I completed a master’s degree at the Yale School of Forestry and Environment Science (F&ES) in 2003 and obtained my PhD in 2008 from UC Berkeley’s Dept. of Environmental Science, Policy and Management (ESPM) in Matteo Garbelotto's lab. I did my postdoctoral training at UC Berkeley in the Dept. of Plant & Microbial Biology with Tom Bruns, and at Stanford in the Dept. of Biology with Tadashi Fukami. I was an Assistant Professor in the Dept. of Plant Pathology at the University of Minnesota from 2011-2012 before coming to Stanford in 2012 to join the Dept. of Biology in my current position.
PhD, UC Berkeley (2008)
MESc, Yale School of Forestry (2003)
Current Research and Scholarly Interests
Our lab studies the ecological processes that structure natural communities and the links between community structure and the cycling of nutrients and energy through ecosystems. We focus primarily on fungi, as these organisms are incredibly diverse and are the primary agents of carbon and nutrient cycling in terrestrial ecosystems.
Much of our research focuses on plant-fungal root associations, better known as mycorrhizas, which constitute one of the most pervasive mutualisms in terrestrial ecosystems. We work on questions at three scales of this symbiosis, (1) how does environmental variation and functional variation in mycorrhizal fungi affect the symbiosis at the root tip scale, (2) how does dispersal contribute to the predictability of community assembly patterns at the landscape scale, and (3) how does biogeography affect mycorrhizal community structure and ecosystem function? By integrating these three levels of research we hope to build a 'roots-to-biomes' understanding of plant-microbe symbiosis.
- Introduction to Ecology
BIO 81 (Aut)
- The Hidden Kingdom - Evolution, Ecology and Diversity of Fungi
BIO 115, BIO 239 (Win)
Independent Studies (6)
- Advanced Research Laboratory in Experimental Biology
BIO 199 (Aut, Win, Spr)
- Directed Reading in Environment and Resources
ENVRES 398 (Aut, Win, Spr, Sum)
- Directed Research
EARTHSYS 250 (Win)
- Directed Research in Environment and Resources
ENVRES 399 (Aut, Win, Spr, Sum)
- Graduate Research
BIO 300 (Aut, Win, Spr, Sum)
- Honors Program in Earth Systems
EARTHSYS 199 (Aut, Win, Spr)
- Advanced Research Laboratory in Experimental Biology
Prior Year Courses
BIO 101 (Aut)
BIO 101 (Aut)
- The hidden kingdom - evolution, ecology and diversity of fungi
BIO 115 (Win)
BIO 101 (Aut)
- The hidden kingdom - evolution, ecology and diversity of fungi
BIO 115 (Win)
Doctoral Dissertation Reader (AC)
Po-Ju Ke, Beth Morrison, Jeffrey Smith
Postdoctoral Faculty Sponsor
Brian Steidinger, Michael Van Nuland
Doctoral Dissertation Advisor (AC)
Laura Bogar, Glade Dlott
Doctoral Dissertation Co-Advisor (AC)
Master's Program Advisor
Ali Hoffer, Nicholas Romano
Laura Bogar, Glade Dlott
Graduate and Fellowship Programs
Biology (School of Humanities and Sciences) (Phd Program)
Convergence and contrast in the community structure of Bacteria, Fungi and Archaea along a tropical elevation-climate gradient.
FEMS microbiology ecology
2017; 93 (5)
Changes in species richness along climatological gradients have been instrumental in developing theories about the general drivers of biodiversity. Previous studies on microbial communities along climate gradients on mountainsides have revealed positive, negative and neutral richness trends. We examined changes in richness and composition of Fungi, Bacteria and Archaea in soil along a 50-1000 m elevation, 280-3280 mm/yr precipitation gradient in Hawai'i. Soil properties and their drivers are exceptionally well understood along this gradient. All three microbial groups responded strongly to the gradient, with community ordinations being similar along axes of environmental conditions (pH, rainfall) and resource availability (nitrogen, phosphorus). However, the form of the richness-climate relationship varied between Fungi (positive linear), Bacteria (unimodal) and Archaea (negative linear). These differences were related to resource-ecology and limiting conditions for each group, with fungal richness increasing most strongly with soil carbon, ammonia-oxidizing Archaea increasing with nitrogen mineralization rate, and Bacteria increasing with both carbon and pH. Reponses to the gradient became increasingly variable at finer taxonomic scales and within any taxonomic group most individual OTUs occurred in narrow climate-elevation ranges. These results show that microbial responses to climate gradients are heterogeneous due to complexity of underlying environmental changes and the diverse ecologies of microbial taxa.
View details for DOI 10.1093/femsec/fix045
View details for PubMedID 28402397
- Continental-level population differentiation and environmental adaptation in the mushroom Suillus brevipes MOLECULAR ECOLOGY 2017; 26 (7): 2063-2076
Controls of nitrogen cycling evaluated along a well-characterized climate gradient.
