic status correlated with shifts in spore size, but the strength of this effect varied widely among phyla. Symbiotic status explained more variation than climatic variables in the current distribution of spore sizes of plant-associated fungi at a global scale while the dispersal potential of their spores is more restricted compared to free-living fungi. Our work advances life-history theory by highlighting how the interaction between symbiosis and offspring morphology shapes the reproductive and dispersal strategies among living forms.

GlobalAMFungi: a global database of arbuscular mycorrhizal fungal occurrences from high-throughput sequencing metabarcoding studies.

Arbuscular mycorrhizal (AM) fungi are crucial mutualistic symbionts of the majority of plant species, with essential roles in plant nutrient uptake and stress mitigation. The importance of AM fungi in ecosystems contrasts with our limited understanding of the patterns of AM fungal biogeography and the environmental factors that drive those patterns. This article presents a release of a newly developed global AM fungal dataset (GlobalAMFungi database, https://globalamfungi.com) that aims to reduce this knowledge gap. It contains almost 50 million observations of Glomeromycotinian AM fungal amplicon DNA sequences across almost 8500 samples with geographical locations and additional metadata obtained from 100 original studies. The GlobalAMFungi database is built on sequencing data originating from AM fungal taxon barcoding regions in: i) the small subunit rRNA (SSU) gene; ii) the internal transcribed spacer 2 (ITS2) region; and iii) the large subunit rRNA (LSU) gene. The GlobalAMFungi database is an open source and open access initiative that compiles the most comprehensive atlas of AM fungal distribution. It is designed as a permanent effort that will be continuously updated by its creators and through the collaboration of the scientific community. This study also documented applicability of the dataset to better understand ecology of AM fungal taxa.

Temporal turnover of the soil microbiome composition is guild-specific.

Although spatial and temporal variation are both important components structuring microbial communities, the exact quantification of temporal turnover rates of fungi and bacteria has not been performed to date. In this study, we utilised repeated resampling of bacterial and fungal communities at specific locations across multiple years to describe their patterns and rates of temporal turnover. Our results show that microbial communities undergo temporal change at a rate of 0.010-0.025 per year (in units of Sorensen similarity), and the change in soil is slightly faster in fungi than in bacteria, with bacterial communities changing more rapidly in litter than soil. Importantly, temporal development differs across fungal guilds and bacterial phyla with different ecologies. While some microbial guilds show consistent responses across regional locations, others show site-specific development with weak general patterns. These results indicate that guild-level resolution is important for understanding microbial community assembly, dynamics and responses to environmental factors.

PacBio sequencing of Glomeromycota rDNA: a novel amplicon covering all widely used ribosomal barcoding regions and its applicability in taxonomy and ecology of arbuscular mycorrhizal fungi.

There is no consensus barcoding region for determination of arbuscular mycorrhizal fungal (AMF) taxa. To overcome this obstacle, we have developed an approach to sequence an AMF marker within the ribosome-encoding operon (rDNA) that covers all three widely applied variable molecular markers. Using a nested PCR approach specific to AMF, we amplified a part (c. 2.5 kb) of the rDNA spanning the majority of the small subunit rRNA (SSU) gene, the complete internal transcribed spacer (ITS) region and a part of the large subunit (LSU) rRNA gene. The PCR products were sequenced on the PacBio platform utilizing Single Molecule Real Time (SMRT) sequencing. Employing this method for selected environmental DNA samples, we were able to describe complex AMF communities consisting of various glomeromycotan lineages. We demonstrate the applicability of this new 2.5 kb approach to provide robust phylogenetic assignment of AMF lineages without known sequences from pure cultures and to consolidate information about AMF taxon distributions coming from three widely used barcoding regions into one integrative dataset.

Temperature and pH define the realised niche space of arbuscular mycorrhizal fungi.

The arbuscular mycorrhizal (AM) fungi are a globally distributed group of soil organisms that play critical roles in ecosystem function. However, the ecological niches of individual AM fungal taxa are poorly understood. We collected > 300 soil samples from natural ecosystems worldwide and modelled the realised niches of AM fungal virtual taxa (VT; approximately species-level phylogroups). We found that environmental and spatial variables jointly explained VT distribution worldwide, with temperature and pH being the most important abiotic drivers, and spatial effects generally occurring at local to regional scales. While dispersal limitation could explain some variation in VT distribution, VT relative abundance was almost exclusively driven by environmental variables. Several environmental and spatial effects on VT distribution and relative abundance were correlated with phylogeny, indicating that closely related VT exhibit similar niche optima and widths. Major clades within the Glomeraceae exhibited distinct niche optima, Acaulosporaceae generally had niche optima in low pH and low temperature conditions, and Gigasporaceae generally had niche optima in high precipitation conditions. Identification of the realised niche space occupied by individual and phylogenetic groups of soil microbial taxa provides a basis for building detailed hypotheses about how soil communities respond to gradients and manipulation in ecosystems worldwide.

