Fairy Rings Research Articles

Characteristics of Suillus bovinus fairy rings and genets associated with thinning intensity in Pinus densiflora forests

Characteristics of Suillus bovinus fairy rings and genets associated with thinning intensity in Pinus densiflora forests

Fairy rings harbor distinct soil fungal communities and high fungal diversity in a montane grassland

Abstract Increasing numbers of fungal species have been described recently from semi-natural grassland soils, raising the conservation interest of these species-rich habitats. Here, we characterize the soil fungal community inhabiting six fairy rings in a montane grassland of the Eastern Pre-Pyrenees through fungal DNA metabarcoding of ITS2 amplicons. Distinct soil fungal communities were observed outside of the rings compared to inside the ring areas. Higher abundances of fungi belonging to Pleosporales and Eurotiales were observed outside fairy rings, whereas zones belonging to the fairy rings showed higher abundances of Agaricales. Fungal diversity was higher inside the rings than outside. We found diverse saprotrophic or putative saprotrophic taxa associated with the studied rings, including the genera Clavaria, Psathyrella, Tricholoma, Amanita and Lycoperdon. These findings highlight the importance of particular keystone taxa in the structuring of fungal communities and their effect on the overall grassland fungal community.

One ring to rule them all: an ecosystem engineer fungus fosters plant and microbial diversity in a Mediterranean grassland.

Species coexistence in grasslands is regulated by several environmental factors and interactions with the soil microbial community. Here, the development of the Basidiomycetes fungus Agaricus arvensis, forming fairy rings, in a species-rich Mediterranean grassland, is described. Effects of the mycelial front on plants, fungi and bacteria were assessed by vegetation survey and next generation sequencing approaches. Our results showed a fungal-dependent shift in the community structure operated by a wave-like spread of fairy rings that decreased plant, fungal and bacterial diversity, indicating a detrimental effect of fairy rings on most species. The fairy rings induced successional processes in plants that enhanced the replacement of a community dominated by perennial plants with short-living and fast-growing plant species. In parallel, fungal and bacterial communities showed evident differences in species composition with several taxa associated within distinct sampling zone across the fairy rings. Notably, bacteria belonging to the Burkholderia genus and fungi of the genus Trichoderma increased in response to the advancing mycelium of A.arvensis. The profound changes in community composition and the overall increase in taxa diversity at ecosystemic scale suggest that fairy ring-forming fungi may act as ecosystem engineer species in Mediterranean grasslands.

Opportunistic fungi found in fairy rings are present on different moss species in the Antarctic Peninsula

We surveyed the distribution and diversity of fungi present in moss fairy rings from the South Shetland Islands. In the different islands accessed, the mosses Bartramia patens, Brachythecium austrosalebrosum, Bryum pseudotriquetrum, Pohlia nutans, Polytrichastrum alpinum, Sanionia uncinata, Syntrichia magellanica, and Syntrichia saxicola were infected with fairy rings. Among them, B. patens, B. pseudotriquetrum, P. nutans, P. alpinum, S. magellanica, and S. saxicola were reported for the first time as species susceptible to infection with fairy rings. From five different fairy ring moss species sampled, we isolated 40 fungal taxa identified as belonging to the genera Alpinaria, Cadophora, Cladosporium, Chalara, Cosmospora, Drechmera, Glarea, Gyoerffyella, Hymenoscyphus, Juncaceicola, Melanodiplodia, Mortierella, Mycosysmbioses, Pseudogymnoascus, Phoma, and Velucrispora. A high level of fungal richness was associated with the infected mosses, and Mortierella was the dominant genus. However, most of the fungi were present as minor components of the fungal assemblages. Among the mosses studied, S. uncinata harboured the greatest fungal diversity. Some fungal taxa present have previously been reported as opportunistic plant pathogens, including Cladosporium sp. and Phoma herbarum. We hypothesize that some of the fungi recovered from fairy ring mosses might represent secondary opportunistic pathogens and contribute to the reduced natural defences of the infected mosses, thus accelerating the dissemination of the pathogenic fairy rings in the Antarctic Peninsula. In addition, the presence of fairy rings on previously unreported moss species suggests that the disease may be becoming more widespread in Antarctica.

