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Fungal Endophyte Communities Reflect Environmental Structuring Across a Hawaiian Landscape

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Fungal Endophyte Communities Reflect Environmental Structuring Across a Hawaiian Landscape Fungal endophyte communities reflect environmental structuring across a Hawaiian landscape Naupaka B. Zimmerman1 and Peter M. Vitousek1 Department of Biology, Stanford University, Stanford, CA 94305 Contributed by Peter M. Vitousek, June 12, 2012 (sent for review August 20, 2011) We surveyed endophytic fungal communities in leaves of a single (6, 13), the phyllosphere remains one of the least-studied envi- tree species (Metrosideros polymorpha) across wide environmental ronments of the Earth. Within this environment, some of the gradients (500–5,500 mm of rain/y; 10–22 °C mean annual temper- most diverse and potentially influential members of the biotic ature) spanning short geographic distances on Mauna Loa Volcano, community are the fungal endophytes (FEs) (7, 8, 14–16). FEs Hawai’i. Using barcoded amplicon pyrosequencing at 13 sites (10 inhabit the asymptomatic aboveground tissues of their hosts (9, trees/site; 10 leaves/tree), we found very high levels of diversity 17–19) and are found in all species and in all divisions of land within sites (a mean of 551 ± 134 taxonomic units per site). How- plants (20). These organisms have been the subjects of significant ever, among-site diversity contributed even more than did within- research for several decades (e.g., refs. 21–23). In comparison site diversity to the overall richness of more than 4,200 taxonomic with FEs in agricultural grasses, research on endophytes in units observed in M. polymorpha, and this among-site variation in woody plants has been relatively sparse (14), attributable, in part, endophyte community composition correlated strongly with tem- to much higher fungal species heterogeneity within and among perature and rainfall. These results are consistent with suggestions hosts (24–26). Foliar endophytes of woody plants appear to be that foliar endophytic fungi are hyperdiverse. They further suggest highly diverse (13, 27), particularly in the tropics (8, 19), and this that microbial diversity may be even greater than has been assumed diversity has inspired recent studies by mycologists, ecologists, and that broad-scale environmental controls such as temperature and natural products researchers (e.g., refs. 28–30). and rainfall can structure eukaryotic microbial diversity. Appropri- In this study, we sought to acquire basic information on the ately constrained study systems across strong environmental gra- diversity of FEs within individual trees, within sites, between ad- ECOLOGY dients present a useful means to understand the environmental jacent sites that differ in nutrient availability, and across a land- factors that structure the diversity of microbial communities. scape encompassing wide environmental gradients over small geographic distances in a tropical system. In addition, we asked: Mauna Loa matrix | microbial biogeography | beta diversity i) How does variation in endophyte diversity among sites reflect he rapid advance of sequencing technologies has facilitated environmental characteristics? The diversity of most plant Tresearch describing the extent of microbial richness in hundreds and animal communities is much greater in tropical than of environments around the world. Work using culture-independent, temperate environments and greater in lowland rainforests high-throughput sequencing methods has found very high levels of than other tropical environments. When sampling is con- diversity, much of it resulting from unknown species, many of strained to a single host species, do individuals in lowland which are rare (1, 2). Despite these new tools and a growing ap- wet rainforests support the highest diversity of FEs? ii preciation for the diversity of the microbial world, it has proved ) Does the composition of the FE community vary among sites? challenging to understand spatial patterns in microbial diversity Less diverse communities could be subsets of more diverse and their controls (3–5). It is clear that microbial communities can communities (as is often observed when comparing the com- vary at different scales than do plant and animal communities (5) munities of different-sized islands) or each community could support a different group of species. If the latter is observed, and that substantial changes in soil communities can occur over β very short distances (6). Questions that remain include: How does how much does variation among sites (or -diversity) contrib- ute to the overall species richness in the landscape? the number of microbial species within a community differ from iii site to site, and to what extent does environmental variation ) Most importantly, to what extent is spatial variation in the