The supply of nitrogen (N) constrains primary productivity in many ecosystems, raising the question "what controls the availability and cycling of N"? As a step toward answering this question, we evaluated N cycling processes and aspects of their regulation on a climate gradient on Kohala Volcano, Hawaii, USA. The gradient extends from sites receiving <300 mm/yr of rain to those receiving >3,000 mm/yr, and the pedology and dynamics of rock-derived nutrients in soils on the gradient are well understood. In particular, there is a soil process domain at intermediate rainfall within which ongoing weathering and biological uplift have enriched total and available pools of rock-derived nutrients substantially; sites at higher rainfall than this domain are acid and infertile as a consequence of depletion of rock-derived nutrients, while sites at lower rainfall are unproductive and subject to wind erosion. We found elevated rates of potential net N mineralization in the domain where rock-derived nutrients are enriched. Higher-rainfall sites have low rates of potential net N mineralization and high rates of microbial N immobilization, despite relatively high rates of gross N mineralization. Lower-rainfall sites have moderately low potential net N mineralization, relatively low rates of gross N mineralization, and rates of microbial N immobilization sufficient to sequester almost all the mineral N produced. Bulk soil δ(15) N also varied along the gradient, from +4‰ at high rainfall sites to +14‰ at low rainfall sites, indicating differences in the sources and dynamics of soil N. Our analysis shows that there is a strong association between N cycling and soil process domains that are defined using soil characteristics independent of N along this gradient, and that short-term controls of N cycling can be understood in terms of the supply of and demand for N.
View details for DOI 10.1002/ecy.1751
View details for PubMedID 28130777
Survey of corticioid fungi in North American pinaceous forests reveals hyperdiversity, underpopulated sequence databases, and species that are potentially ectomycorrhizal
2017; 109 (1): 115-127
The corticioid fungi are commonly encountered, highly diverse, ecologically important, and understudied. We collected specimens in 60 pine and spruce forests across North America to survey corticioid fungal frequency and distribution and to compile an internal transcribed spacer (ITS) database for the group. Sanger sequences from the ITS region of vouchered specimens were compared with sequences on GenBank and UNITE, and with high-throughput sequence data from soil and roots taken at the same sites. Out of 425 high-quality Sanger sequences from vouchered specimens, we recovered 223 distinct operational taxonomic units (OTUs), the majority of which could not be assigned to species by matching to the BLAST database. Corticioid fungi were found to be hyperdiverse, as supported by the observations that nearly two-thirds of our OTUs were represented by single collections and species estimator curves showed steep slopes with no plateaus. We estimate that 14.8-24.7% of our voucher-based OTUs are likely to be ectomycorrhizal (EM). Corticioid fungi recovered from the soil formed a different community assemblage, with EM taxa accounting for 40.5-58.6% of OTUs. We compared basidioma sequences with EM root tips from our data, GenBank, or UNITE, and with this approach, we reiterate existing speculations that Trechispora stellulata is EM. We found that corticioid fungi have a significant distance-decay pattern, adding to the literature supporting fungi as having geographically structured communities. This study provides a first view of the diversity of this important group across North American pine forests, but much of the biology and taxonomy of these diverse, important, and widespread fungi remains unknown.
View details for DOI 10.1080/00275514.2017.1281677
View details for Web of Science ID 000400536200011
View details for PubMedID 28402791
Continental-level population differentiation and environmental adaptation in the mushroom Suillus brevipes.
Recent advancements in sequencing technology allowed researchers to better address the patterns and mechanisms involved in microbial environmental adaptation at large spatial scales. Here we investigated the genomic basis of adaptation to climate at the continental scale in Suillus brevipes, an ectomycorrhizal fungus symbiotically associated with the roots of pine trees. We used genomic data from 55 individuals in seven locations across North America to perform genome scans to detect signatures of positive selection and assess whether temperature and precipitation were associated with genetic differentiation. We found that S. brevipes exhibited overall strong population differentiation, with potential admixture in Canadian populations. This species also displayed genomic signatures of positive selection as well as genomic sites significantly associated with distinct climatic regimes and abiotic environmental parameters. These genomic regions included genes involved in transmembrane transport of substances and helicase activity potentially involved in cold stress response. Our study sheds light on large-scale environmental adaptation in fungi by identifying putative adaptive genes and providing a framework to further investigate the genetic basis of fungal adaptation.
View details for DOI 10.1111/mec.13892
View details for PubMedID 27761941
Dimensions of biodiversity in the Earth mycobiome
NATURE REVIEWS MICROBIOLOGY
2016; 14 (7): 434-447
Fungi represent a large proportion of the genetic diversity on Earth and fungal activity influences the structure of plant and animal communities, as well as rates of ecosystem processes. Large-scale DNA-sequencing datasets are beginning to reveal the dimensions of fungal biodiversity, which seem to be fundamentally different to bacteria, plants and animals. In this Review, we describe the patterns of fungal biodiversity that have been revealed by molecular-based studies. Furthermore, we consider the evidence that supports the roles of different candidate drivers of fungal diversity at a range of spatial scales, as well as the role of dispersal limitation in maintaining regional endemism and influencing local community assembly. Finally, we discuss the ecological mechanisms that are likely to be responsible for the high heterogeneity that is observed in fungal communities at local scales.
View details for DOI 10.1038/nrmicro.2016.59
View details for Web of Science ID 000378073200009
View details for PubMedID 27296482
- Common foliar fungi of Populus trichocarpa modify Melampsora rust disease severity NEW PHYTOLOGIST 2016; 209 (4): 1681-1692
Soil moisture and chemistry influence diversity of ectomycorrhizal fungal communities associating with willow along an hydrologic gradient.
