Search

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.

Fungi represent a large proportion of the genetic diversity on Earth and fungal activity influences the structure of plant and animal communities, as well as rates of ecosystem processes. Large-scale DNA-sequencing datasets are beginning to reveal the dimensions of fungal biodiversity, which seem to be fundamentally different to bacteria, plants and animals. In this Review, we describe the patterns of fungal biodiversity that have been revealed by molecular-based studies. Furthermore, we consider the evidence that supports the roles of different candidate drivers of fungal diversity at a range of spatial scales, as well as the role of dispersal limitation in maintaining regional endemism and influencing local community assembly. Finally, we discuss the ecological mechanisms that are likely to be responsible for the high heterogeneity that is observed in fungal communities at local scales.

The carbon use efficiency (CUE) of microbial communities partitions the flow of C from primary producers to the atmosphere, decomposer food webs, and soil C stores. CUE, usually defined as the ratio of growth to assimilation, is a critical parameter in ecosystem models, but is seldom measured directly in soils because of the methodological difficulty of measuring in situ rates of microbial growth and respiration. Alternatively, CUE can be estimated indirectly from the elemental stoichiometry of organic matter and microbial biomass, and the ratios of C to nutrient-acquiring ecoenzymatic activities. We used this approach to estimate and compare microbial CUE in >2000 soils from a broad range of ecosystems. Mean CUE based on C:N stoichiometry was 0.269 ± 0.110 (mean ± SD). A parallel calculation based on C:P stoichiometry yielded a mean CUE estimate of 0.252 ± 0.125. The mean values and frequency distributions were similar to those from aquatic ecosystems, also calculated from stoichiometric models, and to those calculated from direct measurements of bacterial and fungal growth and respiration. CUE was directly related to microbial biomass C with a scaling exponent of 0.304 (95% CI 0.237–0.371) and inversely related to microbial biomass P with a scaling exponent of −0.234 (95% CI −0.289 to −0.179). Relative to CUE, biomass specific turnover time increased with a scaling exponent of 0.509 (95% CI 0.467–0.551). CUE increased weakly with mean annual temperature. CUE declined with increasing soil pH reaching a minimum at pH 7.0, then increased again as soil pH approached 9.0, a pattern consistent with pH trends in the ratio of fungal : bacteria abundance and growth. Structural equation models that related geographic variables to CUE component variables showed the strongest connections for paths linking latitude and pH to β-glucosidase activity and soil C:N:P ratios. The integration of stoichiometric and metabolic models provides a quantitative description of the functional organization of soil microbial communities that can improve the representation of CUE in microbial process and ecosystem simulation models.

The ectomycorrhizal (ECM) fungal communities associated with the host genus Alnus have been widely noted for their low richness and high proportion of host-specific species, but the processes underlying their atypical structure remain poorly understood. In this study, we investigated whether the high acidity and nitrate concentrations characteristic of Alnus soils may act as important environmental filters that limit the membership in Alnus ECM fungal communities. Using a pure culture approach, we grew four species from two host groups ( Alnus and non- Alnus ) in liquid media containing different acidity and nitrate concentrations. We found that the growth of the Alnus -associated ECM fungi was not, on average, affected by high acidity, while the non- Alnus -associated ECM fungi had a significantly negative growth response under the same conditions. Similarly, when grown at high nitrate, the non- Alnus -associated ECM fungi also generally performed more poorly. Growth responses of the Alnus -associated ECM fungi in both the high acidity and high nitrate treatments indicated tolerance rather than preference for those chemical conditions. The mechanism underlying the differential acidity tolerance may involve active hyphal buffering of local acidity environments. Taken together, our results suggest that soil chemical conditions likely do act as significant environmental filters that, along with other ecological and evolutionary factors, drive the atypical specificity of Alnus ECM interactions.