Atmospheric fallout impact on 210Po and 210Pb content in wild growing mushrooms

The atmospheric fallout impact on 210Po and 210Pb content in fruitbodies of wild growing mushrooms collected from different environments were investigated. The samples of morphologically different mushroom species, namely bay bolete (Imleria badia (Fr.) Vizzini), slippery jack (Suillus luteus (L.) Roussel), fairy ring mushroom (Marasmius oreades (Bolton) Fr.) and common earthball (Scleroderma citrinum Pers.) with their mycelium and soil substrate were collected. Their fruitbodies were separated into cap skin, cap flesh and stem. Also mycelium and soil substrate were collected. The results showed the highest 210Po and 210Pb activity concentrations were found in Marasmius oreades cap skin: 3.20 ± 0.12 and 21.1 ± 0.5 Bq kg−1 ww, respectively, which constituted 31.2 and 78.7% of their content in the total fruitbody mass. In the case of open space wild growing mushrooms, their whole caps contain a significantly higher amount of 210Po and 210Pb when compared to the stem, and their content in the whole cap was determined mainly by concentrations in the cap skin.

Fairy rings magically prevent mutation

Fungal Genetics Mutation can often occur as part of the process of cellular division and may have deleterious consequences for multicellular organisms. Through genomic sequencing of Marasmius oreades , a species of fairy ring mushroom, Hiltunen et al. found that in this relatively long-lived species, the accumulation of mutations is an order of magnitude less than previously discovered for any organism. This could not be attributed to purifying selection and indicates that this species has evolved high-fidelity replication and/or repair mechanisms to prevent mutation accumulation. Given that fungi, unlike mammals, do not sequester their reproductive germ cells, this is of interest in understanding how an organism can police its own cell division to maintain a low rate of mutation accumulation. Curr. Biol. 29 , 2758 (2019).

Germline Evolution: Sequestered Cells or Immortal Strands?

Mutation accumulation in long-lived fairy-ring mushrooms is orders of magnitude lower than predicted based on per-cell division mutation rates in other organisms. A possible explanation is the maintenance of 'immortal' template-DNA in the active periphery of the fairy ring.

A Fairy Chemical, Imidazole-4-carboxamide, is Produced on a Novel Purine Metabolic Pathway in Rice

Rings or arcs of fungus-regulated plant growth occurring on the floor of woodlands and grasslands are commonly called “fairy rings”. Fairy chemicals, 2-azahypoxanthine (AHX), imidazole-4-carboxamide (ICA), and 2-aza-8-oxohypoxanthine (AOH), are plant growth regulators involved in the phenomenon. The endogeny and biosynthetic pathways of AHX and AOH in plants have already been proven, however, those of ICA have remained unclear. We developed a high-sensitivity detection method for FCs including ICA and the endogenous ICA was detected in some plants for the first time. The quantitative analysis of the endogenous level of ICA in rice and Arabidopsis were performed using 13C-double labeled ICA. In addition, the incorporation experiment and enzyme assay using the labeled compound into rice and partially purified fraction of rice indicated that ICA is biosynthesized from 5-aminoimidazole-4-carboxamide (AICA), a metabolite on the purine metabolic pathway. The relationship between ICA and AHX was also discussed based on quantitative analysis and gene expression analysis.

The Influence of Microfungi on the Mycelial Growth of Ectomycorrhizal Fungus Tricholoma matsutake.

Pine mushroom (Tricholoma matsutake) is one of the most valued ectomycorrhizal fungi in Asia because of its unique pine-like aroma; however, due to exceptionally slow growth of its mycelia in artificial conditions, its cultivation has been largely deemed as not possible. Previous studies have shown that some bacteria and a few Trichoderma species associated with pine mushroom promoted the growth of T. matsutake isolate, but this effect is relatively unexplored. In this study, we investigated the diversity of microfungi in the fairy ring of T. matsutake and their effect on the growth of T. matsutake isolate. From 184 fungal isolates, 28 species were identified based on suitable molecular markers. Penicillium was most frequently observed (16 species), followed by Trichoderma (4 species). Five Zygomycota species showed a high promoting effect on the growth of T. matsutake while the effects of ascomycetes were mixed. The microfungi that promote the growth of T. matsutake can be useful for forest nursery and artificial cultivation of T. matsutake.

