R. Vilgalys's research while affiliated with Duke University and other places
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Publications (896)
Ectomycorrhizal (EM) fungal communities that associate with invading pines (Pinus spp.) are expected to be poor in species diversity. However, long-term successional trajectories and the persistence of dispersal limitations of EM fungi in the exotic range are not well understood. We sampled the roots and surrounding soil of Pinus elliottii and P. t...
Symbiotic soil microbes can facilitate plant invasions, yet it is unclear whether the invasive capacity of plants can be explained by the invasiveness of their microbial symbionts. After compiling a global dataset on associations between non‐native invasive pine trees and ectomycorrhizal fungi (EMF), we found that the interaction with invasive EMF...
The jasmonic acid (JA) signaling pathway plays an important role in the establishment of the ectomycorrhizal symbiosis (ECM) between Laccaria bicolor and poplar. We previously showed that the L. bicolor effector MiSSP7 induces the stabilization of the poplar JAZ6, a JA co-repressor protein that binds to Populus MYC2.1 and MYC2.2, orthologs of the A...
Optimizing loblolly pine (Pinus taeda L.) productivity using fertilizers and various site management practices has been a goal of foresters for decades. Nitrogen (N), phosphorus (P), and potassium (K) are the three most operationally applied fertilizers to loblolly pine silviculture and are of primary importance to their total productivity. Fertili...
Fungi of the Conidiobolus group belong to the family Ancylistaceae (Entomophthorales, Entomophthoromycotina, Zoopagomycota) and include over 70 predominantly saprotrophic species in four similar and closely related genera, that were separated phylogenetically recently. Entomopathogenic fungi of the genus Batkoa are very close morphologically to the...
Small genes (<150 nucleotides) have been systematically overlooked in phage genomes. We employ a large-scale comparative genomics approach to predict >40,000 small-gene families in ∼2.3 million phage genome contigs. We find that small genes in phage genomes are approximately 3-fold more prevalent than in host prokaryotic genomes. Our approach enric...
Closely related species are expected to have similar functional traits due to shared ancestry and phylogenetic inertia. However, few tests of this hypothesis are available for plant‐associated fungal symbionts. Fungal leaf endophytes occur in all land plants and can protect their host plant from disease by a variety of mechanisms, including by para...
Within the forest community, competition and facilitation between adjacent-growing conspecific and heterospecific plants are mediated by interactions involving common mycorrhizal networks. The ability of plants to alter their neighbor’s microbiome is well documented, but the molecular biology of plant-fungal interactions during competition and faci...
Increasing temperature and decreasing precipitation has led to more frequent and extreme drought events in many regions throughout the world. In the western United States, multi‐year drought events have led to widespread plant mortality and extreme wildfires (Asner et al. 2016, Pickrell and Pennisi 2020). Communities of ectomycorrhizal fungi (EMF)...
PurposeWildfire, an increasing disturbance in peatlands, could dramatically change carbon stocks and reshape plant/microbial communities, with long-lasting effects on peatland functions. Soil fungi are important in controlling the belowground carbon and nutrient cycling in peatlands; however, the impact of altered fire regimes on these fungi is sti...
Pines (Pinus spp.) rely on co-introduced ectomycorrhizal (EM) fungi to invade native ecosystems in the Southern Hemisphere. Although co-invasive EM fungal communities are expected to be poor in species, long-term successional trajectories and the persistence of dispersal limitations are not well understood. We sampled the roots and surrounding soil...
Peatlands have persisted as massive carbon sinks over millennia, even during past periods of climate change. The commonly accepted theory of abiotic controls (mainly anoxia and low temperature) over carbon decomposition cannot fully explain how vast low-latitude shrub/tree dominated (wooded) peatlands consistently accrete peat under warm and season...
Purpose: Wildfire, an increasing disturbance in peatlands, could dramatically change carbon stocks and reshape plant/microbial communities, with long-lasting effects on peatland functions. Soil fungi are important in controlling the belowground carbon and nutrient cycling in peatlands; however, the impact of altered fire regimes on these fungi is s...
Clitopilus hobsonii (Entolomataceae, Agaricales, Basidiomycetes) is a common soil saprotroph. There is also evidence that C. hobsonii can act as a root endophyte benefitting tree growth. Here, we report the genome assembly of C. hobsonii QYL-10, isolated from ectomycorrhizal root tips of Quercus lyrata. The genome size is 36.93 Mb, consisting of 13...
The ectomycorrhizal fungal symbiont Cenococcum geophilum is of high interest as it is globally distributed, associates with many plant species, and has resistance to multiple environmental stressors. C . geophilum is only known from asexual states but is often considered a cryptic species complex, since extreme phylogenetic divergence is often obse...