Summary Ectomycorrhizal (EM) fungi form symbiotic associations with plant roots that regulate nutrient exchange between forest plants and soil. Environmental metagenomics approaches that employ next-generation sequencing show great promise for studying EM symbioses; however, metatranscriptomic studies have been constrained by the inherent difficulties associated with isolation and sequencing of RNA from mycorrhizae. Here we apply an optimized method for combined DNA/RNA extraction using field-collected EM fungal–pine root clusters, together with protocols for taxonomic identification of expressed ribosomal RNA, and inference of EM function based on plant and fungal metatranscriptomics. We used transcribed portions of ribosomal RNA genes to identify several transcriptionally dominant fungal taxa associated with loblolly pine including Amphinema, Russula and Piloderma spp. One taxon, Piloderma croceum, has a publically available genome that allowed us to identify patterns of gene content and transcript abundance. Over 1500 abundantly expressed Piloderma genes were detected from mycorrhizal roots, including genes for protein metabolism, cell signalling, electron transport, terpene synthesis and other extracellular activities. In contrast, Piloderma gene encoding an ammonia transporter showed highest transcript abundance in soil samples. Our methodology highlights the potential of metatranscriptomics to identify genes associated with symbiosis and ecosystem function using field-collected samples.

The relative roles of ectomycorrhizal (ECM) and saprotrophic communities in controlling the decomposition of soil organic matter remain unclear. We tested the hypothesis that ECM community structure and activity influences the breakdown of nutrient-rich biopolymers in soils, while saprotrophic communities primarily regulate the breakdown of carbon-rich biopolymers. To test this hypothesis, we used high-throughput techniques to measure ECM and saprotrophic community structure, soil resource availability, and extracellular enzyme activity in whole soils and on ECM root tips in a coastal pine forest. We found that ECM and saprotroph richness did not show spatial structure and did not co-vary with any soil resource. However, species richness of ECM fungi explained variation in the activity of enzymes targeting recalcitrant N sources (protease and peroxidase) in bulk soil. Activity of carbohydrate- and organic P- targeting enzymes (e.g. cellobiohydrolase, β-glucosidase, α-glucosidase, hemicellulases, N-acetyl-glucosaminidase, and acid phosphatase) was correlated with saprotroph community structure and soil resource abundance (total soil C, N, and moisture), both of which varied along the soil profile. These observations suggest independent roles of ECM fungi and saprotrophic fungi in the cycling of N-rich, C-rich, and P-rich molecules through soil organic matter. Enzymatic activity on ECM root tips taken from the same soil cores used for bulk enzyme analysis did not correlate with the activity of any enzyme measured in the bulk soil, suggesting that ECM contributions to larger-scale soil C and nutrient cycling may occur primarily via extramatrical hyphae outside the rhizosphere.

Accurate prediction of future atmospheric CO2 concentrations is essential for evaluating climate change impacts on ecosystems and human societies. One major source of uncertainty in model predictions is the extent to which global warming will increase atmospheric CO2 concentrations through enhanced microbial decomposition of soil organic carbon. Recent advances in microbial ecology could help reduce this uncertainty, but current global models do not represent direct microbial control over decomposition. Instead, all of the coupled climate models reviewed in the most recent Intergovernmental Panel on Climate Change (IPCC) report assume that decomposition is a first-order decay process, proportional to the size of the soil carbon pool. Here we argue for the development of a new generation of models that link decomposition directly to the size and activity of microbial communities in coupled global models. This process begins with the formulation and validation of fine-scale models that capture fundamental microbial mechanisms without excessive mathematical complexity. These mechanistic models must then be scaled up through an aggregation process and validated at ecosystem to global scales prior to incorporation into global climate models (GCMs). Parameterizing microbial models at the global scale is challenging because some microbial properties such as in situ extracellular enzyme activities are very difficult to measure directly. New parameter fitting procedures may therefore be needed to infer the values of important microbial variables. Validating decomposition models at the global scale is also a challenge, and has not yet been accomplished with the land carbon models embedded in current GCMs. Fortunately new global datasets on soil carbon stocks and fluxes offer promising opportunities to validate both existing land carbon models and new microbial models. If challenges in scaling, parameterization, and validation can be overcome, a new generation of microbially-based decomposition models could substantially improve predictions of carbon–climate feedbacks in the Earth system. Development of new models structures would also reduce any bias due to the assumption of first-order decomposition across all of the models currently referenced in reports of the IPCC.

