Extreme rainfall affects assembly of the root-associated fungal community.
ABSTRACT: Global warming is resulting in increased frequency of weather extremes. Root-associated fungi play important roles in terrestrial biogeochemical cycling processes, but the way in which they are affected by extreme weather is unclear. Here, we performed long-term field monitoring of the root-associated fungus community of a short rotation coppice willow plantation, and compared community dynamics before and after a once in 100 yr rainfall event that occurred in the UK in 2012. Monitoring of the root-associated fungi was performed over a 3-yr period by metabarcoding the fungal internal transcribed spacer (ITS) region. Repeated soil testing and continuous climatic monitoring supplemented community data, and the relative effects of environmental and temporal variation were determined on the root-associated fungal community. Soil saturation and surface water were recorded throughout the early growing season of 2012, following extreme rainfall. This was associated with a crash in the richness and relative abundance of ectomycorrhizal fungi, with each declining by over 50%. Richness and relative abundance of saprophytes and pathogens increased. We conclude that extreme rainfall events may be important yet overlooked determinants of root-associated fungal community assembly. Given the integral role of ectomycorrhizal fungi in biogeochemical cycles, these events may have considerable impacts upon the functioning of terrestrial ecosystems.
Project description:Rapid responses of microbial biomass and community composition following a precipitation event have been reported for soil bacteria and fungi, but measurements characterizing ectomycorrhizal fungi remain limited. The response of ectomycorrhizal fungi after a precipitation event is crucial to understanding biogeochemical cycles and plant nutrition. Here, we examined changes in ectomycorrhizal formation, diversity, and community composition at the end of a summer drought and following precipitation events in a conifer-oak mixed forest under a semiarid, Mediterranean-type climate in CA, USA. To study the effects of different amounts of precipitation, a water addition treatment was also undertaken. Ectomycorrhizal fungal diversity and community composition changed within 6 days following precipitation, with increased simultaneous mortality and re-growth. Ectomycorrhizal diversity increased and community composition changed both in the natural rainfall (less than 10 mm) and water addition (50 mm) treatments, but larger decreases in ectomycorrhizal diversity were observed from 9 to 16 days after precipitation in the water addition treatment. The changes were primarily a shift in richness and abundance of Basidiomycota species, indicating higher drought sensitivity of Basidiomycota species compared with Ascomycota species. Our results indicate that ectomycorrhizal formation, diversity, and community composition rapidly respond to both precipitation events and to the amount of precipitation. These changes affect ecosystem functions, such as nutrient cycling, decomposition, and plant nutrient uptake, in semiarid regions.
Project description:Plant-mycorrhizal fungal interactions are ubiquitous in forest ecosystems. While ectomycorrhizal plants and their fungi generally dominate temperate forests, arbuscular mycorrhizal symbiosis is common in the tropics. In subtropical regions, however, ectomycorrhizal and arbuscular mycorrhizal plants co-occur at comparable abundances in single forests, presumably generating complex community structures of root-associated fungi. To reveal root-associated fungal community structure in a mixed forest of ectomycorrhizal and arbuscular mycorrhizal plants, we conducted a massively-parallel pyrosequencing analysis, targeting fungi in the roots of 36 plant species that co-occur in a subtropical forest. In total, 580 fungal operational taxonomic units were detected, of which 132 and 58 were probably ectomycorrhizal and arbuscular mycorrhizal, respectively. As expected, the composition of fungal symbionts differed between fagaceous (ectomycorrhizal) and non-fagaceous (possibly arbuscular mycorrhizal) plants. However, non-fagaceous plants were associated with not only arbuscular mycorrhizal fungi but also several clades of ectomycorrhizal (e.g., Russula) and root-endophytic ascomycete fungi. Many of the ectomycorrhizal and root-endophytic fungi were detected from both fagaceous and non-fagaceous plants in the community. Interestingly, ectomycorrhizal and arbuscular mycorrhizal fungi were concurrently detected from tiny root fragments of non-fagaceous plants. The plant-fungal associations in the forest were spatially structured, and non-fagaceous plant roots hosted ectomycorrhizal fungi more often in the proximity of ectomycorrhizal plant roots. Overall, this study suggests that belowground plant-fungal symbiosis in subtropical forests is complex in that it includes "non-typical" plant-fungal combinations (e.g., ectomycorrhizal fungi on possibly arbuscular mycorrhizal plants) that do not fall within the conventional classification of mycorrhizal symbioses, and in that associations with multiple functional (or phylogenetic) groups of fungi are ubiquitous among plants. Moreover, ectomycorrhizal fungal symbionts of fagaceous plants may "invade" the roots of neighboring non-fagaceous plants, potentially influencing the interactions between non-fagaceous plants and their arbuscular-mycorrhizal fungal symbionts at a fine spatial scale.
