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Truffle species strongly shape their surrounding soil mycobiota in a Pinus armandii forest

Abstract

Truffles contribute to crucial soil systems dynamics, being involved in plentiful ecological functions important for ecosystems. Despite this, the interactions between truffles and their surrounding mycobiome remain unknown. Here, we investigate soil mycobiome differences between two truffle species, Tuber indicum (Ti) and Tuber pseudohimalayense (Tp), and their relative influence on surrounding soil mycobiota. Using traditional chemical analysis and ITS Illumina sequencing, we compared soil nutrients and the mycobiota, respectively, in soil, gleba, and peridium of the two truffle species inhabiting the same Pinus armandii forest in southwestern China. Tp soil was more acidic (pH 6.42) and had a higher nutrient content (total C, N content) than Ti soil (pH 6.62). Fungal richness and diversity of fruiting bodies (ascomata) and surrounding soils were significantly higher in Tp than in Ti. Truffle species recruited unique soil mycobiota around their ascomata: in Ti soil, fungal taxa, including Suillus, Alternaria, Phacidium, Mycosphaerella, Halokirschsteiniothelia, and Pseudogymnoascus, were abundant, while in Tp soil species of Melanophyllum, Inocybe, Rhizopogon, Rhacidium, and Lecanicillium showed higher abundances. Three dissimilarity tests, including adonis, anosim, and MRPP, showed that differences in fungal community structure between the two truffle species and their surrounding soils were stronger in Tp than in Ti, and these differences extended to truffle tissues (peridium and gleba). Redundancy analysis (RDA) further demonstrated that correlations between soil fungal taxa and soil properties changed from negative (Tp) to positive (Ti) and shifted from a moisture-driven (Tp) to a total N-driven (Ti) relationship. Overall, our results shed light on the influence that truffles have on their surrounding soil mycobiome. However, further studies are required on a broader range of truffle species in different soil conditions in order to determine causal relationships between truffles and their soil mycobiome.

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Availability of data and materials

Raw sequence data were deposited in the NCBI under the accession number PRJNA649675.

Abbreviations

ANOVA:

Analysis of variance

PCR:

Polymerase chain reaction

QIIME:

Quantitative insights into microbial ecology

OTU:

Operational taxonomic unit

rRNA:

Ribosomal RNA

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Acknowledgements

The authors are grateful to Shanping Wan comments for the first draft. They thank technicians in the elemental content analysis center, and Mr. Zhonghua Li for technical assistance in laboratory and data analyses.

Funding

This research was funded by the CAS "Light of West China" Program (Y923217), Basic Research—General Program of Yunnan Province, China (E13A44), Science and Technology Service Network Initiative, Chinese Academy of Sciences (2017), and Guizhou Science and Technology Program (4002, 2018).

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DL developed the concept. JPM and FQY designed all the experiments. DL and MH performed the lab experiments. DL performed the statistical analyses, constructed the figures, and interpreted data. DL, JPM, and XH wrote the manuscript. MH and XH critically reviewed the manuscript. All the authors discussed the results, critically reviewed the manuscript, and approved its publication.

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Correspondence to Dong Liu or Fuqiang Yu.

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Liu, D., Herrera, M., Zhang, P. et al. Truffle species strongly shape their surrounding soil mycobiota in a Pinus armandii forest. Arch Microbiol 203, 6303–6314 (2021). https://doi.org/10.1007/s00203-021-02598-8

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Keywords

  • Hypogeous ectomycorrhizal fungi
  • Truffles
  • Soil nutrient
  • Fungal community
  • Mycobiota