Mycorrhizal plants from a variety of ecosystems have the capacity to take up organic forms of nitrogen, yet the fraction of plant nitrogen demand met by organic N (ON) uptake remains unclear. ON uptake by mycorrhizal plants is a biochemical process that involves multiple steps, including breakdown and uptake of soil ON by mycorrhizal fungi, internal transformation of ON, and transfer of N to the host plant. We present hypothetical mechanisms controlling each of these steps and outline predictions for how these mechanisms structure patterns of ON uptake by mycorrhizal plants in ecosystems. Using a synthesis of published data, we found that uptake of amino acids by mycorrhizal fungi is related to the relative abundance, N content, and carbon structure of the amino acid. We hypothesize that the bond strength and structural diversity of soil ON controls the breakdown of polymeric ON by mycorrhizal fungi. In addition, the availability of carbon resources for the mycorrhizal fungus influences the capacity for mycorrhizal fungi to assimilate amino acids and produce extracellular enzymes that catalyze the breakdown of polymeric ON.

Author(s): Talbot, JM; Allison, SD; Treseder, KK | Abstract: 1. In the conventional view of soil carbon (C) cycling, mycorrhizal fungi are primarily considered vectors for plant C input to soils. However, there is accumulating evidence that mycorrhizal fungi may also contribute to the direct loss of soil C by acting as decomposers, that is by producing extracellular lytic enzymes and metabolizing soil C. 2. Most of the evidence that mycorrhizal fungi can act as decomposers comes from studies of ericoid and ectomycorrhizal fungi, although there is increasing experimental evidence for a role of arbuscular mycorrhizal fungi in soil C decomposition. Decomposition by mycorrhizal fungi implies that soil C balance is subjected to the ecological factors that affect both plant and fungal symbionts; this interaction has important consequences for how soil C stocks respond to global change. 3. In this synthesis, we propose a new model of soil C cycling, including decomposition of soil C by mycorrhizal fungi, and we evaluate how this new integrative model alters our predictions of soil C feedbacks to global change. We present three hypothetical mechanisms by which mycorrhizal fungi may metabolize significant quantities of soil C. The first hypothesis ('Plan B' hypothesis) is that mycorrhizal fungi metabolize soil C as an alternate C source when supplies of photosynthate from the host plant are low. Our second hypothesis ('Coincidental Decomposer' hypothesis) is that mycorrhizal fungi decompose soil C as a consequence of mining soil for organic nutrients. The third hypothesis ('Priming Effects' hypothesis) is that mycorrhizal fungi decompose soil C when allocation of plant photosynthate to mycorrhizal roots is high, such that plant C 'primes' the growth and activity of mycorrhizal fungi. 4. Further empirical tests of these hypotheses will clarify the role of mycorrhizal fungi in soil C balance and improve our understanding of soil C responses to global change. © 2008 The Authors.

Tannins are abundant secondary chemicals in leaf litter that are hypothesized to slow the rate of soil-N cycling by binding protein into recalcitrant polyphenol-protein complexes (PPCs). We studied the effects of tannins purified from sugar maple, red oak, and eastern hemlock leaf litter on microbial activity and N cycling in soils from northern hardwood-conifer forests of the northeastern US. To create ecologically relevant conditions, we applied tannins to soil at a concentration (up to 2 mg g(-1) soil) typical of mineral soil horizons. Sugar maple tannins increased microbial respiration significantly more than red oak or hemlock tannins. The addition of sugar maple tannins also decreased gross N mineralization by 130% and, depending upon the rate of application, decreased net rates of N mineralization by 50-290%. At low concentrations, the decrease in mineralization appeared to be driven by greater microbial-N immobilization, while at higher concentrations the decrease in mineralization was consistent with the formation of recalcitrant PPCs. Low concentrations of red oak and hemlock tannins stimulated microbial respiration only slightly, and did not significantly affect fluxes of inorganic N in the soil. When applied to soils containing elevated levels of protein, red oak and hemlock tannins decreased N mineralization without affecting rates of microbial respiration, suggesting that PPC formation decreased substrate availability for microbial immobilization. Our results indicate that tannins from all three species form recalcitrant PPCs, but that the degree of PPC formation and its attendant effect on soil-N cycling depends on tannin concentration and the pool size of available protein in the soil.

