Habitat-specific changes of plant and soil microbial community composition in response to fairy ring fungus Agaricus xanthodermus on the Qinghai-Tibet Plateau

Juan Du, Cong He, Fuxin Wang, Ning Ling, Shengjing Jiang

PDF(4929 KB)
PDF(4929 KB)
Soil Ecology Letters ›› 2024, Vol. 6 ›› Issue (3) : 230214. DOI: 10.1007/s42832-023-0214-2
RESEARCH ARTICLE

Habitat-specific changes of plant and soil microbial community composition in response to fairy ring fungus Agaricus xanthodermus on the Qinghai-Tibet Plateau

Author information +
History +

Highlights

● A new fairy ring fungus was reported in this study.

● Fairy ring fungi influence plants and soil microbes by promoting soil nutrients.

● The effect of fairy ring fungi on plants and soil microbes depends on the habitat type.

Abstract

Fairy rings are common in diverse global biomes and often appear as lush vegetation in one to three concentric zones caused by the spread of mycelia in grassland ecosystems. However, the underlying mechanisms and environmental adaptation of fairy rings remain largely unclear. In this study, two fairy rings (A and B) caused by Agaricus xanthodermus were sampled on the Qinghai-Tibet Plateau during a time when fairy rings are most obvious. By conducting a vegetation survey and high-throughput sequencing, the changes of plants and soil microorganisms to fairy ring fungi were examined. Plant above-ground biomass at both fairy rings was greatly increased by fairy ring fungi, but the response of dominant plant species is different at two fairy ring sites. In addition, bacterial and fungal communities significantly varied within distinct sampling zones across the fairy rings, and showed variable genus-specific responses at two fairy ring sites. At fairy ring A, soil available N:P ratio was essential in shaping the structure of plant and microbial community, while soil available N concentration was the most important predictor at fairy ring B. Taken together, our results indicated Agaricus xanthodermus fairy rings have variable effects on alpine meadow plants and soil microbes at different habitats. We propose that the impacts of fairy ring fungi on plants and microbes are determined by the level of soil available N concentration and available N:P ratio. These results contribute to a better understanding of the mechanisms through which fairy rings affect the vegetation of alpine meadows.

Graphical abstract

Keywords

Fairy rings / alpine meadow / soil microbes / plant-soil relationships

Cite this article

Download citation ▾
Juan Du, Cong He, Fuxin Wang, Ning Ling, Shengjing Jiang. Habitat-specific changes of plant and soil microbial community composition in response to fairy ring fungus Agaricus xanthodermus on the Qinghai-Tibet Plateau. Soil Ecology Letters, 2024, 6(3): 230214 https://doi.org/10.1007/s42832-023-0214-2