FEMS microbiology ecology
2016; 92 (1)
Influences of soil environment and willow host species on ectomycorrhizal fungi communities was studied across an hydrologic gradient in temperate North America. Soil moisture, organic matter and pH strongly predicted changes in fungal community composition. In contrast, increased fungal richness strongly correlated with higher plant-available phosphorus. The 93 willow trees sampled for ectomycorrhizal fungi included seven willow species. Host identity did not influence fungal richness or community composition, nor was there strong evidence of willow host preference for fungal species. Network analysis suggests that these mutualist interaction networks are not significantly nested or modular. Across a strong environmental gradient, fungal abiotic niche determined the fungal species available to associate with host plants within a habitat.
View details for DOI 10.1093/femsec/fiv148
View details for PubMedID 26622067
- The Mutualistic Niche: Mycorrhizal Symbiosis and Community Dynamics ANNUAL REVIEW OF ECOLOGY, EVOLUTION, AND SYSTEMATICS, VOL 47 2016; 47: 143-164
Competition-function tradeoffs in ectomycorrhizal fungi.
Background. The extent to which ectomycorrhizal fungi mediate primary production, carbon storage, and nutrient remineralization in terrestrial ecosystems depends upon fungal community composition. However, the factors that govern community composition at the root system scale are not well understood. Here, we explore a potential tradeoff between ectomycorrhizal fungal competitive ability and enzymatic function. Methods. We grew Pinus muricata (Bishop Pine) seedlings in association with ectomycorrhizal fungi from three different genera in a fully factorial experimental design. We measured seedling growth responses, ectomycorrhizal abundance, and the root tip activity of five different extracellular enzymes involved in the mobilization of carbon and phosphorus. Results. We found an inverse relationship between competitiveness, quantified based on relative colonization levels, and enzymatic activity. Specifically, Thelephora terrestris, the dominant fungus, had the lowest enzyme activity levels, while Suillus pungens, the least dominant fungus, had the highest. Discussion. Our results identify a tradeoff between competition and function in ectomycorrhizal fungi, perhaps mediated by the competing energetic demands associated with competitive interactions and enzymatic production. These data suggest that mechanisms such as active partner maintenance by host trees may be important to maintaining "high-quality" ectomycorrhizal fungal partners in natural systems.
View details for DOI 10.7717/peerj.2270
View details for PubMedID 27547573
View details for PubMedCentralID PMC4974999
- Functional guild classification predicts the enzymatic role of fungi in litter and soil biogeochemistry SOIL BIOLOGY & BIOCHEMISTRY 2015; 88: 441-456
Lack of host specificity leads to independent assortment of dipterocarps and ectomycorrhizal fungi across a soil fertility gradient
2015; 18 (8): 807-816
Plants interact with a diversity of microorganisms, and there is often concordance in their community structures. Because most community-level studies are observational, it is unclear if such concordance arises because of host specificity, in which microorganisms or plants limit each other's occurrence. Using a reciprocal transplant experiment, we tested the hypothesis that host specificity between trees and ectomycorrhizal fungi determines patterns of tree and fungal soil specialisation. Seedlings of 13 dipterocarp species with contrasting soil specialisations were seeded into plots crossing soil type and canopy openness. Ectomycorrhizal colonists were identified by DNA sequencing. After 2.5 years, we found no evidence of host specificity. Rather, soil environment was the primary determinant of ectomycorrhizal diversity and composition on seedlings. Despite their close symbiosis, our results show that ectomycorrhizal fungi and tree communities in this Bornean rain forest assemble independently of host-specific interactions, raising questions about how mutualism shapes the realised niche.
View details for DOI 10.1111/ele.12459
View details for Web of Science ID 000357958900008
View details for PubMedID 26032408
Genetic isolation between two recently diverged populations of a symbiotic fungus
2015; 24 (11): 2747-2758
Fungi are an omnipresent and highly diverse group of organisms, making up a significant part of eukaryotic diversity. Little is currently known about the drivers of fungal population differentiation and subsequent divergence of species, particularly in symbiotic, mycorrhizal fungi. Here, we investigate the population structure and environmental adaptation in Suillus brevipes (Peck) Kuntze, a wind-dispersed soil fungus that is symbiotic with pine trees. We assembled and annotated the reference genome for Su. brevipes and resequenced the whole genomes of 28 individuals from coastal and montane sites in California. We detected two clearly delineated coast and mountain populations with very low divergence. Genomic divergence was restricted to few regions, including a region of extreme divergence containing a gene encoding for a membrane Na(+) /H(+) exchanger known for enhancing salt tolerance in plants and yeast. Our results are consistent with a very recent split between the montane and coastal Su. brevipes populations, with few small genomic regions under positive selection and a pattern of dispersal and/or establishment limitation. Furthermore, we identify a putatively adaptive gene that motivates further functional analyses to link genotypes and phenotypes and shed light on the genetic basis of adaptive traits.
View details for DOI 10.1111/mec.13132
View details for Web of Science ID 000355228800013
View details for PubMedID 25728665
A continental view of pine-associated ectomycorrhizal fungal spore banks: a quiescent functional guild with a strong biogeographic pattern
2015; 205 (4): 1619-1631
Ecologists have long acknowledged the importance of seed banks; yet, despite the fact that many plants rely on mycorrhizal fungi for survival and growth, the structure of ectomycorrhizal (ECM) fungal spore banks remains poorly understood. The primary goal of this study was to assess the geographic structure in pine-associated ECM fungal spore banks across the North American continent. Soils were collected from 19 plots in forests across North America. Fresh soils were pyrosequenced for fungal internal transcribed spacer (ITS) amplicons. Adjacent soil cores were dried and bioassayed with pine seedlings, and colonized roots were pyrosequenced to detect resistant propagules of ECM fungi. The results showed that ECM spore banks correlated strongly with biogeographic location, but not with the identity of congeneric plant hosts. Minimal community overlap was found between resident ECM fungi vs those in spore banks, and spore bank assemblages were relatively simple and dominated by Rhizopogon, Wilcoxina, Cenococcum, Thelephora, Tuber, Laccaria and Suillus. Similar to plant seed banks, ECM fungal spore banks are, in general, depauperate, and represent a small and rare subset of the mature forest soil fungal community. Yet, they may be extremely important in fungal colonization after large-scale disturbances such as clear cuts and forest fires.
