Ectomycorrhizal Fungal Community Structure Research Articles

Tree genotype influences ectomycorrhizal fungal community structure: Ecological and evolutionary implications

Abstract Although the eco-evolutionary dynamics of multicellular organisms are intertwined with the microorganisms that colonize them, there is only a rudimentary understanding of how a host's genotype influences its microbiome. We utilize Populus angustifolia to test whether communities of essential symbionts, ectomycorrhizal fungi (EMF), vary among host genotypes. Further, we test whether EMF communities covary among tree genotypes with the chemistry of senescent leaves and aboveground biomass, traits important to tree fitness, and carbon and nutrient cycling. We found: 1) EMF composition, colonization and the Basidiomycota to Ascomycota ratio varied among tree genotypes (broad-sense heritability = 0.10–0.25). 2) EMF composition did not covary among genotypes with aboveground biomass but it did covary with senescent leaf chemistry ( rho = 0.29), primarily due to a single genotype. These findings demonstrate a link between tree genotype and EMF communities, which has implications for fungal diversity, host-symbiont interactions and aboveground-belowground linkages in ecological and evolutionary contexts.

Phosphorus availabilities in beech (Fagus sylvatica L.) forests impose habitat filtering on ectomycorrhizal communities and impact tree nutrition

Phosphorus (P) is an important nutrient, whose concentrations are declining in many European forest ecosystems. Here, we selected five old-aged temperate beech (Fagus sylvatica) forests that represented a sequence of decreasing soil P resources. We addressed the following hypotheses: (i) root P concentrations correspond to soil P concentrations, when P availability is suboptimal for tree nutrition, (ii) decreasing soil P concentrations, and increasing host P demand foster increasing ectomycorrhizal fungal (EMF) species richness and lead to a shift in the EMF community structure towards increasing soil exploration. We found that the decrease in P concentrations along the geosequence was less steep in the organic layer than that in the mineral topsoil. P concentrations in roots showed a positive relationship with P concentrations in soil, with a stronger correlation in coarse than in fine roots. This finding indicates that low P availability mainly affected P storage of the host. The root tips were completely colonized with EMF. In the organic layer EMF biomass was higher than that of saprophytic fungi, and correlated with inorganic P (Pi). In the mineral topsoil EMF biomass was about 10-fold lower than in the organic layer and biomass of saprophytes and microbial P, but not that of EMF, was correlated with Pi and phosphatase activities. Based on these results, we propose that beech P nutrition was mainly achieved by EMF in the organic layer. Variation in EMF species richness was unrelated to P in soil and decreased with increasing N in the organic layer. The EMF community structures were taxonomically divergent and filtered by habitat soil chemistry in the mineral layer and Pi in the organic layer between the P-rich forest and the P-poor forest. Changes in the taxonomic structures of the EMF did not result in corresponding changes in soil exploration. In conclusion, our results support a relationship between soil P concentrations and P storage in roots, but do not support mono-causal relationships between soil P and EMF species richness or hyphal soil exploration. Our results suggest that the taxonomic dissimilarities of the EMF along the P gradient were mainly driven by Pi concentrations in the organic layer and by the nutrient resources in the mineral layer.

Ectomycorrhizal communities in a Tuber aestivum Vittad. orchard in Poland

AbstractCultivation of the Burgundy truffle, Tuber aestivum Vittad., has become a new agricultural alternative in Poland. For rural economies, the concept of landscaping is often considerably more beneficial than conventional agriculture and promotes reforestation, as well as land-use stability. Considering examples from France, Italy, Hungary and Spain, truffle cultivation stimulates economic and social development of small, rural communities. Because there is no long tradition of truffle orchards in Poland, knowledge regarding the environmental factors regulating the formation of fruiting bodies of T. aestivum is limited. Thus, knowledge concerning ectomycorrhizal communities of T. aestivum host species is crucial to ensuring successful Burgundy truffle production. We investigated the persistence of T. aestivum ectomycorrhizae on roots of hazel (Corylus avellana L.) and oak (Quercus robur L.) and checked the host-species influence on community structure of ectomycorrhizal fungi. The study was conducted in an experimental plantation located in eastern Poland and established in 2008. We demonstrated that the number of fungal taxa was not significantly different between oak and hazel. However, the species composition differed between these two host trees. During the three-year study, we observed that species richness did not increase with the age of the plantation.