Effects of fairy ring fungi on plants and soil in the alpine and temperate grasslands of China

Soil fungi are considered to be key regulators of plant and soil relationships. The fairy rings (FRs) caused by basidiomycete fungi can influence plant productivity and soil nutrient and microbiome composition. We sought to explore the role of FRs in plant communities and soil properties for two types of grasslands in China. Plant and soil samples were collected from three concentric zones: outside the ring (OUT), on the ring (ON), and inside the ring (IN). Data were collected on plant productivity, plant diversity, soil properties, and soil bacterial diversity. We found that FRs significantly improved plant productivity and diversity in both alpine and temperate grasslands. In the alpine grassland, soil water content, pH and bacterial diversity were lower in the ON zone compared to the OUT zone. Likewise, in temperate grasslands, water content was lower in the ON zone compared to both OUT and IN zones. Also, soil pH and bacterial diversity were higher on the ON zone compared to other both zones. Based on our data, we believe that FR fungi increase plant productivity and diversity, and change the composition of soil bacterial species and diversity. We suggest that the effects of FR fungi on plants included the increase of the soil nutrient content and the effects of FR fungi on soil bacteria included the changes in soil water content and pH value.

Genome sequence analysis of the fairy ring-forming fungus Lepista sordida and gene candidates for interaction with plants

Circular patterns called “fairy rings” in fields are a natural phenomenon that arises through the interaction between basidiomycete fungi and plants. Acceleration or inhibition of plant vegetative growth and the formation of mushroom fruiting bodies are both commonly observed when fairy rings form. The gene of an enzyme involved in the biosynthesis of these regulators was recently isolated in the fairy ring-forming fungus, Lepista sordida. To identify other genes involved in L. sordida fairy ring formation, we used previously generated sequence data to produce a more complete draft genome sequence for this species. Finally, we predicted the metabolic pathways of the plant growth regulators and 29 candidate enzyme-coding genes involved in fairy-ring formation based on gene annotations. Comparisons of protein coding genes among basidiomycete fungi revealed two nitric oxide synthase gene candidates that were uniquely encoded in genomes of fairy ring-forming fungi. These results provide a basis for the discovery of genes involved in fairy ring formation and for understanding the mechanisms involved in the interaction between fungi and plants. We also constructed a new web database F-RINGS (http://bioinf.mind.meiji.ac.jp/f-rings/) to provide the comprehensive genomic information for L. sordida.

Diversity and effect of Trichoderma isolated from the roots of Pinus densiflora within the fairy ring of pine mushroom (Tricholoma matsutake).

Pine mushroom (PM, Tricholoma matsutake) is an important ectomycorrhizal fungus in Asia primarily due to its value as a food delicacy. Recent studies have shown that fairy rings of PM have distinctive fungal communities, which suggests that other fungi influence the growth of PM. Trichoderma is a well-known saprotrophic fungus commonly found in pine roots within PM fairy rings; however, little is known about the diversity of Trichoderma associated with PM and how these species influence PM growth. This study focused on diversity of Trichoderma isolated from pine roots within PM fairy rings and how these species affect the growth of PM isolate. Based on tef1a phylogenetic analyses, nine Trichoderma species (261 isolates) were identified. Trichoderma songyi and T. spirale were the dominant species, and Trichoderma community varied geographically. Growth experiments indicated that metabolites from five Trichoderma species had a significant influence on the growth of PM isolates. Metabolites of two Trichoderma species increased PM growth, while those of three Trichoderma species suppressed the growth. Within the fairy rings, Trichoderma that had a positive or neutral effect comprised the majority of Trichoderma communities. The results of this study suggest that various Trichoderma species co-exist within PM fairy rings and that these species influence PM growth.

C–H activation charms fairy chemical

Under fairy rings, lush circles of turf, is a natural product made by fungi that spurs the growth of grass. Researchers have now created bioactive compounds that stimulate plant growth even better than the natural product (Org. Lett. 2018, DOI: 10.1021/acs.orglett.8b02407). Crafted via C–H activation, these potent variants should help elucidate the mechanism of the fairy ring chemical and could eventually be used to increase crop yields. Hirokazu Kawagishi of Shizuoka University isolated the molecule responsible for the extra-tall growth of grass in fairy rings he observed on campus. The source was the mushrooms that caused the rings, Lepista sordida, and the molecule was 2-azahypoxanthine (AHX) (ChemBioChem 2010, DOI: 10.1002/cbic.201000112). He dubbed it and its related metabolites fairy chemicals. Kawagishi and his colleagues then found that every crop they tested not only responded to AHX but also made AHX, suggesting it is a common growth hormone (Biosci., Biotechnol., Biochem. 2018,

The optimal Redfield N: P ratio caused by fairy ring fungi stimulates plant productivity in the temperate steppe of China

