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Differences in soil fungal assemblages associated with native and non-native tree species of varying weediness

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Abstract

Here we characterize and compare the diversity of belowground fungal communities of maples (Sapindaceae: Acer) varying in both nativity and weediness, and interpret our findings in the context of multiple non-exclusive theories on tree invasions and fungal associations. We made our fungal community comparisons based on high-throughput Illumina sequencing of the internal transcribed spacer region of fungal ribosomal DNA of soil samples associated with the roots of different species of maple collected from six sites throughout Central Pennsylvania. In our system, we found that weedy species, regardless of nativity, had the greatest soil fungal richness and that the nonnative invasive Norway maple had the highest abundance of mycorrhizal mutualists. Despite that much of the fungal community variability in our system was attributable to inter-site variability, we found that the core fungal communities associated with nonnative tree species were an inclusively larger set that included nearly all of those associated with native trees in addition to many not found with the natives, and the core communities of non-weedy species were largely a subset of those associated with weedy maples. In addition to confirming the strong influence that site variation has on soil fungal communities, our findings are also largely consistent with positive feedback from native fungal communities, possible co-invasion by fungal associates that are only associated with the nonnative trees, and generally add to the growing number of studies that have observed a greater abundance of mutualists associated with invasive trees that interact with arbuscular mycorrhizal fungi.

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Acknowledgements

Funding for this project was provided by GCAT-SEEK through the National Science Foundation (DBI-1248096), by Howard Hughes Medical Institute, and by Juniata College Student Research Fellowship Committee. Special thanks to Maple Brook Nursery and Fox Hill Gardens for their nursery stock to be sampled, Jeff Meadows for access to the Juniata College and Peace Chapel sampling locations, and the US Army Corps of Engineers for access to the Raystown Lake and Seven Points Marina sampling locations. Additional thanks for analytical assistance from Caleb Madder and William Bernard. Thanks to Vince Buonaccorsi for help with the experimental design.

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Authors and Affiliations

  1. Biology Department, Juniata College, Huntingdon, PA, USA

    David R. Toole, Regina Lamendella & Norris Z. Muth

  2. McKusick-Nathans Institute of Genetic Medicine, Johns Hopkins University, Baltimore, MD, USA

    Gabrielle H. Cannon

  3. Biological Sciences Division, Pacific Northwest National Laboratory, Richland, WA, USA

    Colin J. Brislawn

  4. Trout Unlimited, Lock Haven, PA, USA

    Jennifer M. Graves

  5. Biology Department, CUNY-Brooklyn College, Brooklyn, NY, USA

    Theodore R. Muth

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  1. David R. Toole
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Correspondence to Norris Z. Muth.

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Supplementary Fig. 1

Richness estimates calculated for fungal communities present in soil samples collected from the roots of maples varying in nativity and invasiveness (n = 46). Estimates were calculated from the untransformed OTU table after the data were filtered to remove samples with less than 1000 sequence counts from the analysis and rarefied down to the lowest sequencing depth across all samples. In each plot, alpha diversity values were plotted along the y-axis while the maple species were plotted along the x-axis. Richness estimates were made using the metrics for Observed OTUs (left), Chao1 (middle), and inverse of Simpson’s Diversity Index (right). Error bars were created to show standard error within a 95% confidence interval of each Chao1 estimate. Plots and estimates were generated with the Phyloseq R-package (McMurdie and Holmes 2013) along with a visual overlay produced by the ggplot2 R-package (Wickham 2009) (TIFF 250 kb)

Supplementary Fig. 2

Richness estimates calculated for fungal communities present in soil samples collected from the roots of maples varying in nativity and invasiveness (n = 46). Estimates were calculated from the untransformed OTU table after the data were filtered to remove samples with less than 1000 sequence counts from the analysis and rarefied down to the lowest sequencing depth across all samples. In each plot, alpha diversity values were plotted along the y-axis while the maple species were plotted along the x-axis. Richness estimates were made using the metric for Observed OTUs. Richness plots were facetted by sample site. Plots and estimates were generated with the Phyloseq R-package (McMurdie and Holmes 2013) along with a visual overlay produced by the ggplot2 R-package (Wickham 2009) (TIFF 285 kb)

Supplementary Fig. 3

Non-metric multidimensional scaling (NMDS) plots generated for soil samples collected from the roots of maples varying in nativity and invasiveness (n = 46). Plots were made from an OTU table normalized using metagenomeSeq’s Cumulative Sum Scaling algorithm after the data were filtered to remove samples with less than 1000 sequence counts from the analysis and trimmed to not retain singleton reads. Sample points were plotted on several axes of variation and represented in 2D space by the axes showing the most variation between samples. Samples were colored by (a) maple species and (b) site location. Plots and estimates were generated with the Phyloseq R-package (McMurdie and Holmes 2013) along with a visual overlay produced by the ggplot2 R-package (Wickham 2009) (TIFF 655 kb)

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Supplementary material 7 (DOCX 46 kb)

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Toole, D.R., Cannon, G.H., Brislawn, C.J. et al. Differences in soil fungal assemblages associated with native and non-native tree species of varying weediness. Biol Invasions 20, 891–904 (2018). https://doi.org/10.1007/s10530-017-1580-4

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