Temporal variation of Bistorta vivipara‐associated ectomycorrhizal fungal communities in the High Arctic

Ectomycorrhizal (ECM) fungi are important for efficient nutrient uptake of several widespread arctic plant species. Knowledge of temporal variation of ECM fungi, and the relationship of these patterns to environmental variables, is essential to understand energy and nutrient cycling in Arctic ecosystems. We sampled roots of Bistorta vivipara ten times over two years; three times during the growing-season (June, July and September) and twice during winter (November and April) of both years. We found 668 ECM OTUs belonging to 25 different ECM lineages, whereof 157 OTUs persisted throughout all sampling time-points. Overall, ECM fungal richness peaked in winter and species belonging to Cortinarius, Serendipita and Sebacina were more frequent in winter than during summer. Structure of ECM fungal communities was primarily affected by spatial factors. However, after accounting for spatial effects, significant seasonal variation was evident revealing correspondence with seasonal changes in environmental conditions. We demonstrate that arctic ECM richness and community structure differ between summer (growing-season) and winter, possibly due to reduced activity of the core community, and addition of fungi adapted for winter conditions forming a winter-active fungal community. Significant month × year interactions were observed both for fungal richness and community composition, indicating unpredictable between-year variation. Our study indicates that addressing seasonal changes requires replication over several years.

Chewing up the Wood-Wide Web: Selective Grazing on Ectomycorrhizal Fungi by Collembola

The mycelia of some symbiotic ectomycorrhizal fungi form extensive networks—the so called “wood-wide web”—that have key roles in biogeochemical cycling. By interacting with myriad soil organisms such as collembola, the fungi directly affect the functioning of above- and below-ground multitrophic interactions in ecosystems. Here we tested whether the grazing activities of collembola affected the growth of ectomycorrhizal fungi in single or mixed species axenic cultures, and their impact on ectomycorrhizal diversity in litterbags in the field. We also used 14CO2 pulse-labelling to test the effects of collembola on respiratory losses of recent plant assimilate from external mycelium of ectomycorrhizal fungi in symbiosis with Scots pine or birch. We found that the effects of collembola varied across species, and caused a significant reduction in the amount of 14CO2 released from external mycorrhizal mycelium from three of the eight species combinations but increased it in one. Selective grazing also significantly affected the community structure of ectomycorrhizal fungi. Our findings demonstrate the importance of collembola in regulating ectomycorrhizal fungal diversity and activity and below-ground pathways of carbon flow.

Elevated Atmospheric CO2 Affects Ectomycorrhizal Species Abundance and Increases Sporocarp Production under Field Conditions

Anthropogenic activities during the last century have increased levels of atmospheric CO2. Forest net primary productivity increases in response to elevated CO2, altering the quantity and quality of carbon supplied to the rhizosphere. Ectomycorrhizal fungi form obligate symbiotic associations with the fine roots of trees that mediate improved scavenging for nutrients in exchange for a carbohydrate supply. Understanding how the community structure of ectomycorrhizal fungi is altered by climate change is important to further our understanding of ecosystem function. Betula pendula and Fagus sylvatica were grown in an elevated CO2 atmosphere delivered using free air carbon dioxide enrichment (FACE) under field conditions in the U.K., and Picea abies was grown under elevated CO2 in glass domes in the Czech Republic. We used morphotyping and sequencing of the internal transcribed spacer region of the fungal ribosomal operon to study ectomycorrhizal community structure. Under FACE, un-colonised roots tips increased in abundance for Fagus sylvatica, and during 2006, sporocarp biomass of Peziza badia significantly increased. In domes, ectomycorrhizal community composition shifted from short-distance and smooth medium-distance to contact exploration types. Supply and competition for carbon belowground can influence ectomycorrhizal community structure with the potential to alter ecosystem function.

