Urmas Kõljalg

University of Tartu, Dorpat, Tartu County, Estonia

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Publications (63)272.46 Total impact

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    ABSTRACT: Fungi play major roles in ecosystem processes, but the determinants of fungal diversity and biogeographic patterns remain poorly understood. Using DNA metabarcoding data from hundreds of globally distributed soil samples, we demonstrate that fungal richness is decoupled from plant diversity. The plant-to-fungus richness ratio declines exponentially toward the poles. Climatic factors, followed by edaphic and spatial variables, constitute the best predictors of fungal richness and community composition at the global scale. Fungi show similar latitudinal diversity gradients to other organisms, with several notable exceptions. These findings advance our understanding of global fungal diversity patterns and permit integration of fungi into a general macroecological framework. Copyright © 2014, American Association for the Advancement of Science.
    Science 11/2014; 346(6213):1256688. · 31.03 Impact Factor
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    ABSTRACT: Ectomycorrhizal symbiosis has evolved multiple times in plants and fungi, but the trophic status of certain fungal groups remains poorly understood due to their unculturability or ambiguous interpretation of biotrophic associations. Combining field observations, molecular identification of root tips, synthesis experiments and analysis of stable isotopes, we address the lifestyle of Tomentella crinalis and another species closely related to T. fibrosa that represents a sister group to the ectomycorrhizal genera Tomentella and Thelephora. Based on molecular analyses these two and other related species are moved to the genus Odontia. In Odontia species, ectomycorrhizal associations were not observed in nature or in various synthesis experiments. Although Odontia species normally fruit in old forests, Odontia ferruginea has also been identified from a deep belowground mine. Unlike saprotrophs, Odontia spp. and ectomycorrhizal fungi were not enriched in 13C compared with their woody fruiting substratum, suggesting that wood is not their major energy source. In contrast to ectomycorrhizal fungi, Odontia species and saprotrophs were not enriched in 15N relative to their substratum. Taken together, we suggest that Odontia spp. are non-mycorrhizal, but their nutrition differs from typical wood-rotting Basidiomycota.
    Fungal Ecology 10/2014; 11:80–90. · 2.85 Impact Factor
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    ABSTRACT: Macroecological patterns of microbes have received relatively little attention until recently. This study aimed to disentangle the determinants of the global biogeographic community of Alnus-associated actinobacteria belonging to the Frankia alni complex.By determining a global sequence similarity threshold for the nitrogenase reductase (nifH) gene, we separated Frankia into operational taxonomic units (OTUs) and tested the relative effects of Alnus phylogeny, geographic relatedness, and climatic and edaphic variables on community composition at the global scale.Based on the optimal nifH gene sequence similarity threshold of 99.3%, we distinguished 43 Frankia OTUs from root systems of 22 Alnus species on four continents. Host phylogeny was the main determinant of Frankia OTU-based community composition, but there was no effect on the phylogenetic structure of Frankia. Biogeographic analyses revealed the strongest cross-continental links over the Beringian land bridge.Despite the facultative symbiotic nature of Frankia, phylogenetic relations among Alnus species play a prominent role in structuring root-associated Frankia communities and their biogeographic patterns. Our results suggest that Alnus species exert strong phylogenetically determined selection pressure on compatible Actinobacteria.
    New Phytologist 08/2014; · 6.74 Impact Factor
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    ABSTRACT: Compared with plants and animals, large-scale biogeographic patterns of microbes including fungi are poorly understood. By use of a comparative phylogenetics approach and ancestral state reconstructions, we addressed the global biogeography, rate of evolution and evolutionary origin of the widely distributed ectomycorrhizal /sebacina lineage that forms a large proportion of the Sebacinales order. We downloaded all publicly available Internal Transcribed Spacer (ITS) sequences and metadata, and supplemented sequence information from three genes to construct dated phylogenies and test biogeographic hypotheses. The /sebacina lineage evolved 45-57 million years ago that groups it with relatively young ectomycorrhizal taxa in other studies. The most parsimonious origin for /sebacina is inferred to be North American temperate coniferous forests. Among biogeographic traits, region and biome exhibited stronger phylogenetic signal than host family. Consistent with the resource availability (environmental energy) hypothesis, the ITS region is evolving at a faster rate in tropical than non-tropical regions. Most biogeographic regions exhibited substantial phylogenetic clustering suggesting a strong impact of dispersal limitation over a large geographical scale. In northern Holarctic regions, however, phylogenetic distances and phylogenetic grouping of isolates indicate multiple recent dispersal events.This article is protected by copyright. All rights reserved.