Project description:Root-associated fungal communities are important components in ecosystem processes, impacting plant growth and vigor by influencing the quality, direction, and flow of nutrients and water between plants and fungi. Linkages of plant phenological characteristics with belowground root-associated fungal communities have rarely been investigated, and thus our aim was to search for an interplay between contrasting phenology of host ectomycorrhizal trees from the same location and root-associated fungal communities (ectomycorrhizal, endophytic, saprotrophic and pathogenic root-associated fungi) in young and in adult silver fir trees. The study was performed in a managed silver fir forest site. Twenty-four soil samples collected under two phenologically contrasting silver fir groups were analyzed for differences in root-associated fungal communities using Illumina sequencing of a total root-associated fungal community. Significant differences in beta diversity and in mean alpha diversity were confirmed for overall community of ectomycorrhizal root-associated fungi, whereas for ecologically different non-ectomycorrhizal root-associated fungal communities the differences were significant only for beta diversity and not for mean alpha diversity. At genus level root-associated fungal communities differed significantly between early and late flushing young and adult silver fir trees. We discuss the interactions through which the phenology of host plants either drives or is driven by the root-associated fungal communities in conditions of a sustainably co-naturally managed silver fir forest.
Project description:Most terrestrial plants interact with diverse clades of mycorrhizal and root-endophytic fungi in their roots. Through belowground plant-fungal interactions, dominant plants can benefit by interacting with host-specific mutualistic fungi and proliferate in a community based on positive plant-mutualistic fungal feedback. On the other hand, subordinate plant species may persist in the community by sharing other sets (functional groups) of fungal symbionts with each other. Therefore, revealing how diverse clades of root-associated fungi are differentially hosted by dominant and subordinate plant species is essential for understanding plant community structure and dynamics. Based on 454-pyrosequencing, we determined the community composition of root-associated fungi on 36 co-occurring plant species in an oak-dominated forest in northern Japan and statistically evaluated the host preference phenotypes of diverse mycorrhizal and root-endophytic fungi. An analysis of 278 fungal taxa indicated that an ectomycorrhizal basidiomycete fungus in the genus Lactarius and a possibly endophytic ascomycete fungus in the order Helotiales significantly favored the dominant oak (Quercus) species. In contrast, arbuscular mycorrhizal fungi were generally shared among subordinate plant species. Although fungi with host preferences contributed to the compartmentalization of belowground plant-fungal associations, diverse clades of ectomycorrhizal fungi and possible root endophytes were associated not only with the dominant Quercus but also with the remaining plant species. Our findings suggest that dominant-ectomycorrhizal and subordinate plant species can host different subsets of root-associated fungi, and diverse clades of generalist fungi can counterbalance the compartmentalization of plant-fungal associations. Such insights into the overall structure of belowground plant-fungal associations will help us understand the mechanisms that facilitate the coexistence of plant species in natural communities.
Project description:In terrestrial ecosystems, plant roots are colonized by various clades of mycorrhizal and endophytic fungi. Focused on the root systems of an oak-dominated temperate forest in Japan, we used 454 pyrosequencing to explore how phylogenetically diverse fungi constitute an ecological community of multiple ecotypes. In total, 345 operational taxonomic units (OTUs) of fungi were found from 159 terminal-root samples from 12 plant species occurring in the forest. Due to the dominance of an oak species (Quercus serrata), diverse ectomycorrhizal clades such as Russula, Lactarius, Cortinarius, Tomentella, Amanita, Boletus, and Cenococcum were observed. Unexpectedly, the root-associated fungal community was dominated by root-endophytic ascomycetes in Helotiales, Chaetothyriales, and Rhytismatales. Overall, 55.3% of root samples were colonized by both the commonly observed ascomycetes and ectomycorrhizal fungi; 75.0% of the root samples of the dominant Q. serrata were so cocolonized. Overall, this study revealed that root-associated fungal communities of oak-dominated temperate forests were dominated not only by ectomycorrhizal fungi but also by diverse root endophytes and that potential ecological interactions between the two ecotypes may be important to understand the complex assembly processes of belowground fungal communities.