References

[1]
Allegrezza, M., Bonanomi, G., Zotti, M., Carteni, F., Moreno, M., Olivieri, L., Garbarino, M., Tesei, G., Giannino, F., Mazzoleni, S., 2022. Biogeography and shape of fungal fairy rings in the Apennine mountains, Italy. Journal of Biogeography49, 353–363.
CrossRef Google scholar
[2]
Angulo, V., Beriot, N., Garcia‐Hernandez, E., Li, E., Masteling, R., Lau, J.A., 2022. Plant–microbe eco-evolutionary dynamics in a changing world. New Phytologist234, 1919–1928.
CrossRef Google scholar
[3]
Bonanomi, G., Mingo, A., Incerti, G., Mazzoleni, S., Allegrezza, M., 2012. Fairy rings caused by a killer fungus foster plant diversity in species-rich grassland. Journal of Vegetation Science23, 236–248.
CrossRef Google scholar
[4]
Cao, M., Liu, F., Sun, L., Wang, Y., Wan, J., Wang, R., Zhou, H., Wang, W., Xu, J., 2021. Floccularia luteovirens modulates the growth of alpine meadow plants and affects soil metabolite accumulation on the Qinghai-Tibet Plateau. Plant and Soil459, 125–136.
CrossRef Google scholar
[5]
Caporaso, J.G., Lauber, C.L., Walters, W.A., Berg-Lyons, D., Huntley, J., Fierer, N., Owens, S.M., Betley, J., Fraser, L., Bauer, M., Gormley, N., Gilbert, J.A., Smith, G., Knight, R., 2012. Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. ISME Journal6, 1621–1624.
CrossRef Google scholar
[6]
Edgar, R.C., 2016. UNOISE2: improved error-correction for Illumina 16S and ITS amplicon sequencing. BioRxiv, 081257
[7]
Fidanza, M.A., Cisar, J.L., Kostka, S.J., Gregos, J.S., Schlossberg, M.J., Franklin, M., 2007. Preliminary investigation of soil chemical and physical properties associated with type-I fairy ring symptoms in turfgrass. Hydrological Processes21, 2285–2290.
CrossRef Google scholar
[8]
Jiang, S., Liu, Y., Luo, J., Qin, M., Johnson, N.C., Öpik, M., Vasar, M., Chai, Y., Zhou, X., Mao, L., Du, G., An, L., Feng, H., 2018. Dynamics of arbuscular mycorrhizal fungal community structure and functioning along a nitrogen enrichment gradient in an alpine meadow ecosystem. New Phytologist220, 1222–1235.
CrossRef Google scholar
[9]
Kang, S., Xu, Y., You, Q., Flügel, W.A., Pepin, N., Yao, T., 2010. Review of climate and cryospheric change in the Tibetan Plateau. Environmental Research Letters5, 015101.
CrossRef Google scholar
[10]
Karyagina, L.A., Mikhailovskaya, N.A., 1986. Determination of polyphenoloxidaze and peroxidase activity. Bulletin of the Academy of Sciences of the BSSR2, 40–41.
[11]
Lau, J.A., Lennon, J.T., 2011. Evolutionary ecology of plant–microbe interactions: soil microbial structure alters selection on plant traits. New Phytologist192, 215–224.
CrossRef Google scholar
[12]
Li, J., Guo, L., Wilson, G.W.T., Cobb, A.B., Wang, K., Liu, L., Zhao, H., Huang, D., 2022. Assessing soil microbes that drive fairy ring patterns in temperate semiarid grasslands. BMC Ecology and Evolution22, 130.
CrossRef Google scholar
[13]
Liu, F., Liu, P., Zhang, Y., Sun, L., Zhang, P., Cao, M., Zhou, H., Wang, W., Xu, J., 2021. Comparative metabolomics reveals that Agaricus bisporus fairy ring modulates the growth of alpine meadow plant on the Qinghai-Tibet Plateau. Ecological Indicators129, 107865.
CrossRef Google scholar
[14]
Marx, M.C., Wood, M., Jarvis, S.C., 2001. A microplate fluorimetric assay for the study of enzyme diversity in soils. Soil Biology & Biochemistry33, 1633–1640.
CrossRef Google scholar
[15]
Miller, S.L., Gongloff, A., 2021. Fairy rings, associated fungi, and assessment of their distribution across environmental variables using GIS. Fungal Ecology50, 101040.
CrossRef Google scholar
[16]
Oh, S.Y., Park, M.S., Cho, H.J., Lim, Y.W., 2018. Diversity and effect of Trichoderma isolated from the roots of Pinus densiflora within the fairy ring of pine mushroom (Tricholoma matsutake). PLoS One13, e0205900.
CrossRef Google scholar
[17]
Oksanen, J., Blanchet, F.G., Kindt, R., Legendre, P., Minchin, P.R., O’Hara, R.B., Simpson, G.L., Solymos, P., Stevens, M.H.H., Wagner, H., 2013. Package ‘vegan’: community ecology package. R package version 2.6-3.
[18]
