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Peay, Kabir G.

Publications and source records attributed to Peay, Kabir G..

Arbuscular mycorrhizal fungi equalize differences in plant fitness and facilitate plant species coexistence through niche differentiation

Mycorrhizal fungi are essential to the establishment of the vast majority of plant species but are often conceptualized with contradictory roles in plant community assembly. On the one hand, host-specific mycorrhizal fungi may allow a plant to be competitively dominant by enhancing growth. On the other hand, host-specific mycorrhizal fungi with different functional capabilities may increase nutrient niche partitioning, allowing plant species to coexist. Here, to resolve the balance of these two contradictory forces, we used a controlled greenhouse study to manipulate the presence of two main types of mycorrhizal fungus, ectomycorrhizal fungi and arbuscular mycorrhizal fungi, and used a range of conspecific and heterospecific competitor densities to investigate the role of mycorrhizal fungi in plant competition and coexistence. We find that the presence of arbuscular mycorrhizal fungi equalizes fitness differences between plants and stabilizes competition to create conditions for host species coexistence. Furthermore, our results show how below-ground mutualisms can shift outcomes of plant competition and that a holistic view of plant communities that incorporates their mycorrhizal partners is important in predicting plant community dynamics.

09 BIOMASS FUELS↗

Ectomycorrhizal fungi alter soil food webs and the functional potential of bacterial communities

Most of Earth’s trees rely on critical soil nutrients that ectomycorrhizal fungi (EcMF) liberate and provide, and all of Earth’s land plants associate with bacteria that help them survive in nature. Yet, our understanding of how the presence of EcMF modifies soil bacterial communities, soil food webs, and root chemistry requires direct experimental evidence to comprehend the effects that EcMF may generate in the belowground plant microbiome. To this end, we grew Pinus muricata plants in soils that were either inoculated with EcMF and native forest bacterial communities or only native bacterial communities. We then profiled the soil bacterial communities, applied metabolomics and lipidomics, and linked omics data sets to understand how the presence of EcMF modifies belowground biogeochemistry, bacterial community structure, and their functional potential. We found that the presence of EcMF (i) enriches soil bacteria linked to enhanced plant growth in nature, (ii) alters the quantity and composition of lipid and non-lipid soil metabolites, and (iii) modifies plant root chemistry toward pathogen suppression, enzymatic conservation, and reactive oxygen species scavenging. Using this multi-omic approach, we therefore show that this widespread fungal symbiosis may be a common factor for structuring soil food webs.

59 BASIC BIOLOGICAL SCIENCES↗

Potential for functional divergence in ectomycorrhizal fungal communities across a precipitation gradient

Abstract Functional traits influence the assembly of microbial communities, but identifying these traits in the environment has remained challenging. We studied ectomycorrhizal fungal (EMF) communities inhabiting Populus trichocarpa roots distributed across a precipitation gradient in the Pacific Northwest, USA. We profiled these communities using taxonomic (meta-barcoding) and functional (metagenomic) approaches. We hypothesized that genes involved in fungal drought-stress tolerance and fungal mediated plant water uptake would be most abundant in drier soils. We were unable to detect support for this hypothesis; instead, the abundance of genes involved in melanin synthesis, hydrophobins, aquaporins, trehalose-synthases, and other gene families exhibited no significant shifts across the gradient. Finally, we studied variation in sequence homology for certain genes, finding that fungal communities in dry soils are composed of distinct aquaporin and hydrophobin gene sequences. Altogether, our results suggest that while EMF communities exhibit significant compositional shifts across this gradient, coupled functional turnover, at least as inferred using community metagenomics is limited. Accordingly, the consequences of these distinct EMF communities on plant water uptake remain critically unknown, and future studies targeting the expression of genes involved in drought stress tolerance are required.