Linking community composition to ecosystem function is a challenge in complex microbial communities. We tested the hypothesis that key biological features of fungi - evolutionary history, functional guild, and abundance of functional genes – can predict the biogeochemical activity of fungal species during decay. We measured the activity of 10 different enzymes produced by 48 model fungal species on leaf litter in laboratory microcosms. Taxa included closely related species with different ecologies (i.e. species in different “functional guilds”) and species with publicly available genomes. Decomposition capabilities differed less among phylogenetic lineages of fungi than among different functional guilds. Activity of carbohydrases and acid phosphatase was significantly higher in litter colonized by saprotrophs compared to ectomycorrhizal species. By contrast, oxidoreductase activities per unit fungal biomass were statistically similar across functional guilds, with white rot fungi having highest polyphenol oxidase activity and ectomycorrhizal fungi having highest peroxidase activity. On the ecosystem level, polyphenol oxidase activity in soil correlated with the abundance of white rot fungi, while soil peroxidase activity correlated with the abundance of ectomycorrhizal fungi in soil. Copy numbers of genes coding for different enzymes explained the activity of some carbohydrases and polyphenol oxidase produced by fungi in culture, but were not significantly better predictors of activity than specific functional guild. Collectively, our data suggest that quantifying the specific functional guilds of fungi in soil, potentially through environmental sequencing approaches, allows us to predict activity of enzymes that drive soil biogeochemical cycles.

The roles that microorganisms play in carbon storage are not fully understood. Now modelling results show that the activity of a single group of soil fungi may significantly enhance ecosystem carbon-storage capacity.

© 2015 The Authors. New Phytologist © 2015 New Phytologist Trust. 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.

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.

Litter decay rates often correlate with the initial ratios of lignin:nitrogen (N) or lignin:cellulose in litter. However, the chemical and microbial mechanisms that give rise to these patterns are still unclear. To identify these mechanisms, we studied the decomposition of a model plant system, Arabidopsis thaliana, in which plants were manipulated to have low levels of lignin, cellulose, or litter N. Nitrogen fertilizer often increases the loss of cellulose, but it suppresses the breakdown of lignin in plant litter. To understand the mechanisms driving these patterns, we decomposed plants in litterbags for one year in control and N-fertilized plots in an Alaskan boreal forest. We found that litter N had a positive effect on total mass loss because it increased the loss of lignin, N, and soluble C. Lignin had a negative effect on rates of total litter mass loss due to decreases in the loss of cellulose and hemicellulose. Cellulose had a positive effect on lignin loss, supporting the concept of a "priming effect" for lignin breakdown. However, the low-cellulose plants also lost more of their original cellulose compared to the other plant types, indicating that decomposers mined the litter for cellulose despite the presence of lignin. Low-lignin litter had higher fungal biomass and N-acetyl glucosaminidase (NAG, a chitinase) activity, suggesting that lignin restricted fungal growth and may have influenced competitive interactions between decomposers. Nitrogen fertilization increased NAG activity in the early stages of decay. In the later stages, N fertilization led to increased cellulase activity on the litters and tended to reduce lignin losses. The transition over time from competition among decomposers to high cellulase activity and suppressed lignin loss under N fertilization suggests that, in N-limited systems, N fertilization may alter decomposer community structure by favoring a shift toward cellulose- and mineral-N users.

Empirical and modeling studies of the N cycle in temperate forests of eastern North America have focused on the mechanisms regulating the production of inorganic N, and assumed that only inorganic forms of N are available for plant growth. Recent isotope studies in field conditions suggest that amino acid capture is a widespread ecological phenomenon, although northern temperate forests have yet to be studied. We quantified fine root biomass and applied tracer-level quantities of U-(13)C(2)-(15)N-glycine, (15)NH(4) (+) and (15)NO(3) (-) in two stands, one dominated by sugar maple and white ash, the other dominated by red oak, beech, and hemlock, to assess the importance of amino acids to the N nutrition of northeastern US forests. Significant enrichment of (13)C in fine roots 2 and 5 h following tracer application indicated intact glycine uptake in both stands. Glycine accounted for up to 77% of total N uptake in the oak-beech-hemlock stand, a stand that produces recalcitrant litter, cycles N slowly and has a thick, amino acid-rich organic horizon. By contrast, glycine accounted for only 20% of total N uptake in the sugar maple and white ash stand, a stand characterized by labile litter and rapid rates of amino acid production and turnover resulting in high rates of mineralization and nitrification. This study shows that amino acid uptake is an important process occurring in two widespread, northeastern US temperate forest types with widely differing rates of N cycling.