The distance decay of similarity in communities of ectomycorrhizal fungi in different ecosystems and scales

Summary Despite recent advances in understanding community ecology of ectomycorrhizal fungi, little is known about their spatial patterning and the underlying mechanisms driving these patterns across different ecosystems. This meta‐study aimed to elucidate the scale, rate and causes of spatial structure of ectomycorrhizal fungal communities in different ecosystems by analysing 16 and 55 sites at the local and global scales, respectively. We examined the distance decay of similarity relationship in species‐ and phylogenetic lineage‐based communities in relation to sampling and environmental variables. Tropical ectomycorrhizal fungal communities exhibited stronger distance‐decay patterns compared to non‐tropical communities. Distance from the equator and sampling area were the main determinants of the extent of distance decay in fungal communities. The rate of distance decay was negatively related to host density at the local scale. At the global scale, lineage‐level community similarity decayed faster with latitude than with longitude. Synthesis. Spatial processes play a stronger role and over a greater scale in structuring local communities of ectomycorrhizal fungi than previously anticipated, particularly in ecosystems with greater vegetation age and closer to the equator. Greater rate of distance decay occurs in ecosystems with lower host density that may stem from increasing dispersal and establishment limitation. The relatively strong latitude effect on distance decay of lineage‐level community similarity suggests that climate affects large‐scale spatial processes and may cause phylogenetic clustering of ectomycorrhizal fungi at the global scale.

Ectomycorrhizal Fungal Communities of Red Pine (Pinus densiflora) Seedlings in Disturbed Sites and Undisturbed Old Forest Sites

This study aimed to investigate differences in ectomycorrhizal (ECM) fungal communities between disturbed sites and undisturbed old forest sites. ECM root tips of Pinus densiflora were collected from 4 sites disturbed by human activities and 3 undisturbed old forest sites adjacent to the disturbed sites. Results in this study showed that the number of ECM root tips, species diversity, and number of species were significantly higher in the disturbed sites than in the undisturbed sites, suggesting that the ECM fungal community structure was affected by the degree of disturbance.

Phylogenetic structure of ectomycorrhizal fungal communities of western hemlock changes with forest age and stand type

On Vancouver Island, British Columbia, fertilization with nitrogen (N) and phosphorus (P) following clearcutting increases growth of western hemlock. To explore whether fertilization also resulted in ectomycorrhizal fungal communities that were more or less similar to neighboring unlogged stands, we sampled roots from western hemlock from three replicate plots from each of five different, well-characterized, forest stand types that differed in site type, and in logging and fertilization history. We harvested four samples of 100 ectomycorrhizal root tips from each plot, a total of 60 samples per stand type. From each sample, we analyzed fungal ribosomal internal transcribed spacers and 28S DNA, sequencing 15-29 clones per sample and 60-116 clones per plot. We detected 147 fungal operational taxonomic units among a total of 1435 sequences. Craterellus tubaeformis was frequently present and resulted in a pattern of phylogenetic overdispersion in the fungal communities. Fungal species composition was strongly correlated with foliar nitrogen concentration. However, other site quality factors were also important because the fertilized regenerating hemlock and mature hemlock-amabilis fir forests had similar foliar nitrogen content but little overlap in fungal species. Compared with unfertilized regenerating forests, fungal communities in N + P-fertilized regenerating forests had significantly more species overlap with old growth forests. However, the fungal communities of all regenerating forest were similar to one another and all differed significantly from older forests. By correlating fungal clades with habitats, this research improves understanding of how forest management can contribute to maintaining diverse ectomycorrhizal fungal communities across a landscape.

Scaling up: examining the macroecology of ectomycorrhizal fungi

Ectomycorrhizal (ECM) fungi play major ecological roles in temperate and tropical ecosystems. Although the richness of ECM fungal communities and the factors controlling their structure have been documented at local spatial scales, how they vary at larger spatial scales remains unclear. In this issue of Molecular Ecology, Tedersoo et al. (2012) present the results of a meta-analysis of ECM fungal community structure that sheds important new light on global-scale patterns. Using data from 69 study systems and 6021 fungal species, the researchers found that ECM fungal richness does not fit the classic latitudinal diversity gradient in which species richness peaks at lower latitudes. Instead, richness of ECM fungal communities has a unimodal relationship with latitude that peaks in temperate zones. Intriguingly, this conclusion suggests the mechanisms driving ECM fungal community richness may differ from those of many other organisms, including their plant hosts. Future research will be key to determine the robustness of this pattern and to examine the processes that generate and maintain global-scale gradients of ECM fungal richness.