Abstract The Redfield ratio (or stoichiometry) is widely used as a reference to differentiate between nitrogen (N) and phosphorus (P) limitations in plankton and in the deep oceanic waters. Whether the Redfield ratio is applicable to plant and soil fungal growth is rarely considered. Fairy rings (FRs) caused by Agaricus gennadii can influence plant productivity and soil nutrient composition. However, the internal mechanisms associated with the optimal Redfield N: P ratio remain unclear. Changes in plant and soil stoichiometry in three concentric zones of FRs occurring in the temperate steppe of China, namely outside the ring (Out), on the ring (On), and inside the ring (In), were assessed in order to confirm the effects of FR fungi on plants and soil and explain the mechanisms using nutrient stoichiometry. We observed a significantly higher aboveground biomass only in the On zone. The plant N: P ratio was 14.5, 10.4, and 7.3 in the Out, On, and In zones, respectively. This indicates that the limiting element of the aboveground biomass was P in the Out zone and N in the In zone, while the On zone possessed an optimal plant N: P ratio and relatively high aboveground biomass. As with the plant N: P ratio, the On and In zones displayed a significantly lower soil inorganic N: available P ratio than the Out zone. The plant N: P ratio was highly positively correlated with the soil inorganic N: available P ratio. Our results suggest that FR fungi with low N: P ratio shift the soil ecosystem from P- to N-limited, thereby accelerating the uptake of soil N by plants. As with the plant N: P ratio, the soil inorganic N: available P ratio can also be used to evaluate whether N or P is more limiting for plant production in grassland ecosystems.

Cover: Journal of Basic Microbiology. 6/2018

Journal of Basic MicrobiologyVolume 58, Issue 6 COVER PICTUREFree Access Cover: Journal of Basic Microbiology. 6/2018 First published: 03 June 2018 https://doi.org/10.1002/jobm.201870020AboutPDF ToolsRequest permissionExport citationAdd to favoritesTrack citation ShareShare Give accessShare full text accessShare full-text accessPlease review our Terms and Conditions of Use and check box below to share full-text version of article.I have read and accept the Wiley Online Library Terms and Conditions of UseShareable LinkUse the link below to share a full-text version of this article with your friends and colleagues. Learn more.Copy URL Share a linkShare onFacebookTwitterLinkedInRedditWechat Graphical Abstract Cover illustration: Floccularia luteovirens, the edible mushroom distributed in the alpine meadow of Qinghai-Tebit plateau. The fungus forms visible fruiting bodies that can occur in fairy rings. (Photo: Rui Xing, Key Laboratory of Adaptation and Evolution of Plateau Biota, Northwest Institute of Plateau Biology, Chinese Academy of Sciences, Xining Qinghai, P.R. China) Volume58, Issue6June 2018 RelatedInformation

Changes in soil bacterial communities in response to the fairy ring fungus Agaricus gennadii in the temperate steppes of China

Fairy rings (FRs), mysterious circles of fungal fruiting bodies that occur in open grassy areas, have long been reported, but scientists know little about their effects on the physiochemical properties of soil and the associated bacterial communities. We investigated three concentric zones of Agaricus gennadii FRs in June, August and October 2016 in a temperate steppe of China outside of rings (OUT), within rings (IN) and adjacent to fruiting bodies (ON) to determine the effects of FR fungus on soil properties and bacterial community structure. Significantly higher aboveground biomass was only observed in the ON zone because of an increase in available soil P (P < 0.05). Soil total N, total P and inorganic N were lower in the ON and IN zones than in the OUT zone. The bacterial Shannon and Chao 1 indices were significantly higher in samples associated with the rings in August and October (P < 0.05). At the family level, only the abundance of Microbacteriaceae was significantly higher in the ON zone than in the OUT zone during the three-month study period (P < 0.05), indicating that species of the Microbacteriaceae are associated with Agaricus gennadii FRs. Moreover, the changes of soil pH and soil available P caused by FRs were found to be better indicators of changes in soil bacterial communities than total N, total P and inorganic N in soil.