Project description:Root-associated fungi, including ectomycorrhizal and root-endophytic fungi, are among the most diverse and important belowground plant symbionts in dipterocarp rainforests. Our study aimed to reveal the biodiversity, host association, and community structure of ectomycorrhizal Basidiomycota and root-associated Ascomycota (including root-endophytic Ascomycota) in a lowland dipterocarp rainforest in Southeast Asia. The host plant chloroplast ribulose-1,5-bisphosphate carboxylase/oxygenase large subunit (rbcL) region and fungal internal transcribed spacer 2 (ITS2) region were sequenced using tag-encoded, massively parallel 454 pyrosequencing to identify host plant and root-associated fungal taxa in root samples. In total, 1245 ascomycetous and 127 putative ectomycorrhizal basidiomycetous taxa were detected from 442 root samples. The putative ectomycorrhizal Basidiomycota were likely to be associated with closely related dipterocarp taxa to greater or lesser extents, whereas host association patterns of the root-associated Ascomycota were much less distinct. The community structure of the putative ectomycorrhizal Basidiomycota was possibly more influenced by host genetic distances than was that of the root-associated Ascomycota. This study also indicated that in dipterocarp rainforests, root-associated Ascomycota were characterized by high biodiversity and indistinct host association patterns, whereas ectomycorrhizal Basidiomycota showed less biodiversity and a strong host phylogenetic preference for dipterocarp trees. Our findings lead to the working hypothesis that root-associated Ascomycota, which might be mainly represented by root-endophytic fungi, have biodiversity hotspots in the tropics, whereas biodiversity of ectomycorrhizal Basidiomycota increases with host genetic diversity.
Project description:Background. The extent to which ectomycorrhizal fungi mediate primary production, carbon storage, and nutrient remineralization in terrestrial ecosystems depends upon fungal community composition. However, the factors that govern community composition at the root system scale are not well understood. Here, we explore a potential tradeoff between ectomycorrhizal fungal competitive ability and enzymatic function. Methods. We grew Pinus muricata (Bishop Pine) seedlings in association with ectomycorrhizal fungi from three different genera in a fully factorial experimental design. We measured seedling growth responses, ectomycorrhizal abundance, and the root tip activity of five different extracellular enzymes involved in the mobilization of carbon and phosphorus. Results. We found an inverse relationship between competitiveness, quantified based on relative colonization levels, and enzymatic activity. Specifically, Thelephora terrestris, the dominant fungus, had the lowest enzyme activity levels, while Suillus pungens, the least dominant fungus, had the highest. Discussion. Our results identify a tradeoff between competition and function in ectomycorrhizal fungi, perhaps mediated by the competing energetic demands associated with competitive interactions and enzymatic production. These data suggest that mechanisms such as active partner maintenance by host trees may be important to maintaining "high-quality" ectomycorrhizal fungal partners in natural systems.
Project description:Diverse clades of mycorrhizal and endophytic fungi are potentially involved in competitive or facilitative interactions within host-plant roots. We investigated the potential consequences of these ecological interactions on the assembly process of root-associated fungi by examining the co-occurrence of pairs of fungi in host-plant individuals. Based on massively-parallel pyrosequencing, we analyzed the root-associated fungal community composition for each of the 249 Quercus serrata and 188 Quercus glauca seedlings sampled in a warm-temperate secondary forest in Japan. Pairs of fungi that co-occurred more or less often than expected by chance were identified based on randomization tests. The pyrosequencing analysis revealed that not only ectomycorrhizal fungi but also endophytic fungi were common in the root-associated fungal community. Intriguingly, specific pairs of these ectomycorrhizal and endophytic fungi showed spatially aggregated patterns, suggesting the existence of facilitative interactions between fungi in different functional groups. Due to the large number of fungal pairs examined, many of the observed aggregated/segregated patterns with very low P values (e.g., < 0.005) turned non-significant after the application of a multiple comparison method. However, our overall results imply that the community structures of ectomycorrhizal and endophytic fungi could influence each other through interspecific competitive/facilitative interactions in root. To test the potential of host-plants' control of fungus-fungus ecological interactions in roots, we further examined whether the aggregated/segregated patterns could vary depending on the identity of host plant species. Potentially due to the physiological properties shared between the congeneric host plant species, the sign of hosts' control was not detected in the present study. The pyrosequencing-based randomization analyses shown in this study provide a platform of the high-throughput investigation of fungus-fungus interactions in plant root systems.
