Climate mismatches with ectomycorrhizal fungi contribute to migration lag in North American tree range shifts.

Climate change will likely shift plant and microbial distributions, creating geographic mismatches between plant hosts and essential microbial symbionts (e.g., ectomycorrhizal fungi, EMF). The loss of historical interactions, or the gain of novel associations, can have important consequences for biodiversity, ecosystem processes, and plant migration potential, yet few analyses exist that measure where mycorrhizal symbioses could be lost or gained across landscapes. Here, we examine climate change impacts on tree-EMF codistributions at the continent scale. We built species distribution models for 400 EMF species and 50 tree species, integrating fungal sequencing data from North American forest ecosystems with tree species occurrence records and long-term forest inventory data. Our results show the following: 1) tree and EMF climate suitability to shift toward higher latitudes; 2) climate shifts increase the size of shared tree-EMF habitat overall, but 35% of tree-EMF pairs are at risk of declining habitat overlap; 3) climate mismatches between trees and EMF are projected to be greater at northern vs. southern boundaries; and 4) tree migration lag is correlated with lower richness of climatically suitable EMF partners. This work represents a concentrated effort to quantify the spatial extent and location of tree-EMF climate envelope mismatches. Our findings also support a biotic mechanism partially explaining the failure of northward tree species migrations with climate change: reduced diversity of co-occurring and climate-compatible EMF symbionts at higher latitudes. We highlight the conservation implications for identifying areas where tree and EMF responses to climate change may be highly divergent.

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 (C) and nitrogen (N) through forested ecosystems. The factors governing the exchange of plant C for fungal N, however, remain obscure. Because competition and soil resources may influence ectomycorrhizal resource movement, we performed a 10-month split-root microcosm study using Pinus muricata seedlings with Thelephora terrestris, Suillus pungens, or no ectomycorrhizal fungus, under two N concentrations in artificial soil. Fungi competed directly with roots and indirectly with each other. We used stable isotope enrichment to track plant photosynthate and fungal N. For T. terrestris, plants received N commensurate with the C given to their fungal partners. Thelephora terrestris was a superior mutualist under high-N conditions. For S. pungens, plant C and fungal N exchange were not coupled. However, in low-N conditions, plants preferentially allocated C to S. pungens rather than T. terrestris. 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. Understanding the diversity of fungal strategies, and how they change with environmental context, reveals mechanisms driving this important symbiosis.

Multiple distinct, scale-dependent links between fungi and decomposition.

Decomposition has historically been considered a function of climate and substrate but new research highlights the significant role of specific micro-organisms and their interactions. In particular, wood decay is better predicted by variation in fungal communities than in climate. Multiple links exist: interspecific competition slows decomposition in more diverse fungal communities, whereas trait variation between different communities also affects process rates. Here, we paired field and laboratory experiments using a dispersal gradient at a forest-shrubland ecotone to examine how fungi affect wood decomposition across scales. We observed that while fungal communities closer to forests were capable of faster decomposition, wood containing diverse fungal communities decomposed more slowly, independent of location. Dispersal-driven stochasticity in small-scale community assembly was nested within large-scale turnover in the regional species pool, decoupling the two patterns. We thus find multiple distinct links between microbes and ecosystem function that manifest across different spatial scales.

Optimal Allocation Ratios: A Square Root Relationship between the Ratios of Symbiotic Costs and Benefits.

AbstractAll organisms struggle to make sense of environmental stimuli in order to maximize their fitness. For animals, the responses of single cells and superorganisms to stimuli are generally proportional to stimulus ratios, a phenomenon described by Weber's law. However, Weber's law has not yet been used to predict how plants respond to stimuli generated from their symbiotic partners. Here we develop a model for quantitatively predicting the ratios of carbon (C) allocation to symbionts that provide nutrients to their plant host. Consistent with Weber's law, our model demonstrates that the optimal ratio of resources allocated to a less beneficial relative to a more beneficial symbiont scale to the ratio of the growth benefits of the two strains. As C allocation to symbionts increases, the ratio of C allocation to two strains approaches the square root of the ratio of symbiotic growth benefits (e.g., a worse symbiont providing one-fourth the benefits gets 1/4=1/2 the C of a better symbiont). We document a compelling correspondence between our square root model prediction and a meta-analysis of experimental literature on C allocation. This type of preferential allocation can promote coexistence between more beneficial and less beneficial symbionts, offering a potential mechanism behind the high diversity of microbial symbionts observed in nature.