While there has been significant progress characterizing the ‘symbiotic tool kit’ of ectomycorrhizal (ECM) fungi, how host specificity may be encoded into ECM fungal genomes remains poorly understood. We conducted a comparative genomic analysis of ECM fungal host specialists and generalists, focusing on the specialist genus Suillus. Global analyses...
Mycorrhizal fungi are mutualists that play crucial roles in nutrient acquisition in terrestrial ecosystems. Mycorrhizal symbioses arose repeatedly across multiple lineages of Mucor-omycotina, Ascomycota, and Basidiomycota. Considerable variation exists in the capacity of mycorrhizal fungi to acquire carbon from soil organic matter. Here, we present...
Human‐altered environments can shape the evolution of organisms. Fungi are no exception, though little is known about how they withstand anthropogenic pollution. Here, we document adaptation in the mycorrhizal fungus Suillus luteus driven by soil heavy metal contamination. Genome scans across individuals from recently polluted and nearby unpolluted...
Introductions and invasions by fungi, especially pathogens and mycorrhizal fungi, are widespread and potentially highly consequential for native ecosystems, but may also offer opportunities for linking microbial traits to their ecosystem functions. In particular, treating ectomycorrhizal (EM) invasions, i.e., co-invasions by EM fungi and their EM h...
Recent studies have shown that M. elongata (M. elongata) isolated from Populus field sites has a dual endophyte-saprotroph lifestyle and is able to promote the growth of Populus. However, little is known about the host fidelity of M. elongata and whether M. elongata strains differ from one another in their ability to promote plant growth. Here, we...
Blumeriella jaapii is the causal agent of cherry leaf spot (CLS), the most important disease of tart cherry in the Midwestern United States. Infection of leaves by B. jaapii leads to premature defoliation, which places trees at heightened risk of winter injury and death. Current management of CLS relies primarily on the application of three importa...
Peatlands have persisted over millennia as massive carbon sinks even during past periods of climate change. The commonly accepted theory of abiotic controls (mainly anoxia and low temperature) over carbon decomposition cannot explain how vast low-latitude wooded peatlands consistently accrete peat under warm and seasonally unsaturated conditions. S...
The ectomycorrhizal fungal symbiont Cenococcum geophilum is of great interest as it is globally distributed, associates with many plant species, and has resistance to multiple environmental stressors. C. geophilum is only known from asexual states but is often considered a cryptic species complex, since extreme phylogenetic divergence is often obse...
Even though many fungi are known to degrade a range of organic chemicals and may be advantageous for targeting hydrophobic chemicals with low bioavailability due to their ability to secrete extracellular enzymes, fungi are not commonly leveraged in the context of bioremediation. Here we sought to examine the fungal microbiome (mycobiome) at a model...
Ectomycorrhizal fungi (ECMF) are partners in a globally distributed tree symbiosis implicated in most major ecosystem functions. However, resilience of ECMF to future climates is uncertain. We forecast these changes over the extent of North American Pinaceae forests. About 68 sites from North American Pinaceae forests ranging from Florida to Ontari...
Human-altered environments can shape the evolution of organisms. Fungi are no exception, though little is known about how they withstand anthropogenic pollution. Here, we document incipient polygenic local adaptation in the mycorrhizal fungus Suillus luteus driven by recent soil heavy metal contamination. Genome scans across individuals from recent...
We identified two poplar (Populus sp.)-associated microbes, the fungus, Mortierella elongata strain AG77, and the bacterium, Burkholderia strain BT03, that mutually promote each other’s growth. Using culture assays in concert with a novel microfluidic device to generate time-lapse videos, we found growth specific media differing in pH and pre-condi...
Chemical pollution mixtures enter aquatic environments and interact with microorganisms in eclectic ways with disparate consequences for microbial ecosystem services. Can using a thermodynamic framework help to determine the net influence of a chemical mixture on the functional capacity of benthic microbial communities? We examined this question by...
Background:
Microfluidic systems are well-suited for studying mixed biological communities for improving industrial processes of fermentation, biofuel production, and pharmaceutical production. The results of which have the potential to resolve the underlying mechanisms of growth and transport in these complex branched living systems. Microfluidic...
Root alkaloids remain highly unexplored in ectomycorrhizae development studies. By employing ultrahigh mass resolution mass spectrometry imaging techniques, we showed substantial relocation and transformation of piperidine alkaloids in pine root tips in response to Suillus mycorrhization. We imaged, in the time frame of ectomycorrhizae formation, a...
Raw bipartite networks representing the occurrence of operational taxonomic units (OTUs) within samples for Experiment 1: Plant genotype. Sample nodes are colored by (A) genotype and (B) soil. Samples clearly separate by soil and not be genotype.