59 BASIC BIOLOGICAL SCIENCES↗

Woodland wildfire enables fungal colonization of encroaching Douglas‐fir

Abstract Self‐reinforcing differences in fire frequency help closed‐canopy forests, which resist fire, and open woodlands, which naturally burn often, to co‐occur stably at landscape scales. Forest tree seedlings, which could otherwise encroach and overgrow woodlands, are killed by regular fire, yet fire has other effects that may also influence these feedbacks. In particular, many forest trees require symbiotic ectomycorrhizal fungi in order to establish. By restructuring soil fungal communities, fire might affect the availability of symbionts or the potential for symbiont sharing between encroaching trees and woodland vegetation. To investigate this possibility, we performed a soil bioassay experiment using inoculum from burned and unburned oak woodlands and Douglas‐fir forests. We examined how fire, ecosystem type, and neighboring heterospecific seedlings affect fungal root community assembly of Douglas‐firs and oaks. We asked whether heterospecific seedlings facilitated fungal colonization of seedling roots in non‐native soil, and if so, whether fire influenced this interaction. External fungal colonization of oak roots was more influenced by fire and ecosystem type than by the presence of a Douglas‐fir, and oaks increased the likelihood that Douglas‐fir roots would be colonized by fungi in oak woodland soil. Yet, fire increased colonization of Douglas‐fir in oak soil, diminishing the otherwise crucial role played by oak facilitation. Fire also strengthened the positive effect of Douglas‐firs on oak root‐associated fungal diversity in Douglas‐fir forest soil. Prior work shows that fire supports woodland ecosystems by stemming recruitment of encroaching seedlings. Here, we find evidence that it may contrastingly reduce fungal limitation of invasive seedling growth and establishment, otherwise relieved only by facilitation. Future work can investigate how these opposing effects might contribute to the net impact of changes in fire regime on landcover stability. Read the free Plain Language Summary for this article on the Journal blog.

54 ENVIRONMENTAL SCIENCES↗

Mycorrhizal nutrient acquisition strategies shape tree competition and coexistence dynamics

Mycorrhizal fungi with different nutrient acquisition strategies influence plant species performance and physiology, thereby defining their trophic niche. This might drive resource competition dynamics that cumulatively impact tree species coexistence, but few manipulative experiments have directly tested this. Combining surveys and experiments in a modern coexistence theory framework, we tested how variation in mycorrhizal strategies and nutrient conditions affects plant competitive outcomes. We focused on two genera of co-occurring tree species with different mycorrhizal states: Acer (arbuscular mycorrhizal, AM) and Populus (dual mycorrhizal, but often considered predominantly ectomycorrhizal, EM). The EM and AM fungal responsiveness in Populus species varied with latitude and nitrogen (N) limitation. Host-specific soil microbiome conditioning and inorganic N fertilization combined to qualitatively affect coexistence outcomes. Lower N conditions favoured Populus over Acer trees, and N fertilization reversed this outcome for southern species, aligning with regional-scale forest mycorrhizal transitions. Results from the coexistence experiment also predict competitive exclusion between the tree species pairs, which could arise, in part, from their mycorrhizal differences and is consistent with alternative stable states in dominant forest mycorrhizal strategies. Such bistability appears in natural systems as a bimodal distribution of Populus vs. Acer tree species dominance using long-term forest inventory data. Synthesis: The magnitude and outcome of microbially mediated competition between Populus and Acer depends on soil nutrient availability, which likely relates to their mycorrhizal differentiation. These findings support the importance of mycorrhizal symbioses for contributing to large-scale biogeographical patterns of tree species trophic niche separation across soil resource gradients and bistability in forest mycorrhizal structure.

54 ENVIRONMENTAL SCIENCES↗

Does resource exchange in ectomycorrhizal symbiosis vary with competitive context and nitrogen addition?

Ectomycorrhizal symbiosis is essential for the nutrition of most temperate forest trees and helps regulate the movement of carbon and nitrogen through forested ecosystems. The factors governing the exchange of plant carbon for fungal nitrogen, however, remain obscure. Because competition and soil resources may influence ectomycorrhizal resource movement, we performed a ten month split-root microcosm study using Pinus muricata seedlings with Thelephora terrestris, Suillus pungens, or no ectomycorrhizal fungus, under two nitrogen levels in artificial soil. Fungi competed directly with roots, and indirectly with each other. We used stable isotope enrichment to track plant photosynthate and fungal nitrogen. For Thelephora, plants received N commensurate with the C given to their fungal partners. Thelephora was a superior mutualist under high nitrogen. For Suillus, plant C and fungal N exchange were not coupled. However, in low nitrogen, plants preferentially allocated C to Suillus rather than Thelephora. Our results suggest that ectomycorrhizal resource transfer depends on competitive and nutritional context. Plants can exchange C for fungal N, but coupling of these resources can depend on the fungal species and soil N. Here, understanding the diversity of fungal strategies, and how they change with environmental context, reveals mechanisms driving this important symbiosis.

stable isotope enrichment↗

Mycorrhizal Distributions Impact Global Patterns of Carbon and Nutrient Cycling

Most tree species predominantly associate with a single type of mycorrhizal fungi, which can differentially affect plant nutrient acquisition and biogeochemical cycling. Uncertainties in mycorrhizal distributions are non-trivial, and current estimates disagree in up to 50% over 40% of the land area, including tropical forests. Remote sensing capabilities for mycorrhizal detection show promise for refining these estimates further. Here, we address for the first time the impact of mycorrhizal distributions on global carbon and nutrient cycling. Using the state-of-the-art carbon-nitrogen economics within the Community Land Model version 5, we found Net Primary Productivity (NPP) increased throughout the 21st century by 20%; however, as soil nitrogen has progressively become limiting, the costs to NPP for nitrogen acquisition—that is, to mycorrhizae—have increased at a faster rate by 60%. This suggests that nutrient acquisition will increasingly demand a higher portion of assimilated carbon to support the same productivity.

