skip to main content

Title: Grass species identity shapes communities of root and leaf fungi more than elevation

Fungal symbionts can buffer plants from environmental extremes and may affect host capacities to acclimate, adapt, or redistribute under environmental change; however, the distributions of fungal symbionts along abiotic gradients are poorly described. Fungal mutualists should be the most beneficial in abiotically stressful environments, and the structure of networks of plant-fungal interactions likely shift along gradients, even when fungal community composition does not track environmental stress. We sampled 634 unique combinations of fungal endophytes and mycorrhizal fungi, grass species identities, and sampling locations from 66 sites across six replicate altitudinal gradients in the western Colorado Rocky Mountains. The diversity and composition of leaf endophytic, root endophytic, and arbuscular mycorrhizal (AM) fungal guilds and the overall abundance of fungal functional groups (pathogens, saprotrophs, mutualists) tracked grass host identity more closely than elevation. Network structures of root endophytes become more nested and less specialized at higher elevations, but network structures of other fungal guilds did not vary with elevation. Overall, grass species identity had overriding influence on the diversity and composition of above- and belowground fungal endophytes and AM fungi, despite large environmental variation. Therefore, in our system climate change may rarely directly affect fungal symbionts. Instead, fungal symbiont distributions will more » most likely track the range dynamics of host grasses.

« less
; ; ; ; ;
Award ID(s):
Publication Date:
Journal Name:
ISME Communications
Nature Publishing Group
Sponsoring Org:
National Science Foundation
More Like this
  1. Despite colonizing nearly every plant on Earth, foliar fungal symbionts have received little attention in studies on the biogeography of host-associated microbes. Evidence from regional scale studies suggests that foliar fungal symbiont distributions are influenced both by plant hosts and environmental variation in climate and soil resources. However, previous surveys have focused on either one plant host across an environmental gradient or one gradient and multiple plant hosts, making it difficult to disentangle the influence of host identity from the influence of the environment on foliar endophyte communities. We used a culture-based approach to survey fungal symbiont composition in the leaves of nine C3 grass species along replicated elevation gradients in grasslands of the Colorado Rocky Mountains. In these ecosystems, the taxonomic richness and composition of foliar fungal symbionts were mostly structured by the taxonomic identity of the plant host rather than by variation in climate. Plant traits related to size (height and leaf length) were the best predictors of foliar fungal symbiont composition and diversity, and composition did not vary predictably with plant evolutionary history. The largest plants had the most diverse and distinctive fungal communities. These results suggest that across the ~ 300 m elevation range that we sampled,more »foliar fungal symbionts may indirectly experience climate change by tracking the shifting distributions of plant hosts rather than tracking climate directly.« less
  2. Druzhinina, Irina S. (Ed.)
    ABSTRACT Trees associating with different mycorrhizas often differ in their effects on litter decomposition, nutrient cycling, soil organic matter (SOM) dynamics, and plant-soil interactions. For example, due to differences between arbuscular mycorrhizal (AM) and ectomycorrhizal (ECM) tree leaf and root traits, ECM-associated soil has lower rates of C and N cycling and lower N availability than AM-associated soil. These observations suggest that many groups of nonmycorrhizal fungi should be affected by the mycorrhizal associations of dominant trees through controls on nutrient availability. To test this overarching hypothesis, we explored the influence of predominant forest mycorrhizal type and mineral N availability on soil fungal communities using next-generation amplicon sequencing. Soils from four temperate hardwood forests in southern Indiana, United States, were studied; three forests formed a natural gradient of mycorrhizal dominance (100% AM tree basal area to 100% ECM basal area), while the fourth forest contained a factorial experiment testing long-term N addition in both dominant mycorrhizal types. We found that overall fungal diversity, as well as the diversity and relative abundance of plant pathogenic and saprotrophic fungi, increased with greater AM tree dominance. Additionally, tree community mycorrhizal associations explained more variation in fungal community composition than abiotic variables, including soilmore »depth, SOM content, nitrification rate, and mineral N availability. Our findings suggest that tree mycorrhizal associations may be good predictors of the diversity, composition, and functional potential of soil fungal communities in temperate hardwood forests. These observations help explain differing biogeochemistry and community dynamics found in forest stands dominated by differing mycorrhizal types. IMPORTANCE Our work explores how differing mycorrhizal associations of temperate hardwood trees (i.e., arbuscular [AM] versus ectomycorrhizal [ECM] associations) affect soil fungal communities by altering the diversity and relative abundance of saprotrophic and plant-pathogenic fungi along natural gradients of mycorrhizal dominance. Because temperate hardwood forests are predicted to become more AM dominant with climate change, studies examining soil communities along mycorrhizal gradients are necessary to understand how these global changes may alter future soil fungal communities and their functional potential. Ours, along with other recent studies, identify possible global trends in the frequency of specific fungal functional groups responsible for nutrient cycling and plant-soil interactions as they relate to mycorrhizal associations.« less
  3. Plants are typically infected by a consortium of internal fungal associates, including endophytes in their leaves, as well as arbuscular mycorrhizal fungi (AMF) and dark septate endophytes (DSE) in their roots. It is logical that these organisms will interact with each other and the abiotic environment in addition to their host, but there has been little work to date examining the interactions of multiple symbionts within single plant hosts, or how the relationships among symbionts and their host change across environmental conditions. We examined the grassAgrostis capillarisin the context of a climate manipulation experiment in prairies in the Pacific Northwest, USA. Each plant was tested for presence of foliar endophytes in the genusEpichloë, and we measured percent root length colonized (PRLC) by AMF and DSE. We hypothesized that the symbionts in our system would be in competition for host resources, that the outcome of that competition could be driven by the benefit to the host, and that the host plants would be able to allocate carbon to the symbionts in such a way as to maximize fitness benefit within a particular environmental context. We found a correlation between DSE and AMF PRLC across climatic conditions; we also found a fitnessmore »cost to increasing DSE colonization, which was negated by presence ofEpichloëendophytes. These results suggest that selective pressure on the host is likely to favor host/symbiont relationships that structure the community of symbionts in the most beneficial way possible for the host, not necessarily favoring the individual symbiont that is most beneficial to the host in isolation. These results highlight the need for a more integrative, systems approach to the study of host/symbiont consortia.