View details for DOI 10.1111/nph.13240
View details for Web of Science ID 000349386300031
View details for PubMedID 25557275
- Parsing ecological signal from noise in next generation amplicon sequencing NEW PHYTOLOGIST 2015; 205 (4): 1389-1393
- Local-scale biogeography and spatiotemporal variability in communities of mycorrhizal fungi NEW PHYTOLOGIST 2015; 205 (4): 1454-1463
Metatranscriptomic analysis of ectomycorrhizal roots reveals genes associated with Piloderma-Pinus symbiosis: improved methodologies for assessing gene expression in situ
2014; 16 (12): 3730-3742
Ectomycorrhizal (EM) fungi form symbiotic associations with plant roots that regulate nutrient exchange between forest plants and soil. Environmental metagenomics approaches that employ next-generation sequencing show great promise for studying EM symbioses; however, metatranscriptomic studies have been constrained by the inherent difficulties associated with isolation and sequencing of RNA from mycorrhizae. Here we apply an optimized method for combined DNA/RNA extraction using field-collected EM fungal-pine root clusters, together with protocols for taxonomic identification of expressed ribosomal RNA, and inference of EM function based on plant and fungal metatranscriptomics. We used transcribed portions of ribosomal RNA genes to identify several transcriptionally dominant fungal taxa associated with loblolly pine including Amphinema, Russula and Piloderma spp. One taxon, Piloderma croceum, has a publically available genome that allowed us to identify patterns of gene content and transcript abundance. Over 1500 abundantly expressed Piloderma genes were detected from mycorrhizal roots, including genes for protein metabolism, cell signalling, electron transport, terpene synthesis and other extracellular activities. In contrast, Piloderma gene encoding an ammonia transporter showed highest transcript abundance in soil samples. Our methodology highlights the potential of metatranscriptomics to identify genes associated with symbiosis and ecosystem function using field-collected samples.
View details for DOI 10.1111/1462-2920.12619
View details for Web of Science ID 000348463100010
View details for PubMedID 25186788
Spore dispersal of basidiomycete fungi at the landscape scale is driven by stochastic and deterministic processes and generates variability in plant-fungal interactions.
2014; 204 (1): 180-191
Fungi play an important role in plant communities and ecosystem function. As a result, variation in fungal community composition can have important consequences for plant fitness. However, there are relatively few empirical data on how dispersal might affect fungal communities and the ecological processes they mediate. We established sampling stations across a large area of coastal landscape varying in their spatial proximity to each other and contrasting vegetation types. We measured dispersal of spores from a key group of fungi, the Basidomycota, across this landscape using qPCR and 454 pyrosequencing. We also measured the colonization of ectomycorrhizal fungi at each station using sterile bait seedlings. We found a high degree of spatial and temporal variability in the composition of Basidiomycota spores. This variability was in part stochastic and in part explained by spatial proximity to other vegetation types and time of year. Variation in spore community also affected colonization by ectomycorrhizal fungi and seedling growth. Our results demonstrate that fungal host and habitat specificity coupled with dispersal limitation can lead to local variation in fungal community structure and plant-fungal interactions. Understanding fungal communities also requires explicit knowledge of landscape context in addition to local environmental conditions.
View details for DOI 10.1111/nph.12906
View details for PubMedID 24975121
Endemism and functional convergence across the North American soil mycobiome
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA
2014; 111 (17): 6341-6346
Identifying the ecological processes that structure communities and the consequences for ecosystem function is a central goal of ecology. The recognition that fungi, bacteria, and viruses control key ecosystem functions has made microbial communities a major focus of this field. Because many ecological processes are apparent only at particular spatial or temporal scales, a complete understanding of the linkages between microbial community, environment, and function requires analysis across a wide range of scales. Here, we map the biological and functional geography of soil fungi from local to continental scales and show that the principal ecological processes controlling community structure and function operate at different scales. Similar to plants or animals, most soil fungi are endemic to particular bioregions, suggesting that factors operating at large spatial scales, like dispersal limitation or climate, are the first-order determinants of fungal community structure in nature. By contrast, soil extracellular enzyme activity is highly convergent across bioregions and widely differing fungal communities. Instead, soil enzyme activity is correlated with local soil environment and distribution of fungal traits within the community. The lack of structure-function relationships for soil fungal communities at continental scales indicates a high degree of functional redundancy among fungal communities in global biogeochemical cycles.
View details for DOI 10.1073/pnas.1402584111
View details for Web of Science ID 000335199000060
View details for PubMedID 24733885
View details for PubMedCentralID PMC4035912
Ectomycorrhizal fungal traits reflect environmental conditions along a coastal California edaphic gradient.