    Molecular Ecology 06/2014; · 6.28 Impact Factor
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    ABSTRACT: Plant pathogenic fungi are a large and diverse assemblage of eukaryotes with substantial impacts on natural ecosystems and human endeavours. These taxa often have complex and poorly understood life cycles, lack observable, discriminatory morphological characters, and may not be amenable to in vitro culturing. As a result, species identification is frequently difficult. Molecular (DNA sequence) data have emerged as crucial information for the taxonomic identification of plant pathogenic fungi, with the nuclear ribosomal internal transcribed spacer (ITS) region being the most popular marker. However, international nucleotide sequence databases are accumulating numerous sequences of compromised or low-resolution taxonomic annotations and substandard technical quality, making their use in the molecular identification of plant pathogenic fungi problematic. Here we report on a concerted effort to identify high-quality reference sequences for various plant pathogenic fungi and to re-annotate incorrectly or insufficiently annotated public ITS sequences from these fungal lineages. A third objective was to enrich the sequences with geographical and ecological metadata. The results – a total of 31,954 changes – are incorporated in and made available through the UNITE database for molecular identification of fungi (http://unite.ut.ee), including standalone FASTA files of sequence data for local BLAST searches, use in the next-generation sequencing analysis platforms QIIME and mothur, and related applications. The present initiative is just a beginning to cover the wide spectrum of plant pathogenic fungi, and we invite all researchers with pertinent expertise to join the annotation effort.
    Fungal diversity 05/2014; 67(1):11-19. · 5.32 Impact Factor
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    ABSTRACT: Despite recent advances in understanding community ecology of ectomycorrhizal fungi, little is known about their spatial patterning and the underlying mechanisms driving these patterns across different ecosystems.This meta‐study aimed to elucidate the scale, rate and causes of spatial structure of ectomycorrhizal fungal communities in different ecosystems by analysing 16 and 55 sites at the local and global scales, respectively. We examined the distance decay of similarity relationship in species‐ and phylogenetic lineage‐based communities in relation to sampling and environmental variables.Tropical ectomycorrhizal fungal communities exhibited stronger distance‐decay patterns compared to non‐tropical communities. Distance from the equator and sampling area were the main determinants of the extent of distance decay in fungal communities. The rate of distance decay was negatively related to host density at the local scale. At the global scale, lineage‐level community similarity decayed faster with latitude than with longitude.Synthesis. Spatial processes play a stronger role and over a greater scale in structuring local communities of ectomycorrhizal fungi than previously anticipated, particularly in ecosystems with greater vegetation age and closer to the equator. Greater rate of distance decay occurs in ecosystems with lower host density that may stem from increasing dispersal and establishment limitation. The relatively strong latitude effect on distance decay of lineage‐level community similarity suggests that climate affects large‐scale spatial processes and may cause phylogenetic clustering of ectomycorrhizal fungi at the global scale.
    Journal of Ecology 09/2013; 101(5). · 5.69 Impact Factor
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    ABSTRACT: Fungi from the Ceratobasidiaceae family have important ecological roles as pathogens, saprotrophs, non-mycorrhizal endophytes, orchid mycorrhizal and ectomycorrhizal symbionts, but little is known about the distribution and evolution of these nutritional modes. All public ITS sequences of Ceratobasidiaceae were downloaded from databases, annotated with ecological and taxonomic metadata, and tested for the non-random phylogenetic distribution of nutritional modes. Phylogenetic analysis revealed six main clades within Ceratobasidiaceae and a poor correlation between molecular phylogeny and morphological–cytological characters traditionally used for taxonomy. Sequences derived from soil (representing putative saprotrophs) and orchid mycorrhiza clustered together, but remained distinct from pathogens. All nutritional modes were phylogenetically conserved in the Ceratobasidiaceae based on at least one index. Our analyses suggest that in general, autotrophic orchids form root symbiosis with available Ceratobasidiaceae isolates in soil. Ectomycorrhiza-forming capability has evolved twice within the Ceratobasidiaceae and it had a strong influence on the evolution of mycoheterotrophy and host specificity in certain orchid taxa.