    « less
  4. Background

    Fungal endophytes inhabit symptomless, living tissues of all major plant lineages to form one of earth’s most prevalent groups of symbionts. Many reproduce from senesced and/or decomposing leaves and can produce extracellular leaf-degrading enzymes, blurring the line between symbiotrophy and saprotrophy. To better understand the endophyte–saprotroph continuum we compared fungal communities and functional traits of focal strains isolated from living leaves to those isolated from leaves after senescence and decomposition, with a focus on foliage of woody plants in five biogeographic provinces ranging from tundra to subtropical scrub forest.


    We cultured fungi from the interior of surface-sterilized leaves that were living at the time of sampling (i.e., endophytes), leaves that were dead and were retained in plant canopies (dead leaf fungi, DLF), and fallen leaves (leaf litter fungi, LLF) from 3–4 species of woody plants in each of five sites in North America. Our sampling encompassed 18 plant species representing two families of Pinophyta and five families of Angiospermae. Diversity and composition of fungal communities within and among leaf life stages, hosts, and sites were compared using ITS-partial LSU rDNA data. We evaluated substrate use and enzyme activity by a subset of fungi isolated only from living tissues vs. fungi isolatedmore »only from non-living leaves.


    Across the diverse biomes and plant taxa surveyed here, culturable fungi from living leaves were isolated less frequently and were less diverse than those isolated from non-living leaves. Fungal communities in living leaves also differed detectably in composition from communities in dead leaves and leaf litter within focal sites and host taxa, regardless of differential weighting of rare and abundant fungi. All focal isolates grew on cellulose, lignin, and pectin as sole carbon sources, but none displayed ligninolytic or pectinolytic activityin vitro. Cellulolytic activity differed among fungal classes. Within Dothideomycetes, activity differed significantly between fungi from living vs. non-living leaves, but such differences were not observed in Sordariomycetes.


    Although some fungi with endophytic life stages clearly persist for periods of time in leaves after senescence and incorporation into leaf litter, our sampling across diverse biomes and host lineages detected consistent differences between fungal assemblages in living vs. non-living leaves, reflecting incursion by fungi from the leaf exterior after leaf death and as leaves begin to decompose. However, fungi found only in living leaves do not differ consistently in cellulolytic activity from those fungi detected thus far only in dead leaves. Future analyses should consider Basidiomycota in addition to the Ascomycota fungi evaluated here, and should explore more dimensions of functional traits and persistence to further define the endophytism-to-saprotrophy continuum.

    « less
  5. Abstract While the relationship between plant and microbial diversity has been well studied in grasslands, less is known about similar relationships in forests, especially for obligately symbiotic arbuscular mycorrhizal (AM) fungi. To assess the effect of varying tree diversity on microbial alpha- and beta-diversity, we sampled soil from plots in a high-density tree diversity experiment in Minnesota, USA three years after establishment. Three of 12 tree species are AM hosts; the other nine primarily associate with ectomycorrhizal fungi. We used phospho- and neutral lipid fatty acid analysis to characterize the biomass and functional identity of the whole soil bacterial and fungal community and high throughput sequencing to identify the species-level richness and composition of the AM fungal community. We found that plots of differing tree composition had different bacterial and fungal communities; plots with conifers, and especially Juniperus virginiana, had lower densities of several bacterial groups. In contrast, plots with a higher density or diversity of AM hosts showed no sign of greater AM fungal abundance or diversity. Our results indicate that early responses to plant diversity vary considerably across microbial groups, with AM fungal communities potentially requiring longer timescales to respond to changes in host tree diversity.