Enrichment of operational taxonomic units (OTUs) in genotypes, within each soil. OTU nodes are connected to genotype nodes via colored “soil specific” edges. An edge between an OTU and a genotype represents that the OTU is enriched in that genotype within the soil denoted by the edge color. One can clearly see that the enrichment of OTUs in genotyp...
Boxplots showing the relative abundance of fungi and bacteria across different hierarchical classification for the two experiments. (A) Fungi across different soils (Experiment 2: Soil origin); (B) Fungi across different Populus genotypes; (C) Bacteria across different soils (Experiment 2: Soil origin); (D) Bacteria across different Populus genotyp...
Distributions of selected network topology measures for the Experiment 2 operational taxonomic unit (OTU) correlation network.
Characteristics of soils used in this study.
Unique fungal operational taxonomic units (OTUs) recovered from uninoculated control plants.
Correlation network maximum spanning tree of soil physicochemical and environmental parameters.
Operational taxonomic units (OTUs) assigned to Markov Cluster (MCL) communities for Experiment 1, as well as various network topology measures each OTU node in the pearson correlation network the communities were constructed from.
Contingency table used in the calculation of Fisher Exact Tests. Each mij is entry ij of an operational taxonomic unit (out) matrix/binned OTU matrix M.
Assessments of arbuscular mycorrhizal fungal diversity.
Summary of the sizes of Markov Cluster (MCL) communities for Experiment 2, as we as the number of fungi vs bacterial members.
Rarefaction curves for ITS and 16S rDNA from Experiments 1 and 2.
Cytoscape session containing the networks for Experiment 1.
Degree of each operational taxonomic unit (OTU) in the Experiment 1 bipartite network, as well as the number of different genotypes the OTU is found in.
Distributions of selected network topology measures for the Experiment 1 operational taxonomic unit (OTU) correlation network.
Summary of the sizes of Markov Cluster (MCL) communities for Experiment 1, as we as the number of fungi vs bacterial members.
Primer sequence information for 454 primers used in this study.
Degree of each operational taxonomic unit (OTU) in the Experiment 1 enrichment network, the number of different genotypes the OTU is significantly enriched in, as well as the quotient of degree/#genotypes. The quotient gives an indication of how genotype-specific the OTU is.
Operational taxonomic units (OTUs) assigned to Markov Cluster (MCL) communities for Experiment 2, as well as various network topology measures each OTU node in the pearson correlation network the communities were constructed from.
Cytoscape session containing the networks for Experiment 2.
Plant root-associated microbial symbionts comprise the plant rhizobiome. These microbes function in provisioning nutrients and water to their hosts, impacting plant health and disease. The plant microbiome is shaped by plant species, plant genotype, soil and environmental conditions, but the contributions of these variables are hard to disentangle...
Mortierella and Ilyonectria include common species of soil fungi which are frequently detected as root endophytes in many plants including Populus spp. However, the ecological roles of these and other endophytic fungi with respect to plant growth and function are still not well understood. The functional ecology of two key taxa from the Populus rhi...
Belowground biota can deeply influence plant invasion. The presence of proper soil mutualists can act as a driver that enable plants to colonize new ranges. We review the species of ectomycorrhizal fungi (EMF) that facilitate pine establishment in both native and non‐native ranges and that are associated with their invasion into nonforest settings....
Phylogenetic taxon definitions (PTDs) are explicit, phylogeny-based statements that specify clades. PTDs are central to the system of rank-free classification that is governed by the PhyloCode, but they can also be used to clarify the meanings of ranked names. We present PTDs for four major groups: Fungi, Dikarya, Ascomycota, and Basidiomycota.
[This corrects the article DOI: 10.1371/journal.pgen.1006348.].
Ectomycorrhizal fungi (ECMF) are partners in a globally distributed tree symbiosis that enhanced ecosystem carbon (C)-sequestration and storage. However, resilience of ECMF to future climates is uncertain. We sampled ECMF across a broad climatic gradient in North America, modeled climatic drivers of diversity and community composition, and then for...
Knowledge of the factors controlling the diverse chemical emissions of common environmental bacteria and fungi is crucial because they are important signal molecules for these microbes that also could influence humans. We show here not only a high diversity of mVOCs but that their abundance can differ greatly in different environmental contexts. Mi...
Phylogenomic approaches have the potential to improve confidence about the inter-relationships of species in the order Mucorales within the fungal tree of life. Rhizopus species are especially important as plant and animal pathogens and bioindustrial fermenters for food and metabolite production. A dataset of 192 orthologous genes was used to const...
Background:
Microorganisms serve important functions within numerous eukaryotic host organisms. An understanding of the variation in the plant niche-level microbiome, from rhizosphere soils to plant canopies, is imperative to gain a better understanding of how both the structural and functional processes of microbiomes impact the health of the ove...