    Fungal Ecology 08/2013; 6(4):256–268. · 2.85 Impact Factor
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    ABSTRACT: Novel high-throughput sequencing methods outperform earlier approaches in terms of resolution and magnitude. They enable identification and relative quantification of community members and offer new insights into fungal community ecology. These methods are currently taking over as the primary tool to assess fungal communities of plant-associated endophytes, pathogens, and mycorrhizal symbionts, as well as free-living saprotrophs. Taking advantage of the collective experience of six research groups, we here review the different stages involved in fungal community analysis, from field sampling via laboratory procedures to bioinformatics and data interpretation. We discuss potential pitfalls, alternatives, and solutions. Highlighted topics are challenges involved in: obtaining representative DNA/RNA samples and replicates that encompass the targeted variation in community composition, selection of marker regions and primers, options for amplification and multiplexing, handling of sequencing errors, and taxonomic identification. Without awareness of methodological biases, limitations of markers, and bioinformatics challenges, large-scale sequencing projects risk yielding artificial results and misleading conclusions.
    New Phytologist 03/2013; · 6.74 Impact Factor
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    ABSTRACT: Much of the macroecological information about microorganisms is confounded by the lack of standardized methodology, paucity of metadata and sampling effect of a particular substrate or interacting host taxa. This study aims to disentangle the relative effects of biological, geographical and edaphic variables on the distribution of Alnus-associated ectomycorrhizal (ECM) fungi at the global scale by using comparable sampling and analysis methods. Ribosomal DNA sequence analysis revealed 146 taxa of ECM fungi from 22 Alnus species across 96 sites worldwide. Use of spatial and phylogenetic eigenvectors along with environmental variables in model selection indicated that phylogenetic relations among host plants and geographical links explained 43 and 10%, respectively,in ECM fungal community composition, whereas soil calcium concentration positively influenced taxonomic richness. Intrageneric phylogenetic relations among host plants and regional processes largely account for the global biogeographic distribution of Alnus-associated ECM fungi. The biogeography of ECM fungi is consistent with ancient host migration patterns from Eurasia to North America and from southern Europe to northern Europe after the last glacial maximum, indicating codispersal of hosts and their mycobionts.
    New Phytologist 02/2013; · 6.74 Impact Factor
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    ABSTRACT: The nuclear ribosomal internal transcribed spacer (ITS) region is the formal fungal barcode and in most cases the marker of choice for 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 dataset, 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 tresholds (97-99%). An automatically or manually designated sequence is chosen to represent each such species hypothesis. These reference sequences are released (http://unite.ut.ee/repository.php) for use by the scientific community in, e.g., 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.This article is protected by copyright. All rights reserved.
    Molecular Ecology 01/2013; · 6.28 Impact Factor
  • Li-Wei Zhou, Urmas Kõljalg
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    ABSTRACT: Lenzitopsis (Thelephorales, Basidiomycota), typified by Lenzitopsis oxycedri, was monotypic before we described the second species of this genus, Lenzitopsis daii in this study. L. daii resembles L. oxycedri in producing lenzitoid hymenophore as well as brown hyphae and echinulate spores, but it differs from the type species by its annual basidiocarps, amyloid spores and growth exclusively on Juniperus chinensis (Cupressaceae). In the phylogenetic perspective inferred with nuclear large subunit ribosomal DNA sequences, the two species were separated from each other and formed a strongly supported clade in the Thelephorales. The two Lenzitopsis species showed a more than 5% difference in internal transcribed spacer sequences. Lenzitopsis species are wood-decaying fungi, and this is the second genus of the order where mycorrhizal life style is unknown, besides of Amaurodon.
    Mycoscience 01/2013; 54(1):87–92. · 1.17 Impact Factor