54 ENVIRONMENTAL SCIENCES↗

Decadal changes in fire frequencies shift tree communities and functional traits

Global change has resulted in chronic shifts in fire regimes. Variability in the sensitivity of tree communities to multi-decadal changes in fire regimes is critical to anticipating shifts in ecosystem structure and function, yet remains poorly understood. Here, we address the overall effects of fire on tree communities and the factors controlling their sensitivity in 29 sites that experienced multi-decadal alterations in fire frequencies in savanna and forest ecosystems across tropical and temperate regions. Fire had a strong overall effect on tree communities, with an average fire frequency (one fire every three years) reducing stem density by 48% and basal area by 53% after 50 years, relative to unburned plots. Here, the largest changes occurred in savanna ecosystems and in sites with strong wet seasons or strong dry seasons, pointing to fire characteristics and species composition as important. Analyses of functional traits highlighted the impact of fire-driven changes in soil nutrients because frequent burning favoured trees with low biomass nitrogen and phosphorus content, and with more efficient nitrogen acquisition through ectomycorrhizal symbioses. Taken together, the response of trees to altered fire frequencies depends both on climatic and vegetation determinants of fire behaviour and tree growth, and the coupling between fire-driven nutrient losses and plant traits.

54 ENVIRONMENTAL SCIENCES↗

Symbiotic niche mapping reveals functional specialization by two ectomycorrhizal fungi that expands the host plant niche

Mutualisms are ubiquitous in natural systems, but less is known about how these positive interactions influence species distributions compared with antagonistic interactions, such as competition and predation. The niche concept is one useful approach for thinking about factors that shape species ranges, which we apply here towards understanding how the nature of plant-mycorrhizal symbioses change across large environmental gradients. We used a continuous niche mapping approach to examine how two ectomycorrhizal fungi (Thelephora terrestris, Suillus pungens) impact pine seedling growth across a two-dimensional soil nitrogen (N) and phosphorus (P) gradient. We found that ectomycorrhizal fungi improved plant growth most in nutrient addition treatments with highly imbalanced N:P ratios, demonstrating that mycorrhizal benefits depend on interactions between niche axes. Nevertheless, T. terrestris (highN:lowP) and S. pungens (lowN:highP) benefited plants most at opposite ends of the resource ratio spectrum, consistent with niche partitioning and functional specialization. While ectomycorrhizal fungi are often thought of as being most beneficial for nitrogen uptake, our results suggest that members of the Thelephoraceae may specialize in improving plant P uptake. Ectomycorrhizal colonization by a single fungus increased plant niche volume (calculated as convex hull volumes of plant growth response surfaces across N and P gradients) compared to non-mycorrhizal control plants and shows the overall positive effects of mutualisms on plant niche volume. Despite plant host benefits in S. pungens and T. terrestris single species treatments, the presence of both fungi together decreased plant niche volume. The lack of functional complementarity, despite functional specialization, indicates that in some environments, either fungal competition or the cost of maintaining a suboptimal mycorrhizal partner can limit the benefits of a higher quality partner. The niche mapping approach we present has the potential to answer fundamental questions about the dimensions of functional diversity in ectomycorrhizal fungi and the distributions of mycorrhizal symbioses.

59 BASIC BIOLOGICAL SCIENCES↗

Warming and disturbance alter soil microbiome diversity and function in a northern forest ecotone

ABSTRACT The response to global change by soil microbes is set to affect important ecosystem processes. These impacts could be most immediate in transitional zones, such as the temperate-boreal forest ecotone, yet previous work in these forests has primarily focused on specific subsets of microbial taxa. Here, we examined how bacterial and fungal communities respond to simulated above- and below-ground warming under realistic field conditions in closed and open canopy treatments in Minnesota, USA. Our results show that warming and canopy disturbance shifted bacterial and fungal community structure as dominant bacterial and fungal groups differed in the direction and intensity of their responses. Ectomycorrhizal and saprotrophic fungal communities with greater connectivity (higher prevalence of strongly interconnected taxa based on pairwise co-occurrence relationships) were more resistant to compositional change. Warming effects on soil enzymes involved in the hydrolytic and oxidative liberation of carbon from plant cell walls and nutrients from organic matter were most strongly linked to fungal community responses, although community structure–function relationships differed between fungal guilds. Collectively, these findings indicate that warming and disturbance will influence the composition and function of microbial communities in the temperate-boreal ecotone, and fungal responses are particularly important to understand for predicting future ecosystem functioning.

Microbiology↗