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Host availability drives distributions of fungal endophytes in the imperilled boreal realm

Abstract

Boreal forests represent the world’s largest terrestrial biome and provide ecosystem services of global importance. Highly imperilled by climate change, these forests host Earth’s greatest phylogenetic diversity of endophytes, a hyperdiverse group of symbionts that are defined by their occurrence within living, symptomless plant and lichen tissues. Endophytes shape the ecological and evolutionary trajectories of plants and are therefore key to the function and resilience of terrestrial ecosystems. A critical step in linking the ecological functions of endophytes with those of their hosts is to understand the distributions of these symbionts at the global scale; however, turnover in host taxa with geography and climate can confound insights into endophyte biogeography. As a result, global drivers of endophyte diversity and distributions are not known. Here, we leverage sampling from phylogenetically diverse boreal plants and lichens across North America and Eurasia to show that host filtering in distinctive environments, rather than turnover with geographical or environmental distance, is the main determinant of the community composition and diversity of endophytes. We reveal the distinctiveness of boreal endophytes relative to soil fungi worldwide and endophytes from diverse temperate biomes, highlighting a high degree of global endemism. Overall, the distributions of endophytes are directly linked to the availability of compatible hosts, highlighting the role of biotic interactions in shaping fungal communities across large spatial scales, and the threat that climate change poses to biological diversity and function in the imperilled boreal realm.

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Fig. 1: Geographical location, climate and host information for 498 individual host collections sampled for endophytes at seven boreal sites.
Fig. 2: Host identity structures endophyte communities at a circumboreal scale.
Fig. 3: Networks reveal host affiliations of endophyte OTUs at local and circumboreal scales.
Fig. 4: Evolutionary context of endophyte–host associations revealed by phylogenetic analyses of the most species-rich fungal phylum (Ascomycota).

Data availability

Raw sequencing data and metadata are deposited in at DDBJ/EMBL/GenBank (BioProject PRJNA514023: SRA BioSamples SAMN10718335–SAMN10718821; Sanger Targeted Locus Study project accession numbers KCRE01000001–KCRE01010802). All of the sequencing data, metadata and other types of data used in this study are publicly available at figshare69.

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Acknowledgements

We thank S. Irwin, L. Taylor, J. Stenlid, R. Andronova, A. Knorre, A. Dutbyeva, M. Zhurbenko, K. Arendt, E. Lefèvre, B. Ball, V. Wong, R. Oono, T. Gleason, J. Gonzales III, J. Riddle and K.-H. Chen for field and laboratory assistance; G. Hestmark, B. Hodkinson, S. LaGreca, J. Lendemer, B. McCune, L. Myllys, S. Stenroos and C. Truong for lichen identifications; B. Hurwitz, R. Steidl and G. Burleigh for helpful discussions; K. Youens-Clark and T. O’Connor for computational assistance; staff at the University of Arizona Genetics Core and D. New and A. Gerritsen at the University of Idaho IBEST Genomics Core for technical assistance; and M. Miller for deploying tools and databases used in T-BAS on CIPRES. This study was funded by the US National Science Foundation (NSF) Dimensions of Biodiversity program (A.E.A., DEB-1045766; I.C., DEB-1046167; G.M., DEB-1045608; F.L., DEB-1046065) and the Huron Mountain Wildlife Foundation (A.E.A.). N.B.Z. was supported by the Gordon and Betty Moore Foundation through grant number GBMF 2550.03 to the Life Sciences Research Foundation. The CIPRES RESTful API is supported by the National Institutes of Health (NIH; 5 R01 GM1264635), NSF (DBI-1759844) and an award (TG-DEB090011) of computer time and development support from the XSEDE project (also sponsored by NSF). Data collection that was performed by the IBEST Genomics Resources Core at the University of Idaho was supported in part by NIH (COBRE grant P30GM103324).

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Authors

Contributions

F.L., J.M. and A.E.A. conceived the study with I.C., G.M. and J.M.U. F.L., J.M., A.E.A., J.M.U. and G.M. conducted the fieldwork. J.M.U., J.M., F.L. and A.E.A. collected the data. J.M.U., A.E.A., N.B.Z., I.C. and F.L. developed the analyses. J.M.U., A.E.A. and N.B.Z. analysed the data. J.M.U., A.E.A. and F.L. wrote the paper with comments from all of the authors.

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Correspondence to A. Elizabeth Arnold.

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Supplementary information

Supplementary Information

Supplementary methods and Figs. 1–16.

Reporting Summary

Supplementary Table 1

Sampling sites and collection information (sampling date, latitude, longitude, elevation and climate).

Supplementary Table 2

Isolation frequency, species richness and diversity of endophytic fungi from 82 plant collections based on culturing and Illumina NGS for seven sites across the circumboreal belt.

Supplementary Table 3

Isolation frequency, putative species richness and diversity of endophytic fungi from 81 lichen collections based on culturing and Illumina NGS for seven sites across the circumboreal belt.

Supplementary Table 4

Taxonomy and lifestyle of 693 fungal OTUs from soil (of 44,563), as described by ref. 22, that have significant matches to boreal endophytes on the basis of clustering at 99% sequence similarity. Information about ectomycorrhizal lineages (ecm_lineage) and lifestyle are presented in ref. 22 and may reference either fungi with multiple ecological modes or cryptic species that perform various ecological roles. Abbreviations and column titles are from ref. 22 (panel A). Taxonomy, read counts and distribution of 153 endophyte OTUs from temperate plants and lichens as described in ref. 7 with high similarity to endophytes from the boreal biome, as represented by culturing and culture-free methods used in the present study (panel B).

Supplementary Table 5

Relationship of endophyte richness to MAP, host lineage and site. Comparison of −2 log likelihood values between linear mixed models revealed the most likely model is the one containing only host lineage (nested within site; P < 0.0001). Richness was defined for the analysis by calculating the residuals of OTU richness in relation to the square-root of the number of reads22. Results were similar to richness calculated from rarefied data (data not shown).

Supplementary Table 6

Results of PERMANOVA examining the relationship of endophyte community composition to host identity and site. For each taxon set we tested different combinations of the following variables (as appropriate): host genus and host lineage; host genus × site; and host lineage × site. Results from each analysis are presented on a separate row. Host lineage is defined at the phylum level for plants and mycobiont family level for lichens.

Supplementary Table 7

Species area relationships (SAR) for fungal endophytes at continental to circumboreal scales.

Supplementary Table 8

Accession numbers, site, host and collection information for endophyte cultures from this study. Endophytes were archived as living cultures at the Robert L. Gilbertson Mycological Herbarium at the University of Arizona.

Supplementary Table 9

Fungi included in the mock community, taxonomy and number of reads per replicate.

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U’Ren, J.M., Lutzoni, F., Miadlikowska, J. et al. Host availability drives distributions of fungal endophytes in the imperilled boreal realm. Nat Ecol Evol 3, 1430–1437 (2019). https://doi.org/10.1038/s41559-019-0975-2

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