Contrasting fungal responses to wildfire across different ecosystem types.

Wildfire affects our planet's biogeochemistry both by burning biomass and by driving changes in ecological communities and landcover. Some plants and ecosystem types are threatened by increasing fire pressure while others respond positively to fire, growing in local and regional abundance when it occurs regularly. However, quantifying total ecosystem response to fire demands consideration of impacts not only on aboveground vegetation, but also on soil microbes like fungi, which influence decomposition and nutrient mineralization. If fire-resistant soil fungal communities co-occur with similarly adapted plants, these above- and belowground ecosystem components should shift and recover in relative synchrony after burning. If not, fire might decouple ecosystem processes governed by these different communities, affecting total functioning. Here, we use a natural experiment to test whether fire-dependent ecosystems host unique, fire-resistant fungal communities. We surveyed burned and unburned areas across two California ecosystem types with differing fire ecologies in the immediate aftermath of a wildfire, finding that the soil fungal communities of fire-dependent oak woodlands differ from those of neighbouring mixed evergreen forests. We discovered furthermore that the latter are more strongly altered compositionally by fire than the former, suggesting that differences in fungal community structure support divergent community responses to fire across ecosystems. Our results thus indicate that fire-dependent ecosystems may host fire-resistant fungal communities.

Lithological constraints on resource economies shape the mycorrhizal composition of a Bornean rain forest.

Arbuscular mycorrhizal fungi (AMF) and ectomycorrhizal fungi (EMF) produce contrasting plant-soil feedbacks, but how these feedbacks are constrained by lithology is poorly understood. We investigated the hypothesis that lithological drivers of soil fertility filter plant resource economic strategies in ways that influence the relative fitness of trees with AMF or EMF symbioses in a Bornean rain forest containing species with both mycorrhizal strategies. Using forest inventory data on 1245 tree species, we found that although AMF-hosting trees had greater relative dominance on all soil types, with declining lithological soil fertility EMF-hosting trees became more dominant. Data on 13 leaf traits and wood density for a total of 150 species showed that variation was almost always associated with soil type, whereas for six leaf traits (structural properties; carbon, nitrogen, phosphorus ratios, nitrogen isotopes), variation was also associated with mycorrhizal strategy. EMF-hosting species had slower leaf economics than AMF-hosts, demonstrating the central role of mycorrhizal symbiosis in plant resource economies. At the global scale, climate has been shown to shape forest mycorrhizal composition, but here we show that in communities it depends on soil lithology, suggesting scale-dependent abiotic factors influence feedbacks underlying the relative fitness of different mycorrhizal strategies.

Effect of Simulated Climate Warming on the Ectomycorrhizal Fungal Community of Boreal and Temperate Host Species Growing Near Their Shared Ecotonal Range Limits.

Ectomycorrhizal (ECM) fungi can influence the establishment and performance of host species by increasing nutrient and water absorption. Therefore, understanding the response of ECM fungi to expected changes in the global climate is crucial for predicting potential changes in the composition and productivity of forests. While anthropogenic activity has, and will continue to, cause global temperature increases, few studies have investigated how increases in temperature will affect the community composition of ectomycorrhizal fungi. The effects of global warming are expected to be particularly strong at biome boundaries and in the northern latitudes. In the present study, we analyzed the effects of experimental manipulations of temperature and canopy structure (open vs. closed) on ectomycorrhizal fungi identified from roots of host seedlings through 454 pyrosequencing. The ecotonal boundary site selected for the study was between the southern boreal and temperate forests in northern Minnesota, USA, which is the southern limit range for Picea glauca and Betula papyrifera and the northern one for Pinus strobus and Quercus rubra. Manipulations that increased air and soil temperature by 1.7 and 3.4 °C above ambient temperatures, respectively, did not change ECM richness but did alter the composition of the ECM community in a manner dependent on host and canopy structure. The prediction that colonization of boreal tree species with ECM symbionts characteristic of temperate species would occur was not substantiated. Overall, only a small proportion of the ECM community appears to be strongly sensitive to warming.

