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Above- and belowground fungal biodiversity of Populus trees on a continental scale

Nature Microbiology volume 8, pages 2406–2419 (2023)Cite this article

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Abstract

Understanding drivers of terrestrial fungal communities over large scales is an important challenge for predicting the fate of ecosystems under climate change and providing critical ecological context for bioengineering plant–microbe interactions in model systems. We conducted an extensive molecular and microscopy field study across the contiguous United States measuring natural variation in the Populus fungal microbiome among tree species, plant niche compartments and key symbionts. Our results show clear biodiversity hotspots and regional endemism of Populus-associated fungal communities explained by a combination of climate, soil and geographic factors. Modelling climate change impacts showed a deterioration of Populus mycorrhizal associations and an increase in potentially pathogenic foliar endophyte diversity and prevalence. Geographic differences among these symbiont groups in their sensitivity to environmental change are likely to influence broader forest health and ecosystem function. This dataset provides an above- and belowground atlas of Populus fungal biodiversity at a continental scale.

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Fig. 1: Tree species and sampling locations.
Fig. 2: Fungal taxonomic distributions among sampling compartments and host tree species.
Fig. 3: Patterns of fungal diversity and community structure, and the relationships to climate and soil and gradients.
Fig. 4: Ectomycorrhizal fungal diversity, distribution and climate response.
Fig. 5: Arbuscular mycorrhizal fungal diversity, distribution and climate response.
Fig. 6: PPFE diversity, distribution and climate response.

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Data availability

All ITS amplicons are archived on the National Center for Biotechnology Information Sequence Read Archive database (BioProject number PRJNA987748) and will be submitted to the GlobalFungi database following publication. The fungal OTU table, ASV table and metadata are archived on Zenodo (https://doi.org/10.5281/zenodo.8062691). The FungalTraits database used for guild assignments is available at https://docs.google.com/spreadsheets/d/1cxImJWMYVTr6uIQXcTLwK1YNNzQvKJJifzzNpKCM6O0/edit?usp=sharing.

Code availability

The bioinformatic code used to process amplicon data is archived on Zenodo (https://doi.org/10.5281/zenodo.8062691).

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Acknowledgements

We thank members of the Peay Lab for their help processing samples and advising on the preparation of sequencing libraries. This research was funded in part by the US Department of Energy Biological and Environmental Research program award DESC0016097 to K.G.P. This work was also supported by CAREER awards to P.E.B. (NSF 2146552, USDA 2022-67013-37437). K.G.P. is a Canadian Institute For Advanced Research Fellow in the program Fungal Kingdom: Threats and Opportunities.

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Author notes

  1. These authors contributed equally: Michael E. Van Nuland, S. Caroline Daws.

Authors and Affiliations

  1. Department of Biology, Stanford University, Stanford, CA, USA

    Michael E. Van Nuland, S. Caroline Daws & Kabir G. Peay

  2. Society for the Protection of Underground Networks, SPUN, Dover, DE, USA

    Michael E. Van Nuland

  3. Ecology and Evolutionary Biology Department, University of Tennessee, Knoxville, TN, USA

    Joseph K. Bailey & Jennifer A. Schweitzer

  4. Department of Botany and Plant Pathology, Oregon State University, Corvallis, OR, USA

    Posy E. Busby

  5. Department of Earth System Science, Stanford University, Stanford, CA, USA

    Kabir G. Peay

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  1. Michael E. Van Nuland
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Contributions

M.E.V.N., S.C.D. and K.G.P. designed the study, with assistance from P.E.B., J.K.B. and J.A.S. on site selection and sampling protocols. M.E.V.N., S.C.D. and K.G.P. performed the field sampling, lab work and fungal amplicon library preparation. M.E.V.N. and S.C.D. performed the bioinformatics and data analysis and wrote the first draft of the manuscript. All co-authors contributed substantial edits to the manuscript.

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Correspondence to Michael E. Van Nuland.

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Nature Microbiology thanks Ari Jumpponen, Brajesh Singh and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

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Extended data

Extended Data Fig. 1 Fungal taxonomic diversity among sampling compartments and host tree species.

Krona charts show the overall fungal taxonomic profile of each plant compartment. Higher taxonomic ranks are located at inner circles moving to family level ranks in outer circles. Expandable versions of these plots for more in-depth examination can be found here: https://mvannuland.github.io/Populus_mycobiome_taxonomy_krona/.

Extended Data Fig. 2 Predicted spatial variation of fungal richness and community turnover across the combined US Populus distribution.

a) Maps show predicted levels of fungal OTU richness based on generalized additive model results projected across a rasterstack of climate and soil variables. b) Maps show predicted gradients of fungal community composition derived by principle component (PC) transformations of climate and soil rasters. The three constituent subplots (representing the first three PC axes) are shown based on their red, green, and blue color scale. Areas with similar colors are expected to have similar fungal communities.

Extended Data Fig. 3 Uncertainty in model projections of fungal responses to climate change.

Maps show per-pixel uncertainty associated with spatial predictions of percent changes in a) ectomycorrhizal fungi (EMF), b) arbuscular mycorrhizal fungi (AMF), and c) foliar pathogen responses to climate change. Uncertainty estimates were calculated as the standard deviation across 17 future climate datasets (2070 RCP8.5) used in spatial predictions based on generalized additive models.

Extended Data Fig. 4 Community-level results of accumulated indicator OTU taxa z-scores.

Cumulative change-point values and distributions of fungal indicator OTUs in each functional guild with negative and positive responses to the environmental gradients. The left axis shows the sum of z-scores from individual indicator OTU taxa plotted as points connected by lines. The right axis shows the cumulative distribution of change points. Peaks in sum(z) points and steep increases in cumulative frequency identify thresholds of fungal community change along environmental gradients. EMF = ectomycorrhizal fungi, AMF = arbuscular mycorrhizal fungi, Pathogen = foliar plant pathogens.

Extended Data Fig. 5 Correlations between measured and predicted (SoilGrids) data.

Correlations show positive relationships between soil organic carbon and organic matter, soil nitrogen, and soil pH.

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Van Nuland, M.E., Daws, S.C., Bailey, J.K. et al. Above- and belowground fungal biodiversity of Populus trees on a continental scale. Nat Microbiol 8, 2406–2419 (2023). https://doi.org/10.1038/s41564-023-01514-8

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