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Fungal and Bacterial Diversity in the Tuber magnatum Ecosystem and Microbiome

  • Environmental Microbiology
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A Correction to this article was published on 11 April 2022

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Abstract

Fungi belonging to the genus Tuber produce edible ascocarps known as truffles. Tuber magnatum Picco may be the most appreciated truffle species given its peculiar aroma. While its life cycle is not yet fully elucidated, some studies demonstrated an active role of microorganisms. The main goal of this study was to determine how the T. magnatum microbiome varies across space and time. To address this, we characterized microbial communities associated with T. magnatum through high-throughput amplicon sequencing of internal transcribed spacer (ITS) and 16S rDNAs in three productive natural sites in Italy across 2 years. At each site, four truffles were sampled as well as the soil underneath and at 40, 100, and 200 cm from the harvesting points, to assess for microbial variation between substrates, years, and sites. A statistically significant site-related effect on microbial communities was identified, whereas only the prokaryotic community was significantly affected by the distance of soil from the truffle. Significant differences between sampling years were also found, demonstrating a possible relation among rainfall precipitation and Firmicutes and Actinobacteria. Thirty-six bacterial OTUs in truffles and 11 bacterial OTUs in soils beneath truffles were identified as indicator taxa. As shown for other truffle species, the dominance of Bradyrhizobium, Rhizobium, and Ensifer spp. within the truffle fruiting body suggests an evolutionary adaptation of this microorganism to the genus Tuber. The present work offers novel and relevant insights into the microbial ecology of T. magnatum ecosystems and fruiting bodies. The function and role of these bacteria in the truffle microbiome and life cycle are in need of further investigation.

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Data Availability

Raw sequence reads have been deposited to the Sequence Read Archive [98] and the submission is linked to the bioproject number PRJNA751865 in the National Center of Biotechnology Information (https://www.ncbi.nlm.nih.gov/bioproject/).

Code Availability

R scripts developed to analyze the data are available in Supplementary File S1 and also at https://github.com/Gian77/Scientific-Papers-R-Code.

Change history

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Acknowledgements

We are thankful to the truffle hunters Matteo Galletti, Gianfranco Berni, and Giuseppe Meocci who indicated the productive sites included in this study and helped to collect the truffles with their trained dogs.

Funding

Giorgio Marozzi was supported by a PhD fellowship for the project: “Contributo alla coltivazione del tartufo bianco: approccio metagenomico per lo studio delle comunità microbiche della micorrizzosfera” Project reference: 2013.0220.021 RICERCA SCIENTIFICA E TECNOLOGIA. Gregory Bonito is grateful for support from NSF grant 1946445.

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Authors and Affiliations

  1. Department of Agricultural, Food and Environmental Sciences, University of Perugia, 06121, Perugia, Italy

    Marozzi Giorgio, Turchetti Benedetta, Baciarelli Falini Leonardo, Buzzini Pietro, Agnelli Alberto, Donnini Domizia & Albertini Emidio

  2. Department of Plant, Soil and Microbial Sciences, Michigan State University, East Lansing, MI, 48824, USA

    Benucci Gian Maria Niccolò & Bonito Gregory

  3. Department for Innovation in Biological, Agro-Food and Forest Systems, University of Tuscia, 01100, Viterbo, Italy

    Massaccesi Luisa

Authors
  1. Marozzi Giorgio
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  2. Benucci Gian Maria Niccolò
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  3. Turchetti Benedetta
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  4. Massaccesi Luisa
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  5. Baciarelli Falini Leonardo
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  6. Bonito Gregory
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  7. Buzzini Pietro
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  8. Agnelli Alberto
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  9. Donnini Domizia
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  10. Albertini Emidio
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Contributions

All authors contributed to the study conception and design. Conceptualization: Gian Maria Niccolò Benucci, Giorgio Marozzi, Domizia Donnini. Methodology: Gian Maria Niccolò Benucci, Benedetta Turchetti, Emidio Albertini, Alberto Agnelli. Data curation: Gian Maria Niccolò Benucci; Giorgio Marozzi, Domizia Donnini, Leonardo Baciarelli Falini. Formal analysis: Gian Maria Niccolò Benucci; Giorgio Marozzi; Luisa Massaccesi. Resources: Domizia Donnini, Gregory Bonito, Emidio Albertini, Alberto Agnelli. Funding acquisition: Domizia Donnini, Gregory Bonito, Emidio Albertini. Investigation: Gian Maria Niccolò Benucci; Giorgio Marozzi; Luisa Massaccesi; Benedetta Turchetti. Writing—original draft: Gian Maria Niccolò Benucci, Giorgio Marozzi; Luisa Massaccesi. Writing—review and editing: Gian Maria Niccolò Benucci, Giorgio Marozzi; Luisa Massaccesi, Pietro Buzzini, Benedetta Turchetti; Alberto Agnelli; Emidio Albertini; Domizia Donnini.

Corresponding author

Correspondence to Benucci Gian Maria Niccolò.

Supplementary Information

Below is the link to the electronic supplementary material.

248_2021_1950_MOESM1_ESM.pdf

Supplementary file1 (PDF 1339 kb) Figure S1. Geographical position and pictures of sampled sites; Umbria: Site 1, in Citta’ di Castello, Perugia province and Site 2, in Ripabianca, Perugia province. Tuscany: Site 3, San Giovanni d’Asso, Siena province.

248_2021_1950_MOESM2_ESM.pdf

Supplementary file2 (PDF 33 kb) Figure S2 - Graphical view of decontamination analysis using the R package decontam and distribution of sample libraries for fungal and prokaryotic datasets. OTUs that were detected as TRUE contaminants on the base of their prevalence were removed from the datasets.

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Supplementary file3 (PDF 41 kb) Figure S3 - Rarefaction curves highlighting differences in species richness soil and truffle samples.

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Supplementary file4 (PDF 38 kb) Figure S4 - Principal coordinates analysis plots, using Bray–Curtis dissimilarity matrices, of fungal (A- C) and prokaryotic (B – D) communities on ST (A – B) and YR (C – D) datasets from truffle samples. Each plot reports the R2 values calculated with PERMANOVA analysis and dispersion analysis (betadisper) with a p-value < 0.05.

248_2021_1950_MOESM5_ESM.pdf

Suppl ementary file5 (PDF 78 kb) Figure S5 - Differential heat trees depicting the change in taxon abundance between 2014 and 2015 in Site 1 at genus taxonomic rank. The colors illustrate the log2 ratio median proportion: brown color indicates a significantly higher (p ≤ 0.05 after "fdr" correction) proportion of a taxon in 2014, green color indicates significantly higher proportion of a taxon in 2015. Node sizes are proportional to the number of OTUs within each taxon.

248_2021_1950_MOESM6_ESM.docx

Supplementary file6 (DOCX 9 kb) Table S1. Multivariate homogeneity of groups dispersions analysis (betadisper) results for both prokaryotic and fungal communities.

Supplementary file7 (XLSX 16 kb) Table S2. Indicators taxa associated with truffle and soil samples for prokaryotes.

Supplementary file8 (XLSX 46 kb) Table S3. Indicators taxa associated with soil from different sites for fungi.

Supplementary file 9 (txt 103  kb) R code to reproduce the data analyses.

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Giorgio, M., Niccolò, B.G.M., Benedetta, T. et al. Fungal and Bacterial Diversity in the Tuber magnatum Ecosystem and Microbiome. Microb Ecol 85, 508–521 (2023). https://doi.org/10.1007/s00248-021-01950-1

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  • DOI: https://doi.org/10.1007/s00248-021-01950-1

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