Genetic host-tree effects on the ectomycorrhizal community and root characteristics of Norway spruce

A greenhouse experiment was used to study the effects of host genotype on short root formation and ectomycorrhizal (ECM) fungal community structure in Norway spruce (Picea abies (L.) Karst.). Rooted cuttings representing 55 clones were inoculated with a mix of vegetative hyphae of five ECM fungal species (Laccaria sp., Amphinema byssoides, Piloderma sp., Cadophora finlandia, Paxillus involutus). After one growing season, the ECM fungal community structure was determined by amplifying the fungal internal transcribed spacer (ITS) of ribosomal DNA directly from ECM root tips. Restriction profiles of obtained amplicons were then compared to those of the inoculated strains. Spruce clones differed in their ECM fungal community composition; we found a statistically significant clone-specific effect on ECM fungal diversity and dominating fungal species. Nevertheless, the broad sense heritabilities of the levels of Laccaria sp., Piloderma sp. and A. byssoides colonisations as well as the ECM fungal community structure were low (H(2) = 0.04-0.11), owing to the high within-clone variation. As nitrogen concentration of needles correlated negatively with ECM fungal richness, our results imply that in the experimental conditions nutrient acquisition of young trees may benefit from colonisation with only one or two ECM fungal species. The heritability of short root density was moderate (H(2) = 0.41) and highest among all the measured shoot and root growth characteristics of Norway spruce cuttings. We suggest that the genetic component determining root growth and short root formation is significant for the performance of young trees in natural environments as these traits drive the formation of the below-ground symbiotic interactions.

Towards global patterns in the diversity and community structure of ectomycorrhizal fungi

Global species richness patterns of soil micro-organisms remain poorly understood compared to macro-organisms. We use a global analysis to disentangle the global determinants of diversity and community composition for ectomycorrhizal (EcM) fungi-microbial symbionts that play key roles in plant nutrition in most temperate and many tropical forest ecosystems. Host plant family has the strongest effect on the phylogenetic community composition of fungi, whereas temperature and precipitation mostly affect EcM fungal richness that peaks in the temperate and boreal forest biomes, contrasting with latitudinal patterns of macro-organisms. Tropical ecosystems experience rapid turnover of organic material and have weak soil stratification, suggesting that poor habitat conditions may contribute to the relatively low richness of EcM fungi, and perhaps other soil biota, in most tropical ecosystems. For EcM fungi, greater evolutionary age and larger total area of EcM host vegetation may also contribute to the higher diversity in temperate ecosystems. Our results provide useful biogeographic and ecological hypotheses for explaining the distribution of fungi that remain to be tested by involving next-generation sequencing techniques and relevant soil metadata.

Long-term effect of apatite on ectomycorrhizal growth and community structure

Ectomycorrhizal (ECM) fungi are efficient at taking up phosphorus (P) from mineral sources, such as apatite, which are not easily available to the host trees. Since ECM fungal species differ in P uptake rates, it can be expected that the composition of the ECM fungal community will change upon exposure to apatite, provided that the P transfer is rewarded by more carbon being transferred to the fungal symbiont. Control and apatite-amended mesh bags were buried in pairs in the humus layer of a P-poor Norway spruce forest. The ECM fungal community that colonized these bags was analyzed by DNA extraction, PCR amplification of the internal transcribed spacer (ITS) region, cloning, and random sequencing. Fungal biomass was estimated by ergosterol analysis. No change in the ECM fungal community structure was seen after 5years of apatite exposure, although the fungal biomass increased threefold upon apatite amendment. Our results indicate that host trees enhance carbon allocation to ECM fungi colonizing P sources in P-poor forests but the lack of change in the composition of the ECM fungal community suggests that P transfer rates were similar among the species. Alternatively, higher P transfer among certain species was not rewarded with higher carbon transfer from the host.