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    ABSTRACT: Ectomycorrhizal (ECM) fungi obtain both mineral and simple organic nutrients from soil and transport these to plant roots. Natural abundance of stable isotopes (¹⁵N and ¹³C) in fruit bodies and potential enzymatic activities of ECM root tips provide insights into mineral nutrition of these mutualistic partners. By combining rDNA sequence analysis with enzymatic and stable isotope assays of root tips, we hypothesized that phylogenetic affinities of ECM fungi are more important than ECM exploration type, soil horizon and host plant in explaining the differences in mineral nutrition of trees in an African lowland rainforest. Ectomycorrhizal fungal species belonging to extraradical mycelium-rich morphotypes generally displayed the strongest potential activities of degradation enzymes, except for laccase. The signature of ¹⁵N was determined by the ECM fungal lineage, but not by the exploration type. Potential enzymatic activities of root tips were unrelated to ¹⁵N signature of ECM root tip. The lack of correlation suggests that these methods address different aspects in plant nutrient uptake. Stable isotope analysis of root tips could provide an additional indirect assessment of fungal and plant nutrition that enables enhancement of taxonomic coverage and control for soil depth and internal nitrogen cycling in fungal tissues.
    New Phytologist 07/2012; 195(4):832-43. · 6.74 Impact Factor
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    ABSTRACT: Introduction of exotic plants change soil microbial communities which may have detrimental ecological consequences for ecosystems. In this study, we examined the community structure and species richness of ectomycorrhizal (EcM) fungi associated with exotic pine plantations in relation to adjacent native ectomycorrhizal trees in Iran to elucidate the symbiont exchange between distantly related hosts, i.e. Fagales (Fagaceae and Betulaceae) and Pinaceae. The combination of morphological and molecular identification approaches revealed that 84.6 % of species with more than one occurrence (at least once on pines) were shared with native trees and only 5.9 % were found exclusively on pine root tips. The community diversity of ectomycorrhizal fungi in the pine plantations adjacent to native EcM trees was comparable to their adjacent native trees, but the isolated plantations hosted relatively a species-poor community. Specific mycobionts of conifers were dominant in the isolated plantation while rarely found in the plantations adjacent to native EcM trees. These data demonstrate the importance of habitat isolation and dispersal limitation of EcM fungi in their potential of host range expansion. The great number of shared and possibly compatible symbiotic species between exotic Pinaceae and local Fagales (Fagaceae and Betulaceae) may reflect their evolutionary adaptations and/or ancestral compatibility with one another.
    Mycorrhiza 05/2012; · 2.96 Impact Factor
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    ABSTRACT: 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.
    Molecular Ecology 05/2012; 21(17):4160-70. · 6.28 Impact Factor
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    ABSTRACT: Six DNA regions were evaluated as potential DNA barcodes for Fungi, the second largest kingdom of eukaryotic life, by a multinational, multilaboratory consortium. The region of the mitochondrial cytochrome c oxidase subunit 1 used as the animal barcode was excluded as a potential marker, because it is difficult to amplify in fungi, often includes large introns, and can be insufficiently variable. Three subunits from the nuclear ribosomal RNA cistron were compared together with regions of three representative protein-coding genes (largest subunit of RNA polymerase II, second largest subunit of RNA polymerase II, and minichromosome maintenance protein). Although the protein-coding gene regions often had a higher percent of correct identification compared with ribosomal markers, low PCR amplification and sequencing success eliminated them as candidates for a universal fungal barcode. Among the regions of the ribosomal cistron, the internal transcribed spacer (ITS) region has the highest probability of successful identification for the broadest range of fungi, with the most clearly defined barcode gap between inter-and intraspecific variation. The nuclear ribosomal large subunit, a popular phylogenetic marker in certain groups, had superior species resolution in some taxonomic groups, such as the early diverging lineages and the ascomycete yeasts, but was otherwise slightly inferior to the ITS. The nuclear ribosomal small subunit has poor species-level resolution in fungi. ITS will be formally proposed for adoption as the primary fungal barcode marker to the Consortium for the Barcode of Life, with the possibility that supplementary barcodes may be developed for particular narrowly circumscribed taxonomic groups.
    Proceedings of the National Academy of Sciences 04/2012; 109(16):6241-6246. · 9.81 Impact Factor

Publication Stats

2k Citations
272.46 Total Impact Points

Institutions

  • 2001–2014
    • University of Tartu
      • • Institute of Ecology and Earth Sciences
      • • Department of Botany
      Dorpat, Tartu County, Estonia
  • 2011
    • Complutense University of Madrid
      Madrid, Madrid, Spain
  • 2010
    • The Ohio State University
      • Department of Evolution, Ecology, and Organismal Biology
      Columbus, OH, United States
  • 2007
    • Clark University
      • Department of Biology
      Worcester, MA, United States
  • 2004–2007
    • University of Gothenburg
      Göteborg, Vaestra Goetaland, Sweden