Geographical Variation in Community Divergence: Insights from Tropical Forest Monodominance by Ectomycorrhizal Trees.

Convergence occurs in both species traits and community structure, but how convergence at the two scales influences each other remains unclear. To address this question, we focus on tropical forest monodominance, in which a single, often ectomycorrhizal (EM) tree species occasionally dominates forest stands within a landscape otherwise characterized by diverse communities of arbuscular mycorrhizal (AM) trees. Such monodominance is a striking potential example of community divergence resulting in alternative stable states. However, it is observed only in some tropical regions. A diverse suite of AM and EM trees locally codominate forest stands elsewhere. We develop a hypothesis to explain this geographical difference using a simulation model of plant community assembly. Simulation results suggest that in a region with a few EM species (e.g., South America), EM trees experience strong selection for convergent traits that match the abiotic conditions of the environment. Consequently, EM species successfully compete against other species to form monodominant stands via positive plant-soil feedbacks. By contrast, in a region with many EM species (e.g., Southeast Asia), species maintain divergent traits because of complex plant-soil feedbacks, with no species having traits that enable monodominance. An analysis of plant trait data from Borneo and Peruvian Amazon was inconclusive. Overall, this work highlights the utility of geographical comparison in understanding the relationship between trait convergence and community convergence.

Continental-level population differentiation and environmental adaptation in the mushroom Suillus brevipes.

Recent advancements in sequencing technology allowed researchers to better address the patterns and mechanisms involved in microbial environmental adaptation at large spatial scales. Here we investigated the genomic basis of adaptation to climate at the continental scale in Suillus brevipes, an ectomycorrhizal fungus symbiotically associated with the roots of pine trees. We used genomic data from 55 individuals in seven locations across North America to perform genome scans to detect signatures of positive selection and assess whether temperature and precipitation were associated with genetic differentiation. We found that S. brevipes exhibited overall strong population differentiation, with potential admixture in Canadian populations. This species also displayed genomic signatures of positive selection as well as genomic sites significantly associated with distinct climatic regimes and abiotic environmental parameters. These genomic regions included genes involved in transmembrane transport of substances and helicase activity potentially involved in cold stress response. Our study sheds light on large-scale environmental adaptation in fungi by identifying putative adaptive genes and providing a framework to further investigate the genetic basis of fungal adaptation.

Controls of nitrogen cycling evaluated along a well-characterized climate gradient.

The supply of nitrogen (N) constrains primary productivity in many ecosystems, raising the question "what controls the availability and cycling of N"? As a step toward answering this question, we evaluated N cycling processes and aspects of their regulation on a climate gradient on Kohala Volcano, Hawaii, USA. The gradient extends from sites receiving <300 mm/yr of rain to those receiving >3,000 mm/yr, and the pedology and dynamics of rock-derived nutrients in soils on the gradient are well understood. In particular, there is a soil process domain at intermediate rainfall within which ongoing weathering and biological uplift have enriched total and available pools of rock-derived nutrients substantially; sites at higher rainfall than this domain are acid and infertile as a consequence of depletion of rock-derived nutrients, while sites at lower rainfall are unproductive and subject to wind erosion. We found elevated rates of potential net N mineralization in the domain where rock-derived nutrients are enriched. Higher-rainfall sites have low rates of potential net N mineralization and high rates of microbial N immobilization, despite relatively high rates of gross N mineralization. Lower-rainfall sites have moderately low potential net N mineralization, relatively low rates of gross N mineralization, and rates of microbial N immobilization sufficient to sequester almost all the mineral N produced. Bulk soil δ15 N also varied along the gradient, from +4‰ at high rainfall sites to +14‰ at low rainfall sites, indicating differences in the sources and dynamics of soil N. Our analysis shows that there is a strong association between N cycling and soil process domains that are defined using soil characteristics independent of N along this gradient, and that short-term controls of N cycling can be understood in terms of the supply of and demand for N.

Endemism and functional convergence across the North American soil mycobiome.