Dramatic changes in ectomycorrhizal community composition, root tip abundance and mycelial production along a stand‐scale nitrogen deposition gradient

• Nitrogen (N) availability is known to influence ectomycorrhizal fungal components, such as fungal community composition, biomass of root tips and production of mycelia, but effects have never been demonstrated within the same forest. • We measured concurrently the abundance of ectomycorrhizal root tips and the production of external mycelia, and explored the changes in the ectomycorrhizal community composition, across a stand-scale N deposition gradient (from 27 to 43 kg N ha⁻¹ yr⁻¹) at the edge of a spruce forest. The N status was affected along the gradient as shown by a range of N availability indices. • Ectomycorrhizal root tip abundance and mycelial production decreased five and 10-fold, respectively, with increasing N deposition. In addition, the ectomycorrhizal fungal community changed and the species richness decreased. The changes were correlated with the measured indices of N status, in particular N deposition and N leaching. • The relationship between the altered ectomycorrhizal community, root tip abundance and mycelial production is discussed in the context of the N parameters. We suggest that increased N deposition to forests will cause large changes in ectomycorrhizal fungal community structure and functioning, which, in turn, may result in reduced N uptake by roots and fungi, and increased losses of N by leaching.

Diversity and community structure of ectomycorrhizal fungi in Pinus thunbergii coastal forests in the eastern region of Korea

We investigated the diversity and community structure of ectomycorrhizal (EcM) fungi in Pinus thunbergii stands on the eastern coast of Korea. We established two 10×10-m plots in six forest stands and sampled soil blocks containing rootlets of mature P. thunbergii trees. EcM roots were classified into morphological groups, and the fungal taxa associated with each morphotype were identified by sequencing the nuclear rDNA internal transcribed spacer region. Cenococcum geophilum and the Atheliales, Clavulinaceae, Russulaceae and Thelephoraceae species were the main members of the EcM fungal community, which included a total of 68 observed fungal taxa. As a whole, the community consisted of a few dominant fungal taxa, such as C. geophilum (28.6% relative abundance), and a large number of rare fungal taxa that showed low abundances and local distributions. Colonization patterns at the local site scale and at the scale of the study plots greatly differed among the EcM fungal taxa; C. geophilum was distributed extensively and was dominant in several study sites, whereas a certain Lactarius sp. was distributed locally but dominated in a given study site. We conclude with a discussion of the relationship between colonization patterns of EcM fungi and soil and environmental conditions.

Ectomycorrhizal fungi: the symbiotic route to the root for phosphorus in forest soils

Many forest trees have evolved mutualistic symbioses with ectomycorrhizal (ECM) fungi that contribute to their phosphorus (P) nutrition. Forest productivity is frequently limited by P, a phenomenon that is likely to become more widespread under future conditions of elevated atmospheric CO2 concentration [CO2]. It is thus timely that this review considers current understanding of the key processes (absorption, translocation and transfer to the plant host) in ECM fungus-mediated P nutrition of forest trees. Solubilisation of inorganic P (Pi) and hydrolysis of organic P by ECM fungi in soil occurs largely at the growing mycelial front, where Pi absorption is facilitated by high affinity transporters. While large gaps remain in our understanding of the physiological and molecular mechanisms that underpin movement of P in ECM mycelia in soil and P transfer to the plant, host P demand seems likely to be a key driver of these processes. ECM fungi may make considerable contributions to meeting the likely increased P demand of trees under elevated [CO2] via increased colonization levels, shifts in ECM fungal community structure and changed patterns of EMM production. Further research into the spatial scale of ECM-mediated P movements in soil, along with the interplay between ECM fungi and other soil microflora is advocated.