contribute to these differences? What proportion of the diversity composition of FE communities associated with environmen- of a region is associated with differences in community composi- tal variation? A substantial degree of environmental control over these microbial communities (all resident in leaves of tion among sites (as opposed to species richness within sites), and a single tree species) would indicate that coarse-scale envi- how does environmental variation contribute to regional diversity? ronmental variation could play a substantial role in structur- The phyllosphere (the leaf surface and particularly its interior) ing microbial communities regionally and globally. represents a useful and tractable context for examining relation- ships between microbes and their environment (7, 8), and several To answer these questions, we used culture-independent, factors enhance its utility for understanding microbial bio- high-throughput barcoded amplicon pyrosequencing to quantify geography in particular. First, the phyllosphere carries out the patterns of variation in FE communities within a single host majority of terrestrial carbon fixation and, thus, represents one of tree species (Metrosideros polymorpha) across an extraordinarily the strongest biotic links between the biosphere and the atmo- sphere (9). Second, the phyllosphere provides habitat for complex assemblages of microorganisms (10–12). Third, leaves represent Author contributions: N.B.Z. and P.M.V. designed research; N.B.Z. performed research; largely discrete, relatively uniform, bounded habitats to the N.B.Z. analyzed data; and N.B.Z. and P.M.V. wrote the paper. microbes that inhabit them. Finally, leaves allow for a high level of The authors declare no conflict of interest. structure to sampling: within and between leaves of the same tree, Data deposition: The sequence reported in this paper has been deposited in the Sequence as well as within and between individual trees of the same species Read Archive database, www.ncbi.nlm.nih.gov/sra (accession no. SRX153137). across a landscape. This nested replication is particularly helpful 1To whom correspondence may be addressed. E-mail: [email protected] or vitousek@ when seeking to understand complex microbial communities. stanford.edu. Despite these experimental incentives, and the fact that its This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. surface area is approximately twice as great as the land surface 1073/pnas.1209872109/-/DCSupplemental. www.pnas.org/cgi/doi/10.1073/pnas.1209872109 PNAS Early Edition | 1of6 broad range of environments (ranging in elevation from 100 to Species Richness Within Sites. Mean OTU richness was similar at 2,400 m and in rainfall from <500 to >5,500 mm/y) on the Island most sites and locations, with a mean of 105 ± 42 OTUs per tree of Hawai’i. At seven locations, we collected samples from paired (68 ± 30 nonsingletons), except for the wet low elevation (100 m) early-successional (ca. 150 y-old) and later-successional (ca. sites, where we observed significantly greater richness of ca. 160 – fi 3,500 y-old) sites, which enabled us to examine independently OTUs per tree [Tables S2 S5; Tukey honestly signi cant dif- P < the effects of rainfall, elevation, and substrate age on endophyte ference (HSD): 0.05]. communities. Variation in Fungal Endophyte Communities Among Sites. We found Results substantial among-site and among-location variation in FE com- munities. Fungal communities of trees in a given location were Diversity of Fungal Endophytes. During the fall of 2009, we sampled significantly different from those in other locations [analysis of the endophytic fungal communities of trees spanning 13 sites on R P < ’ similarities (ANOSIM): = 0.66; 0.001]. The inverse of Mauna Loa Volcano, Hawai i (Fig. 1). Ten leaves were pooled ’ n Whittaker s multiplicative measure (32, 33) of among-site varia- from each of these trees ( = 130 pooled samples; 10 trees/site). tion or β-diversity, in which mean within-site diversity (α-diversity) Genomic (g)DNA was extracted from surface-sterilized leaves and γ fi fi is divided by overall regional diversity ( -diversity), provides an ampli ed with fungal-speci c primers for the nuclear ribosomal index of among-site diversity that ranges from 0 to 1. Results close (nr)DNA internal transcribed spacer region 1 (ITS1) region and to 1 indicate most diversity is within sites; results close to 0 indicate Methods sequenced with barcoded titanium pyrosequencing (see ). the importance of among-site diversity. With the most conserva- After quality control and trimming, we had 665,155 high-quality tive assumptions (that within-location diversity is the Chao esti- x sequences that were used for all primary analyses ( tree = 5,117 mated value at the most speciose location, and that total richness σ sequences; tree= 1,574; mean trimmed ITS1 length:
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