Rodríguez, A., Ibáñez, M., Bol, R., Brüggemann, N., Lobo, A., Jimenez, J.J., Ruess, L., Sebastià, M.T., 2022. Fairy ring‐induced soil potassium depletion gradients reshape microbial community composition in a montane grassland. European Journal of Soil Science73, e13239.
CrossRef Google scholar
[19]
Rognes, T., Flouri, T., Nichols, B., Quince, C., Mahé, F., 2016. VSEARCH: a versatile open source tool for metagenomics. PeerJ4, e2584.
CrossRef Google scholar
[20]
Shantz, H.L., Piemeisel, R.L., 1917. Fungus fairy rings in eastern Colorado and their effect on vegetation. Journal of Agricultural Research11, 191–245.
[21]
Shen, H., Dong, S., DiTommaso, A., Xiao, J., Lu, W., Zhi, Y., 2022. Nitrogen deposition shifts grassland communities through directly increasing dominance of graminoids: a 3-year case study from the Qinghai-Tibetan Plateau. Frontiers in Plant Science13, 811970.
CrossRef Google scholar
[22]
van der Heijden, M.G.A., Bardgett, R.D., van Straalen, N.M., 2008. The unseen majority: soil microbes as drivers of plant diversity and productivity in terrestrial ecosystems. Ecology Letters11, 296–310.
CrossRef Google scholar
[23]
Wang, J., Liu, S., Han, S., Wang, A., 2022. High‐throughput sequencing reveals soil bacterial community structure and their interactions with environmental factors of the grassland fairy ring. Environmental Microbiology Reports14, 479–493.
CrossRef Google scholar
[24]
White, T.J., Bruns, T., Lee, S., Taylor, J., 1990. Amplification and Direct Sequencing of Fungal Ribosomal RNA Genes for Phylogenetics. In: Innis, M.A., Gelfand, D.H., Sninsky, J.J., White, T.J., eds. PCR protocols: a Guide to Methods and Applications. Elsevier, pp. 315–322
[25]
Xing, R., Yan, H., Gao, Q., Zhang, F., Wang, J., Chen, S., 2018. Microbial communities inhabiting the fairy ring of Floccularia luteovirens and isolation of potential mycorrhiza helper bacteria. Journal of Basic Microbiology58, 554–563.
CrossRef Google scholar
[26]
Yang, C., Li, J.J., Liu, N., Zhang, Y.J., 2019. Effects of fairy ring fungi on plants and soil in the alpine and temperate grasslands of China. Plant and Soil441, 499–510.
CrossRef Google scholar
[27]
Zhang, C.F., Tayyab, M., Abubakar, A.Y., Yang, Z.Q., Pang, Z.Q., Islam, W., Lin, Z.L., Li, S.Y., Luo, J., Fan, X.L., Fallah, N., Zhang, H., 2019. Bacteria with different assemblages in the soil profile drive the diverse nutrient cycles in the sugarcane straw retention ecosystem. Diversity (Basel)11, 194.
CrossRef Google scholar
[28]
Zhou, X., Guo, Z., Zhang, P., Li, H., Chu, C., Li, X., Du, G., 2017. Different categories of biodiversity explain productivity variation after fertilization in a Tibetan alpine meadow community. Ecology and Evolution7, 3464–3474.
CrossRef Google scholar
[29]
Zotti, M., Bonanomi, G., Mancinelli, G., Barquero, M., De Filippis, F., Giannino, F., Mazzoleni, S., González-Andrés, F., 2021. Riding the wave: Response of bacterial and fungal microbiota associated with the spread of the fairy ring fungus Calocybe gambosa. Applied Soil Ecology163, 103963.
CrossRef Google scholar
[30]
Zotti, M., De Filippis, F., Cesarano, G., Ercolini, D., Tesei, G., Allegrezza, M., Giannino, F., Mazzoleni, S., Bonanomi, G., 2020. One ring to rule them all: an ecosystem engineer fungus fosters plant and microbial diversity in a Mediterranean grassland. New Phytologist227, 884–898.
CrossRef Google scholar

Acknowledgments

This work was supported by the National Natural Science Foundation of China (31901115), Lanzhou University’s “Double First-Class” Guided Project Team Building-Funding-Research Startup Fee, China (561120221), the Fundamental Research Funds for the Central Universities (lzujbky-2022-ct01), and the Youth Science and Technology Fund program of Gansu Province (22JR5RA522).

Conflict of interest

No conflict of interest exits in the submission of this manuscript.

Electronic supplementary material

Supplementary material is available in the online version of this article at https://doi.org/10.1007/s42832-023-0214-2 and is accessible for authorized users.

RIGHTS & PERMISSIONS

2023 Higher Education Press
AI Summary AI Mindmap
PDF(4929 KB)

Accesses

Citations

Detail

Sections
Recommended

/