FEMS microbiology ecology
2014; 87 (3): 797-806
Multispecies mutualisms, such as the association between trees and ectomycorrhizal fungi, are often shaped by environmental context. Here, we explored the functional mechanisms underlying this environmental filtering. Using a single population of Pinus muricata (Bishop pine) growing along a strong edaphic gradient, we examined how environmental stress affected ectomycorrhizal fungi. The gradient spans c. 400000 years of soil age, and reduced nutrient availability and increased water stress dwarf trees on older sites. Fungal community composition shifted with nutrient and water availability and with the stature of the P. muricata host trees. Not only did pygmy trees host a taxonomically different fungal subset as compared to nonpygmy trees, but associated fungal communities also differed in life history strategies: trees in more stressful conditions hosted fungi with more carbon-intensive foraging strategies. Our results indicate a link between environmental controls of host nutritional status and turnover in the ectomycorrhizal fungal community. The transition to more energy-intensive strategies under nutrient stress may allow for close recycling of recalcitrant nutrient pools within the root zone and facilitate transport of nutrients and water over long distances. These results highlight the value of life history data to understanding the mechanistic underpinnings of species distributions.
View details for DOI 10.1111/1574-6941.12265
View details for PubMedID 24289145
Genetic variation within a dominant shrub structures green and brown community assemblages
2014; 95 (2): 387-398
Two rising challenges in ecology are understanding the linkages between above- and belowground components of terrestrial ecosystems and connecting genes to their ecological consequences. Here, we blend these emerging perspectives using a long-term common-garden experiment in a coastal dune ecosystem, whose dominant shrub species, Baccharis pilularis, exists as erect or prostrate architectural morphotypes. We explored variation in green (foliage-based) and brown (detritus-based) community assemblages, local ecosystem processes, and understory microclimate between the two morphs. Prostrate morphs supported more individuals, species, and different compositions of foliage arthropods, litter microarthropods, and soil bacteria than erect morphs. The magnitude of community compositional differences was maintained from crown to litter to soil. Despite showing strikingly similar responses, green and brown assemblages were associated with different underlying mechanisms. Differences in estimated shrub biomass best explained variation in the green assemblage, while understory abiotic conditions accounted for variation in the brown assemblage. Prostrate morphs produced more biomass and litter, which corresponded with their strong lateral growth in a windy environment. Compared to erect morphs, the denser canopy and thicker litter layer of prostrate morphs helped create more humid understory conditions. As a result, decomposition rates were higher under prostrate shrubs, despite prostrate litter being of poorer quality. Together, our results support the hypothesis that intraspecific genetic variation in primary producers is a key mediator of above- and belowground linkages, and that integrating the two perspectives can lead to new insights into how terrestrial communities are linked with ecosystem pools and processes.
View details for DOI 10.1890/13-0316.1
View details for Web of Science ID 000331429500013
View details for PubMedID 24669732
Sequence depth, not PCR replication, improves ecological inference from next generation DNA sequencing.
2014; 9 (2)
Recent advances in molecular approaches and DNA sequencing have greatly progressed the field of ecology and allowed for the study of complex communities in unprecedented detail. Next generation sequencing (NGS) can reveal powerful insights into the diversity, composition, and dynamics of cryptic organisms, but results may be sensitive to a number of technical factors, including molecular practices used to generate amplicons, sequencing technology, and data processing. Despite the popularity of some techniques over others, explicit tests of the relative benefits they convey in molecular ecology studies remain scarce. Here we tested the effects of PCR replication, sequencing depth, and sequencing platform on ecological inference drawn from environmental samples of soil fungi. We sequenced replicates of three soil samples taken from pine biomes in North America represented by pools of either one, two, four, eight, or sixteen PCR replicates with both 454 pyrosequencing and Illumina MiSeq. Increasing the number of pooled PCR replicates had no detectable effect on measures of α- and β-diversity. Pseudo-β-diversity - which we define as dissimilarity between re-sequenced replicates of the same sample - decreased markedly with increasing sampling depth. The total richness recovered with Illumina was significantly higher than with 454, but measures of α- and β-diversity between a larger set of fungal samples sequenced on both platforms were highly correlated. Our results suggest that molecular ecology studies will benefit more from investing in robust sequencing technologies than from replicating PCRs. This study also demonstrates the potential for continuous integration of older datasets with newer technology.
View details for DOI 10.1371/journal.pone.0090234
View details for PubMedID 24587293
Missing checkerboards? An absence of competitive signal in Alnus-associated ectomycorrhizal fungal communities.
A number of recent studies suggest that interspecific competition plays a key role in determining the structure of ectomycorrhizal (ECM) fungal communities. Despite this growing consensus, there has been limited study of ECM fungal community dynamics in abiotically stressful environments, which are often dominated by positive rather than antagonistic interactions. In this study, we examined the ECM fungal communities associated with the host genus Alnus, which live in soils high in both nitrate and acidity. The nature of ECM fungal species interactions (i.e., antagonistic, neutral, or positive) was assessed using taxon co-occurrence and DNA sequence abundance correlational analyses. ECM fungal communities were sampled from root tips or mesh in-growth bags in three monodominant A. rubra plots at a site in Oregon, USA and identified using Illumina-based amplification of the ITS1 gene region. We found a total of 175 ECM fungal taxa; 16 of which were closely related to known Alnus-associated ECM fungi. Contrary to previous studies of ECM fungal communities, taxon co-occurrence analyses on both the total and Alnus-associated ECM datasets indicated that the ECM fungal communities in this system were not structured by interspecific competition. Instead, the co-occurrence patterns were consistent with either random assembly or significant positive interactions. Pair-wise correlational analyses were also more consistent with neutral or positive interactions. Taken together, our results suggest that interspecific competition does not appear to determine the structure of all ECM fungal communities and that abiotic conditions may be important in determining the specific type of interaction occurring among ECM fungi.