Diversity and community structure of ectomycorrhizal fungi in <i>Pinus thunbergii</i> coastal forests in the eastern region of Korea

We investigated the diversity and community structure of ectomycorrhizal (EcM) fungi in Pinus thunbergii stands on the eastern coast of Korea. We established two 10 × 10-m plots in six forest stands and sampled soil blocks containing rootlets of mature P. thunbergii trees. EcM roots were classified into morphological groups, and the fungal taxa associated with each morphotype were identified by sequencing the nuclear rDNA internal transcribed spacer region. Cenococcum geophilum and the Atheliales, Clavulinaceae, Russulaceae and Thelephoraceae species were the main members of the EcM fungal community, which included a total of 68 observed fungal taxa. As a whole, the community consisted of a few dominant fungal taxa, such as C. geophilum (28.6% relative abundance), and a large number of rare fungal taxa that showed low abundances and local distributions. Colonization patterns at the local site scale and at the scale of the study plots greatly differed among the EcM fungal taxa; C. geophilum was distributed extensively and was dominant in several study sites, whereas a certain Lactarius sp. was distributed locally but dominated in a given study site. We conclude with a discussion of the relationship between colonization patterns of EcM fungi and soil and environmental conditions.

General principles in the community ecology of ectomycorrhizal fungi

Knowledge of the factors that determine ectomycorrhizal fungal community structure is essential in many areas of practical significance including conservation, habitat restoration, prevention or amelioration of species invasions, and the prediction of responses to climate change. With respect to these goals, however, community ecology, in general, and ectomycorrhizal fungal community ecology, in particular, have been rather disappointing. Indeed, some feel that community ecology is, at best, an esoteric discipline and, at worst, an inane one. But there is hope. As we apply what has been learned about other organisms concerning the relationships between functional traits and success (abundance), it may be possible to elucidate general principles that govern much of the structuring of ectomycorrhizal fungal communities. A hierarchical model of ectomycorrhizal fungal community structure is presented that involves abiotic filtering of immigrant propagules based on functional traits, followed by interspecific competition as ameliorated by disturbance and habitat partitioning, the outcomes of which are dependent on functional traits.

Ectomycorrhizal fungi and interspecific competition: species interactions, community structure, coexistence mechanisms, and future research directions

The field of ectomycorrhizal fungal (EMF) ecology has largely developed outside the ecological mainstream, owing in large part to the challenges in studying the structure and dynamics of EMF communities. With advances in molecular identification and other research techniques, however, there has been growing interest among mycologists and ecologists in understanding how different ecological factors affect EMF community structure and diversity. While factors such as soil chemistry and host specificity have long been considered important, an increasing number of laboratory and field studies have documented that interspecific competition also has a major impact on EMF species interactions and may significantly influence EMF community structure. In this review, I examine the progress that has been made in understanding the nature of EMF competition. Currently, there are four conclusions that can be drawn: negative competitive effects are rarely reciprocal; competitive outcomes are environmentally context-dependent; field distributions often reflect competitive interactions; and timing of colonization influences competitive success. In addition, I highlight recent studies documenting links between competitive coexistence and EMF community structure, including checkerboard distributions, lottery models, storage effects, and colonization-competition tradeoffs. Finally, I discuss several aspects of EMF competition needing further investigation and some newer methods with which to address them.

Changes in community structure of ectomycorrhizal fungi associated with Pinus montezumae across a volcanic soil chronosequence at Sierra Chichinautzin, Mexico

Ectomycorrhizal (ECM) communities of Pinus montezumae Lamb. var. montezumae were studied across a volcanic soil chronosequence at Sierra del Chichinautzin, Mexico, to investigate differences in community structure at sites with different soil quality. Study sites were located on volcanic soils of different ages. Both aboveground and belowground fungal communities were compared for 3 years. Species abundance, richness, and diversity were compared among sites. Significant differences were found among the three sites for sporocarp abundance and biomass but not for total ECM root tips. The more diverse sporocarp community was found at the youngest, less fertile site. Dominant species at the sporocarp and ECM morphotype levels differed across the chronosequence. The largest proportion of sporocarp species was site-exclusive, which suggests that aboveground communities depend upon soil conditions. Contrarily, 85% of ECM morphotypes were present at least at two sites. The poor correspondence between the aboveground and belowground views of the ECM fungal community may be due to differences in sampling methodology and level of identification. Inocybe and Laccaria species were abundant fruiters at all sites, and as multisite fungi, they may be tested for inoculum efficiency to be used in reforestation programs in the surroundings of Mexico City.