Project description:In natural forests, hundreds of fungal species colonize plant roots. The preference or specificity for partners in these symbiotic relationships is a key to understanding how the community structures of root-associated fungi and their host plants influence each other. In an oak-dominated forest in Japan, we investigated the root-associated fungal community based on a pyrosequencing analysis of the roots of 33 plant species. Of the 387 fungal taxa observed, 153 (39.5%) were identified on at least two plant species. Although many mycorrhizal and root-endophytic fungi are shared between the plant species, the five most common plant species in the community had specificity in their association with fungal taxa. Likewise, fungi displayed remarkable variation in their association specificity for plants even within the same phylogenetic or ecological groups. For example, some fungi in the ectomycorrhizal family Russulaceae were detected almost exclusively on specific oak (Quercus) species, whereas other Russulaceae fungi were found even on "non-ectomycorrhizal" plants (e.g., Lyonia and Ilex). Putatively endophytic ascomycetes in the orders Helotiales and Chaetothyriales also displayed variation in their association specificity and many of them were shared among plant species as major symbionts. These results suggest that the entire structure of belowground plant-fungal associations is described neither by the random sharing of hosts/symbionts nor by complete compartmentalization by mycorrhizal type. Rather, the colonization of multiple types of mycorrhizal fungi on the same plant species and the prevalence of diverse root-endophytic fungi may be important features of belowground linkage between plant and fungal communities.
Project description:Fine root litter is the principal source of carbon stored in forest soils and a dominant source of carbon for fungal decomposers. Differences in decomposer capacity between fungal species may be important determinants of fine-root decomposition rates. Variable-retention harvesting (VRH) provides refuge for ectomycorrhizal fungi, but its influence on fine-root decomposers is unknown, as are the effects of functional shifts in these fungal communities on carbon cycling. We compared fungal communities decomposing fine roots (in litter bags) under VRH, clear-cut, and uncut stands at two sites (6 and 13 years postharvest) and two decay stages (43 days and 1 year after burial) in Douglas fir forests in coastal British Columbia, Canada. Fungal species and guilds were identified from decomposed fine roots using high-throughput sequencing. Variable retention had short-term effects on ?-diversity; harvest treatment modified the fungal community composition at the 6-year-postharvest site, but not at the 13-year-postharvest site. Ericoid and ectomycorrhizal guilds were not more abundant under VRH, but stand age significantly structured species composition. Guild composition varied by decay stage, with ruderal species later replaced by saprotrophs and ectomycorrhizae. Ectomycorrhizal abundance on decomposing fine roots may partially explain why fine roots typically decompose more slowly than surface litter. Our results indicate that stand age structures fine-root decomposers but that decay stage is more important in structuring the fungal community than shifts caused by harvesting. The rapid postharvest recovery of fungal communities decomposing fine roots suggests resiliency within this community, at least in these young regenerating stands in coastal British Columbia.IMPORTANCE Globally, fine roots are a dominant source of carbon in forest soils, yet the fungi that decompose this material and that drive the sequestration or respiration of this carbon remain largely uncharacterized. Fungi vary in their capacity to decompose plant litter, suggesting that fungal community composition is an important determinant of decomposition rates. Variable-retention harvesting is a forestry practice that modifies fungal communities by providing refuge for ectomycorrhizal fungi. We evaluated the effects of variable retention and clear-cut harvesting on fungal communities decomposing fine roots at two sites (6 and 13 years postharvest), at two decay stages (43 days and 1 year), and in uncut stands in temperate rainforests. Harvesting impacts on fungal community composition were detected only after 6 years after harvest. We suggest that fungal community composition may be an important factor that reduces fine-root decomposition rates relative to those of above-ground plant litter, which has important consequences for forest carbon cycling.