View details for DOI 10.7717/peerj.686
View details for PubMedID 25548729
Towards a unified paradigm for sequence-based identification of fungi
2013; 22 (21): 5271-5277
The nuclear ribosomal internal transcribed spacer (ITS) region is the formal fungal barcode and in most cases the marker of choice for the exploration of fungal diversity in environmental samples. Two problems are particularly acute in the pursuit of satisfactory taxonomic assignment of newly generated ITS sequences: (i) the lack of an inclusive, reliable public reference data set and (ii) the lack of means to refer to fungal species, for which no Latin name is available in a standardized stable way. Here, we report on progress in these regards through further development of the UNITE database (http://unite.ut.ee) for molecular identification of fungi. All fungal species represented by at least two ITS sequences in the international nucleotide sequence databases are now given a unique, stable name of the accession number type (e.g. Hymenoscyphus pseudoalbidus|GU586904|SH133781.05FU), and their taxonomic and ecological annotations were corrected as far as possible through a distributed, third-party annotation effort. We introduce the term 'species hypothesis' (SH) for the taxa discovered in clustering on different similarity thresholds (97-99%). An automatically or manually designated sequence is chosen to represent each such SH. These reference sequences are released (http://unite.ut.ee/repository.php) for use by the scientific community in, for example, local sequence similarity searches and in the QIIME pipeline. The system and the data will be updated automatically as the number of public fungal ITS sequences grows. We invite everybody in the position to improve the annotation or metadata associated with their particular fungal lineages of expertise to do so through the new Web-based sequence management system in UNITE.
View details for DOI 10.1111/mec.12481
View details for Web of Science ID 000325990500001
View details for PubMedID 24112409
Strong coupling of plant and fungal community structure across western Amazonian rainforests
2013; 7 (9): 1852-1861
The Amazon basin harbors a diverse ecological community that has a critical role in the maintenance of the biosphere. Although plant and animal communities have received much attention, basic information is lacking for fungal or prokaryotic communities. This is despite the fact that recent ecological studies have suggested a prominent role for interactions with soil fungi in structuring the diversity and abundance of tropical rainforest trees. In this study, we characterize soil fungal communities across three major tropical forest types in the western Amazon basin (terra firme, seasonally flooded and white sand) using 454 pyrosequencing. Using these data, we examine the relationship between fungal diversity and tree species richness, and between fungal community composition and tree species composition, soil environment and spatial proximity. We find that the fungal community in these ecosystems is diverse, with high degrees of spatial variability related to forest type. We also find strong correlations between α- and β-diversity of soil fungi and trees. Both fungal and plant community β-diversity were also correlated with differences in environmental conditions. The correlation between plant and fungal richness was stronger in fungal lineages known for biotrophic strategies (for example, pathogens, mycorrhizas) compared with a lineage known primarily for saprotrophy (yeasts), suggesting that this coupling is, at least in part, due to direct plant-fungal interactions. These data provide a much-needed look at an understudied dimension of the biota in an important ecosystem and supports the hypothesis that fungal communities are involved in the regulation of tropical tree diversity.
View details for DOI 10.1038/ismej.2013.66
View details for Web of Science ID 000323385600015
View details for PubMedID 23598789
- Host plant genus-level diversity is the best predictor of ectomycorrhizal fungal diversity in a Chinese subtropical forest MOLECULAR ECOLOGY 2013; 22 (12): 3403-3414
- Independent roles of ectomycorrhizal and saprotrophic communities in soil organic matter decomposition SOIL BIOLOGY & BIOCHEMISTRY 2013; 57: 282-291
- Rat invasion of islands alters fungal community structure, but not wood decomposition rates OIKOS 2013; 122 (2): 258-264
Towards global patterns in the diversity and community structure of ectomycorrhizal fungi
2012; 21 (17): 4160-4170
Global species richness patterns of soil micro-organisms remain poorly understood compared to macro-organisms. We use a global analysis to disentangle the global determinants of diversity and community composition for ectomycorrhizal (EcM) fungi-microbial symbionts that play key roles in plant nutrition in most temperate and many tropical forest ecosystems. Host plant family has the strongest effect on the phylogenetic community composition of fungi, whereas temperature and precipitation mostly affect EcM fungal richness that peaks in the temperate and boreal forest biomes, contrasting with latitudinal patterns of macro-organisms. Tropical ecosystems experience rapid turnover of organic material and have weak soil stratification, suggesting that poor habitat conditions may contribute to the relatively low richness of EcM fungi, and perhaps other soil biota, in most tropical ecosystems. For EcM fungi, greater evolutionary age and larger total area of EcM host vegetation may also contribute to the higher diversity in temperate ecosystems. Our results provide useful biogeographic and ecological hypotheses for explaining the distribution of fungi that remain to be tested by involving next-generation sequencing techniques and relevant soil metadata.