A Model of Vegetation Cover in Conditions of Resource Scarcity: Fairy Rings in Namibia

A mosaic of barren grounds (bars) and areas covered by vegetation often forms in grassy or shrubby communities in conditions of scarcity of environmental resources (e.g., water). Such landscapes have been named “two-phase mosaics”; this term emphasizes the discreteness of vegetation cover units. Fairy rings (FRs) are an example of such structures. There are two sets of competing hypotheses on the reasons behind FR formation: insect activity and self-organization. One of the main arguments against the second set of hypotheses is their inability to explain the FR life cycle: their emergence, ripening, maturation, and disappearance (death). The article proposes a simple cellular-automaton model of the vegetation cover formation. The model imitates the scarcity of resources (water and ash constituents) and generates different variants of the two-phase mosaic. The results depend on two parameters: limitation of resource inflow and plant growth rate. Sixteen percent of combinations of these parameters result in the formation of structures similar to FRs. The model reproduces not only the vegetation distribution pattern observed in the nature but also individual FR life cycles that are consistent with field descriptions. Thus, the model removes the main objection to self-organization as the main mechanism of FR formation.

Off-site transport of fungicides with runoff: A comparison of flutolanil and pentachloronitrobeneze applied to creeping bentgrass managed as a golf course fairway

Flutolanil and pentachloronitrobenzene (PCNB) are fungicides used to control or suppress foliar and soil borne diseases in turf and ornamental crops. On golf courses, sports fields, sod farms and commercial lawns these fungicides are used as preventive treatments to combat snow mold, brown patch and fairy ring. Depending on the aquatic organism, flultolanil and PCNB are considered to be moderately to highly toxic. Therefore runoff or drift from treated areas may be hazardous to organisms in adjacent aquatic sites. This research compared the transport of flutolanil and PCNB with runoff from turfgrass managed as a golf course fairway. The quantity of fungicide transported with runoff and observations reported with the chemographs followed trends in agreement with the chemical properties of the compounds. Overall, we observed the rate of transport for flutolanil was greater than PCNB, which contributed to the more than 12 times larger load (µg/m2) of flutolanil transported off-site at the conclusion of the simulated storm runoff. A better understanding of the off-site transport of pesticides with runoff is needed to make informed decisions on management practices to reduce potential adverse effects on non-target organisms, as well as maintain control of targeted pests in the area of application. In addition, data obtained with this research can be used in model simulations to predict nonpoint source pollution potentials beyond experimental conditions.

Host genetic variation strongly influences the microbiome structure and function in fungal fruiting-bodies.

Despite increasing knowledge on host-associated microbiomes, little is known about mechanisms underlying fungus-microbiome interactions. This study aimed to examine the relative importance of host genetic, geographic and environmental variations in structuring fungus-associated microbiomes. We analyzed the taxonomic composition and function of microbiomes inhabiting fungal fruiting-bodies in relation to host genetic variation, soil pH and geographic distance between samples. For this, we sequenced the metagenomes of 40 fruiting-bodies collected from six fairy rings (i.e., genets) of a saprotrophic fungus Marasmius oreades. Our analyses revealed that finegenetic variations between host fungi could strongly affect their associated microbiome, explaining, respectively, 25% and 37% of the variation in microbiome structure and function, whereas geographic distance and soil pH remained of secondary importance. These results, together with the smaller genome size of fungi compared to other eukaryotes, suggest that fruiting-bodies are suitable for furthergenome-centric studies on host-microbiome interactions.

Microbial communities inhabiting the fairy ring of Floccularia luteovirens and isolation of potential mycorrhiza helper bacteria.

Floccularia luteovirens, an important edible mushroom widely distributed in the Qinghai-Tibet plateau, is ecologically important as an ectomycorrhizal fungus and can form the fairy ring. To explore the influence of F. luteovirens fairy ring on soil microbial communities, we compared the soil microbial communities in three different fairy ring zones (inside the fairy ring (IN); beneath the fairy ring (ON); and outside the fairy ring (OUT)). A total of 1.77 million bacterial reads and 1.59 million fungal reads were obtained. Moreover, sequence clustering yielded 519,613 (57,735 per sample) bacterial OTUs, and 513,204 (57,023 per sample) fungal OTUs representing. Microbial diversity was lower in samples from the ON zone compared with the other two zones. Mycorrhiza helper bacteria (MHB) such as Bradyrhizobium and Paenibacillus were more common in the ON zone, and we isolated four potential MHB from rhizosphere soil. Canonical correspondence analysis showed that the soil nutritional condition and physical changes caused by F. luteovirens shaped the microbial communities in the ON zone. This is the first report on the study of soil microbial diversity influenced by fairy ring F. luteovirens, and further studies need to be conducted to study the ecological function influenced by this species.