We examined variation in growth rate, patterns of nitrogen utilization, and competitive interactions of Atractiella rhizophila isolates from the roots of Populus hosts. Atractiella grew significantly faster on media substituted with inorganic nitrogen sources and slower in the presence of another fungal genus. To determine plausible causal mechanis...
Temperate ectomycorrhizal (ECM) fungi show segregation whereby some species dominate in organic layers and others favor mineral soils. Weak layering in tropical soils is hypothesized to decrease niche space and therefore reduce the diversity of ectomycorrhizal fungi. The Neotropical ECM tree Dicymbe corymbosa forms monodominant stands and has a dis...
Deterministic and stochastic factors interact to generate biogeographic patterns in fungal communities, challenging efforts to predict which fungal assemblages will develop in association with introduced plants. The coastal dune grass Ammophila arenaria has been moved around the world. We sampled A. arenaria roots in its native range in the United...
Among fungi isolated from healthy root mycobiomes of Populus, we discovered a new endorrhizal
fungal species belonging to the rust lineage Pucciniomycotina, described here as Atractiella rhizophila.
We characterized this species by transmission electron microscopy (TEM), phylogenetic analysis, and
plant bioassay experiments. Phylogenetic sequence a...
[This corrects the article DOI: 10.1371/journal.pgen.1006348.].
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...
Endosymbiosis of bacteria by eukaryotes is a defining feature of cellular evolution. In addition to well known bacterial origins for mitochondria and chloroplasts, multiple origins of bacterial endosymbiosis are known within the cells of diverse animals, plants, and fungi. Early-diverging lineages of terrestrial fungi harbor endosymbiotic bacteria...
Many plant-associated fungi host endosymbiotic endobacteria with reduced genomes. While endobacteria play important roles in these tri-partite plant-fungal-endobacterial systems, the active physiology of fungal endobacteria has not been characterized extensively by systems biology approaches. Here, we use integrated proteomics and metabolomics to c...
Ectomycorrhizal fungi (EMF) represent one of the major guilds of symbiotic fungi associated with roots of forest trees, where they function to improve plant nutrition and fitness in exchange for plant carbon. Many groups of EMF exhibit preference or specificity for different plant host genera; a good example is the genus Suillus, which grows in ass...
Volcano plots of differential expression patterns of Suillus genes with two different Pinus hosts (Suillus/P. monticola vs. Suillus/P. strobus).
Dots indicate the expression pattern of an individual Suillus gene from Suillus/P. monticola vs. Suillus/P. strobus pairs. The data (normalized expression rates using DESeq package) for all genes are plott...
Gene expression of Suillus genes in response to compatible and incompatible mycorrhzal pairings.
(A) Principal components analysis of loadings for different Suillus-Pinus species pairings (Suillus/P. monticola in blue; Suillus/P. strobus in red; Suillus/P. taeda in green) based on normalized expression (log10) of Suillus genes (average 12,000 conti...
Principal components analysis of normalized expression rates (log2) of Pinus genes for Suillus-root samples paired with (A) P. monticola, (B) P. strobus, and (C) P. taeda.
Within each panel, dots represent the loading of one pine gene from data sources across four root pairs, including Pinus/S. americanus, Pinus/S. granulatus, Pinus/S. spraguei, Pi...
Compatible vs. incompatible gene expression of Suillus for one representative Suillus-Pinus root pair (Sa/Ps1).
In this study, under compatible interactions, 17M reads of Suillus were recovered from a compatible pair, however, only around 1.7M reads were recovered under incompatible pairs. To test if the normalizations for the Suillus reads for com...
Section 1. Numbers of Illumina RNASeq reads of Suillus and Pinus genes recovered from root tip samples; Section 2. The number of contigs recovered from root samples; Section 3. Lists of interactomes identified by comparative transcriptomics (the number of unique genes showed in Fig 4A); Section 4. Published studies describing function of plant gene...
Quality assessment for reference transcriptomes of Suillus spp.
FASTQ Quality Trimmer v1.0.0 was used to trim and quality filter reads (cutoff for quality scores <28). Suillus strain IDs (in parentheses) provided for RNASeq sample ID (e.g. S6_16) and fungal strain ID (e.g. EM31). Additional information for sample IDs is described in S1 Dataset, Tab...
Origins of Suillus collections, cultures and spore prints used in this study.
Cultures (tissue isolates) were isolated from fresh fruit bodies on MMN media (same media used for maintaining and storing cultures). For each Suillus-Pinus species pair examined (Fig 1B), spore prints from three sporocarps (fruit bodies) were pooled and used to inoculate...