View details for DOI 10.1111/j.1365-294X.2012.05602.x
View details for Web of Science ID 000308047100004
View details for PubMedID 22568722
Measuring ectomycorrhizal fungal dispersal: macroecological patterns driven by microscopic propagules
2012; 21 (16): 4122-4136
Dispersal plays a prominent role in most conceptual models of community assembly. However, direct measurement of dispersal across a whole community is difficult at ecologically relevant spatial scales. For cryptic organisms, such as fungi and bacteria, the scale and importance of dispersal limitation has become a major point of debate. We use an experimental island biogeographic approach to measure the effects of dispersal limitation on the ecological dynamics of an important group of plant symbionts, ectomycorrhizal fungi. We manipulated the isolation of uncolonized host seedlings across a natural landscape and used a range of molecular techniques to measure the dispersal rates of ectomycorrhizal propagules and host colonization. Some species were prolific dispersers, producing annual spore loads on the order of trillions of spores per km(2). However, fungal propagules reaching host seedlings decreased rapidly with increasing distance from potential spore sources, causing a concomitant reduction in ectomycorrhizal species richness, host colonization and host biomass. There were also strong differences in dispersal ability across species, which correlated well with the predictable composition of ectomycorrhizal communities associated with establishing pine forest. The use of molecular tools to measure whole community dispersal provides a direct confirmation for a key mechanism underlying island biogeography theory and has the potential to make microbial systems a model for understanding the role of dispersal in ecological theory.
View details for DOI 10.1111/j.1365-294X.2012.05666.x
View details for Web of Science ID 000306897500019
View details for PubMedID 22703050
Flowers as Islands: Spatial Distribution of Nectar-Inhabiting Microfungi among Plants of Mimulus aurantiacus, a Hummingbird-Pollinated Shrub
2012; 63 (4): 711-718
Microfungi that inhabit floral nectar offer unique opportunities for the study of microbial distribution and the role that dispersal limitation may play in generating distribution patterns. Flowers are well-replicated habitat islands, among which the microbes disperse via pollinators. This metapopulation system allows for investigation of microbial distribution at multiple spatial scales. We examined the distribution of the yeast, Metschnikowia reukaufii, and other fungal species found in the floral nectar of the sticky monkey flower, Mimulus aurantiacus, a hummingbird-pollinated shrub, at a California site. We found that the frequency of nectar-inhabiting microfungi on a given host plant was not significantly correlated with light availability, nectar volume, or the percent cover of M. aurantiacus around the plant, but was significantly correlated with the location of the host plant and loosely correlated with the density of flowers on the plant. These results suggest that dispersal limitation caused by spatially nonrandom foraging by pollinators may be a primary factor driving the observed distribution pattern.
View details for DOI 10.1007/s00248-011-9975-8
View details for Web of Science ID 000306127300001
View details for PubMedID 22080257
Phylogenetic relatedness predicts priority effects in nectar yeast communities
PROCEEDINGS OF THE ROYAL SOCIETY B-BIOLOGICAL SCIENCES
2012; 279 (1729): 749-758
Priority effects, in which the outcome of species interactions depends on the order of their arrival, are a key component of many models of community assembly. Yet, much remains unknown about how priority effects vary in strength among species in a community and what factors explain this variation. We experimented with a model natural community in laboratory microcosms that allowed us to quantify the strength of priority effects for most of the yeast species found in the floral nectar of a hummingbird-pollinated shrub at a biological preserve in northern California. We found that priority effects were widespread, with late-arriving species experiencing strong negative effects from early-arriving species. However, the magnitude of priority effects varied across species pairs. This variation was phylogenetically non-random, with priority effects stronger between closer relatives. Analysis of carbon and amino acid consumption profiles indicated that competition between closer relatives was more intense owing to higher ecological similarity, consistent with Darwin's naturalization hypothesis. These results suggest that phylogenetic relatedness between potential colonists may explain the strength of priority effects and, as a consequence, the degree to which community assembly is historically contingent.
View details for DOI 10.1098/rspb.2011.1230
View details for Web of Science ID 000299114100017
View details for PubMedID 21775330
Spongiforma squarepantsii, a new species of gasteroid bolete from Borneo
2011; 103 (5): 1119-1123
A gasteroid bolete collected recently in Sarawak on the island of Borneo is described as the new species Spongiforma squarepantsii. A comprehensive description, illustrations, phylogenetic placement and a comparison with a closely allied species are provided.
View details for DOI 10.3852/10-433
View details for Web of Science ID 000294529400017
View details for PubMedID 21558499
- Rethinking ectomycorrhizal succession: are root density and hyphal exploration types drivers of spatial and temporal zonation? FUNGAL ECOLOGY 2011; 4 (3): 233-240
Evidence of dispersal limitation in soil microorganisms: Isolation reduces species richness on mycorrhizal tree islands
2010; 91 (12): 3631-3640
Dispersal limitation plays an important role in a number of equilibrium and nonequilibrium theories about community ecology. In this study we use the framework of island biogeography to look for evidence of dispersal limitation in ectomycorrhizal fungal assemblages on "tree islands," patches of host trees located in a non-host vegetation matrix. Because of the potentially strong effects of island area on species richness and immigration, we chose to control island size by sampling tree islands consisting of a single host individual. Richness on tree islands was high, with estimates ranging up to 42 species of ectomycorrhizal fungi associating with a single host individual. Species richness decreased significantly with increasing isolation of tree islands, with our regression predicting a 50% decrease in species richness when tree islands are located distances of approximately 1 km from large patches of contiguous forests. Despite the fact that fungal fruit bodies produce large numbers of spores with high potential for long-distance travel, these results suggest that dispersal limitation is significant in ectomycorrhizal assemblages. There were no discernible effects of isolation or environment on the species identity of tree island fungal colonists. In contrast to the highly predictable patterns of tree island colonization we observed in a previous study on early successional forests, we suggest that over longer time periods the community assembly process becomes more dominated by stochastic immigration and local extinction events.