Symbiosis of isoetid plant species with arbuscular mycorrhizal fungi under aquatic versus terrestrial conditions.

Arbuscular mycorrhizal fungi (AMF) colonize the roots of numerous aquatic and wetland plants, but the establishment and functioning of mycorrhizal symbiosis in submerged habitats have received only little attention. Three pot experiments were conducted to study the interaction of isoetid plants with native AMF. In the first experiment, arbuscular mycorrhizal (AM) symbiosis did not establish in roots of Isoëtes echinospora and I. lacustris, while Littorella uniflora roots were highly colonized. Shoot and root biomass of L. uniflora were, however, not affected by AMF inoculation, and only one of nine AMF isolates significantly increased shoot P concentration. In the second experiment, we compared colonization by three Glomus tetrastratosum isolates of different cultivation history and origin (aquatic versus terrestrial) and their effects on L. uniflora growth and phosphorus nutrition under submerged versus terrestrial conditions. The submerged cultivation considerably slowed, but did not inhibit mycorrhizal root colonization, regardless of isolate identity. Inoculation with any AMF isolate improved plant growth and P uptake under terrestrial, but not submerged conditions. In the final experiment, we compared the communities of AMF established in two cultivation regimes of trap cultures with lake sediments, either submerged on L. uniflora or terrestrial on Zea mays. After 2-year cultivation, we did not detect a significant effect of cultivation regime on AMF community composition. In summary, although submerged conditions do not preclude the development of functional AM symbiosis, the contribution of these symbiotic fungi to the fitness of their hosts seems to be considerably less than under terrestrial conditions.

Altered rhizoctonia assemblages in grasslands on ex-arable land support germination of mycorrhizal generalist, not specialist orchids.

Species-rich seminatural grasslands in Central Europe have suffered a dramatic loss of biodiversity due to conversion to arable land, but vast areas are being restored. Population recovery of orchids, which depend on mycorrhizal fungi for germination, is however limited. We hypothesised that ploughing and fertilisation caused shifts in orchid mycorrhizal communities in soil and restricted orchid germination. We examined edaphic conditions in 60 restored and seminatural grasslands, and germination success in 10 restored grasslands. Using a newly designed primer, we screened the composition of rhizoctonias in soil, seedlings and roots of seven orchid species. Seminatural and restored grasslands differed significantly in nutrient amounts and rhizoctonia assemblages in soil. While Serendipitaceae prevailed in seminatural grasslands with a higher organic matter content, Ceratobasidiaceae were more frequent in phosphorus-rich restored grasslands with increased abundance on younger restored sites. Tulasnellaceae displayed no preference. Germination success in restored grasslands differed significantly between orchid species; two mycorrhizal generalist species germinated with a broad range of rhizoctonias at most restored grasslands, while germination success of specialists was low. Past agricultural practices have a long-lasting effect on soil conditions and orchid mycorrhizal communities. Altered mycorrhizal availability may be the main reason for low germination success of specialist orchid species.

Host preference and network properties in biotrophic plant-fungal associations.

Analytical methods can offer insights into the structure of biological networks, but mechanisms that determine the structure of these networks remain unclear. We conducted a synthesis based on 111 previously published datasets to assess a range of ecological and evolutionary mechanisms that may influence the plant-associated fungal interaction networks. We calculated the relative host effect on fungal community composition and compared nestedness and modularity among different mycorrhizal types and endophytic fungal guilds. We also assessed how plant-fungal network structure was related to host phylogeny, environmental and sampling properties. Orchid mycorrhizal fungal communities responded most strongly to host identity, but the effect of host was similar among all other fungal guilds. Community nestedness, which did not differ among fungal guilds, declined significantly with increasing mean annual precipitation on a global scale. Orchid and ericoid mycorrhizal fungal communities were more modular than ectomycorrhizal and root endophytic communities, with arbuscular mycorrhizal fungi in an intermediate position. Network properties among a broad suite of plant-associated fungi were largely comparable and generally unrelated to phylogenetic distance among hosts. Instead, network metrics were predominantly affected by sampling and matrix properties, indicating the importance of study design in properly inferring ecological patterns.