Identifying the ecological processes that structure communities and the consequences for ecosystem function is a central goal of ecology. The recognition that fungi, bacteria, and viruses control key ecosystem functions has made microbial communities a major focus of this field. Because many ecological processes are apparent only at particular spatial or temporal scales, a complete understanding of the linkages between microbial community, environment, and function requires analysis across a wide range of scales. Here, we map the biological and functional geography of soil fungi from local to continental scales and show that the principal ecological processes controlling community structure and function operate at different scales. Similar to plants or animals, most soil fungi are endemic to particular bioregions, suggesting that factors operating at large spatial scales, like dispersal limitation or climate, are the first-order determinants of fungal community structure in nature. By contrast, soil extracellular enzyme activity is highly convergent across bioregions and widely differing fungal communities. Instead, soil enzyme activity is correlated with local soil environment and distribution of fungal traits within the community. The lack of structure-function relationships for soil fungal communities at continental scales indicates a high degree of functional redundancy among fungal communities in global biogeochemical cycles.

Survey of corticioid fungi in North American pinaceous forests reveals hyperdiversity, underpopulated sequence databases, and species that are potentially ectomycorrhizal.

The corticioid fungi are commonly encountered, highly diverse, ecologically important, and understudied. We collected specimens in 60 pine and spruce forests across North America to survey corticioid fungal frequency and distribution and to compile an internal transcribed spacer (ITS) database for the group. Sanger sequences from the ITS region of vouchered specimens were compared with sequences on GenBank and UNITE, and with high-throughput sequence data from soil and roots taken at the same sites. Out of 425 high-quality Sanger sequences from vouchered specimens, we recovered 223 distinct operational taxonomic units (OTUs), the majority of which could not be assigned to species by matching to the BLAST database. Corticioid fungi were found to be hyperdiverse, as supported by the observations that nearly two-thirds of our OTUs were represented by single collections and species estimator curves showed steep slopes with no plateaus. We estimate that 14.8-24.7% of our voucher-based OTUs are likely to be ectomycorrhizal (EM). Corticioid fungi recovered from the soil formed a different community assemblage, with EM taxa accounting for 40.5-58.6% of OTUs. We compared basidioma sequences with EM root tips from our data, GenBank, or UNITE, and with this approach, we reiterate existing speculations that Trechispora stellulata is EM. We found that corticioid fungi have a significant distance-decay pattern, adding to the literature supporting fungi as having geographically structured communities. This study provides a first view of the diversity of this important group across North American pine forests, but much of the biology and taxonomy of these diverse, important, and widespread fungi remains unknown.

Common foliar fungi of Populus trichocarpa modify Melampsora rust disease severity.

Nonpathogenic foliar fungi (i.e. endophytes and epiphytes) can modify plant disease severity in controlled experiments. However, experiments have not been combined with ecological studies in wild plant pathosystems to determine whether disease-modifying fungi are common enough to be ecologically important. We used culture-based methods and DNA sequencing to characterize the abundance and distribution of foliar fungi of Populus trichocarpa in wild populations across its native range (Pacific Northwest, USA). We conducted complementary, manipulative experiments to test how foliar fungi commonly isolated from those populations influence the severity of Melampsora leaf rust disease. Finally, we examined correlative relationships between the abundance of disease-modifying foliar fungi and disease severity in wild trees. A taxonomically and geographically diverse group of common foliar fungi significantly modified disease severity in experiments, either increasing or decreasing disease severity. Spatial patterns in the abundance of some of these foliar fungi were significantly correlated (in predicted directions) with disease severity in wild trees. Our study reveals that disease modification is an ecological function shared by common foliar fungal symbionts of P. trichocarpa. This finding raises new questions about plant disease ecology and plant biodiversity, and has applied potential for disease management.

Lack of host specificity leads to independent assortment of dipterocarps and ectomycorrhizal fungi across a soil fertility gradient.