View details for Web of Science ID 000285635100024
View details for PubMedID 21302834
- Testing the ecological stability of ectomycorrhizal symbiosis: effects of heat, ash and mycorrhizal colonization on Pinus muricata seedling performance PLANT AND SOIL 2010; 330 (1-2): 291-302
Potential link between plant and fungal distributions in a dipterocarp rainforest: community and phylogenetic structure of tropical ectomycorrhizal fungi across a plant and soil ecotone
2010; 185 (2): 529-542
*Relatively little is known about diversity or structure of tropical ectomycorrhizal communities or their roles in tropical ecosystem dynamics. In this study, we present one of the largest molecular studies to date of an ectomycorrhizal community in lowland dipterocarp rainforest. *We sampled roots from two 0.4 ha sites located across an ecotone within a 52 ha forest dynamics plot. Our plots contained > 500 tree species and > 40 species of ectomycorrhizal host plants. Fungi were identified by sequencing ribosomal RNA genes. *The community was dominated by the Russulales (30 species), Boletales (17), Agaricales (18), Thelephorales (13) and Cantharellales (12). Total species richness appeared comparable to molecular studies of temperate forests. Community structure changed across the ecotone, although it was not possible to separate the role of environmental factors vs host plant preferences. Phylogenetic analyses were consistent with a model of community assembly where habitat associations are influenced by evolutionary conservatism of functional traits within ectomycorrhizal lineages. *Because changes in the ectomycorrhizal fungal community parallel those of the tree community at this site, this study demonstrates the potential link between the distribution of tropical tree diversity and the distribution of tropical ectomycorrhizal diversity in relation to local-scale edaphic variation.
View details for DOI 10.1111/j.1469-8137.2009.03075.x
View details for Web of Science ID 000272893800017
View details for PubMedID 19878464
Root tip competition among ectomycorrhizal fungi: Are priority effects a rule or an exception?
2009; 90 (8): 2098-2107
Competition for root colonization among ectomycorrhizal fungi is well documented, but the mechanisms determining competitive outcomes are not clearly understood. In a previous study, we observed that timing of colonization (i.e., a priority effect) had a significant effect on the outcome of competition between two ectomycorrhizal (EM) fungi in the genus Rhizopogon. In this study, we explicitly tested the role of priority effects in competition among EM fungi by experimentally manipulating the timing of colonization of four Rhizopogon species on Pinus muricata seedlings. In a first experiment, we set up 12 two-species combinations, in which seedlings were first inoculated from spores with one species, grown for three months, and then inoculated with an equal density of spores of a second species and grown for an additional three months. Root tip occupation in the two-species treatments was determined by polymerase chain reaction restriction fragment length polymorphism (PCR-RFLP) analysis of internal transcribed spacer region (ITS) of rDNA. In a second experiment, we further examined competitive interactions between two Rhizopogon species using split-root P. muricata seedlings. One side of the root system was pre-colonized by one species, and spores of the second species were added to the other side of the root system in all same and different species pair-wise combinations. We found that for three of the four species (R. occidentalis, R. salebrosus, R. vulgaris), the outcome of competition in the first experiment depended strongly on the timing of colonization, with the first colonizing species always being the competitive dominant. For R. evadens, however, initial colonization did not prevent significant subsequent colonization by R. occidentalis and R. vulgaris. This appeared to be caused by the lower colonization of R. evadens compared to the three other species. In the second experiment, we observed that the portion of the split root system that was initially uncolonized remained receptive to colonization when spores were added. The amount of colonization of R. occidentalis and R. salebrosus on the side of the root system to which they were added was not significantly influenced by species identity on the other side of the seedling. In combination, these results confirm that priority effects do play a major role in dynamics of EM root tip colonization, at least in the early colonization of seedlings, and that the proportion of the root system occupied by a species appears to be a key factor determining competitive success.
View details for Web of Science ID 000268293000009
View details for PubMedID 19739372
- Spore heat resistance plays an important role in disturbance-mediated assemblage shift of ectomycorrhizal fungi colonizing Pinus muricata seedlings JOURNAL OF ECOLOGY 2009; 97 (3): 537-547
- Fungal Community Ecology: A Hybrid Beast with a Molecular Master BIOSCIENCE 2008; 58 (9): 799-810
A strong species-area relationship for eukaryotic soil microbes: island size matters for ectomycorrhizal fungi
2007; 10 (6): 470-480
While the effects of habitat size and isolation have been successfully studied for macro-organisms, there is currently debate about their relative importance in explaining patterns of microbial species richness. In this study, we examine the species richness of a dominant group of eukaryotic soil microbes, ectomycorrhizal fungi, on 'tree islands' of constant age and host composition that range in size from < 10 to > 10,000 m(2). Our results show that ectomycorrhizal species richness is significantly reduced on smaller and more isolated tree islands, and the species-area slope that we observe (0.20-0.23) is similar to average slopes reported for macro-organisms. Additionally, species' occurrence patterns across tree islands and investment trends in fungal fruit bodies suggest that a trade-off between competition and dispersal could play an important role in structuring ectomycorrhizal assemblages.
View details for DOI 10.1111/j.1461-0248.2007.01035.x
View details for Web of Science ID 000246364500004
View details for PubMedID 17498146