Plants interact with a diversity of microorganisms, and there is often concordance in their community structures. Because most community-level studies are observational, it is unclear if such concordance arises because of host specificity, in which microorganisms or plants limit each other's occurrence. Using a reciprocal transplant experiment, we tested the hypothesis that host specificity between trees and ectomycorrhizal fungi determines patterns of tree and fungal soil specialisation. Seedlings of 13 dipterocarp species with contrasting soil specialisations were seeded into plots crossing soil type and canopy openness. Ectomycorrhizal colonists were identified by DNA sequencing. After 2.5 years, we found no evidence of host specificity. Rather, soil environment was the primary determinant of ectomycorrhizal diversity and composition on seedlings. Despite their close symbiosis, our results show that ectomycorrhizal fungi and tree communities in this Bornean rain forest assemble independently of host-specific interactions, raising questions about how mutualism shapes the realised niche.

Local-scale biogeography and spatiotemporal variability in communities of mycorrhizal fungi.

Knowledge of spatiotemporal patterns in species distribution is fundamental to understanding the ecological and evolutionary processes shaping communities. The emergence of DNA-based tools has expanded the geographic and taxonomic scope of studies examining spatial and temporal distribution of mycorrhizal fungi. However, the nature of spatiotemporal patterns documented and subsequent interpretation of ecological processes can vary significantly from study to study. In order to look for general patterns we synthesize the available data across different sampling scales and mycorrhizal types. The results of this analysis shed light on the relative importance of space, time and vertical soil structure on community variability across different mycorrhizal types. Although we found no significant trend in spatiotemporal variation amongmycorrhizal types, the vertical community variation was distinctly greater than the spatial and temporal variability in mycorrhizal fungal communities. Both spatial and temporal variability of communities was greater in topsoil compared with lower horizons, suggesting that greater environmental heterogeneity drives community variation on a fine scale. This further emphasizes the importance of both niche differentiation and environmental filtering in maintaining diverse fungal communities.

A continental view of pine-associated ectomycorrhizal fungal spore banks: a quiescent functional guild with a strong biogeographic pattern.

Ecologists have long acknowledged the importance of seed banks; yet, despite the fact that many plants rely on mycorrhizal fungi for survival and growth, the structure of ectomycorrhizal (ECM) fungal spore banks remains poorly understood. The primary goal of this study was to assess the geographic structure in pine-associated ECM fungal spore banks across the North American continent. Soils were collected from 19 plots in forests across North America. Fresh soils were pyrosequenced for fungal internal transcribed spacer (ITS) amplicons. Adjacent soil cores were dried and bioassayed with pine seedlings, and colonized roots were pyrosequenced to detect resistant propagules of ECM fungi. The results showed that ECM spore banks correlated strongly with biogeographic location, but not with the identity of congeneric plant hosts. Minimal community overlap was found between resident ECM fungi vs those in spore banks, and spore bank assemblages were relatively simple and dominated by Rhizopogon, Wilcoxina, Cenococcum, Thelephora, Tuber, Laccaria and Suillus. Similar to plant seed banks, ECM fungal spore banks are, in general, depauperate, and represent a small and rare subset of the mature forest soil fungal community. Yet, they may be extremely important in fungal colonization after large-scale disturbances such as clear cuts and forest fires.

Genetic isolation between two recently diverged populations of a symbiotic fungus.

Fungi are an omnipresent and highly diverse group of organisms, making up a significant part of eukaryotic diversity. Little is currently known about the drivers of fungal population differentiation and subsequent divergence of species, particularly in symbiotic, mycorrhizal fungi. Here, we investigate the population structure and environmental adaptation in Suillus brevipes (Peck) Kuntze, a wind-dispersed soil fungus that is symbiotic with pine trees. We assembled and annotated the reference genome for Su. brevipes and resequenced the whole genomes of 28 individuals from coastal and montane sites in California. We detected two clearly delineated coast and mountain populations with very low divergence. Genomic divergence was restricted to few regions, including a region of extreme divergence containing a gene encoding for a membrane Na(+) /H(+) exchanger known for enhancing salt tolerance in plants and yeast. Our results are consistent with a very recent split between the montane and coastal Su. brevipes populations, with few small genomic regions under positive selection and a pattern of dispersal and/or establishment limitation. Furthermore, we identify a putatively adaptive gene that motivates further functional analyses to link genotypes and phenotypes and shed light on the genetic basis of adaptive traits.