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      Large-scale generation and analysis of filamentous fungal DNA barcodes boosts coverage for kingdom fungi and reveals thresholds for fungal species and higher taxon delimitation

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          Abstract

          Species identification lies at the heart of biodiversity studies that has in recent years favoured DNA-based approaches. Microbial Biological Resource Centres are a rich source for diverse and high-quality reference materials in microbiology, and yet the strains preserved in these biobanks have been exploited only on a limited scale to generate DNA barcodes. As part of a project funded in the Netherlands to barcode specimens of major national biobanks, sequences of two nuclear ribosomal genetic markers, the Internal Transcribed Spaces and 5.8S gene (ITS) and the D1/D2 domain of the 26S Large Subunit (LSU), were generated as DNA barcode data for ca. 100 000 fungal strains originally assigned to ca. 17 000 species in the CBS fungal biobank maintained at the Westerdijk Fungal Biodiversity Institute, Utrecht. Using more than 24 000 DNA barcode sequences of 12 000 ex-type and manually validated filamentous fungal strains of 7 300 accepted species, the optimal identity thresholds to discriminate filamentous fungal species were predicted as 99.6 % for ITS and 99.8 % for LSU. We showed that 17 % and 18 % of the species could not be discriminated by the ITS and LSU genetic markers, respectively. Among them, ∼8 % were indistinguishable using both genetic markers. ITS has been shown to outperform LSU in filamentous fungal species discrimination with a probability of correct identification of 82 % vs. 77.6 %, and a clustering quality value of 84 % vs. 77.7 %. At higher taxonomic classifications, LSU has been shown to have a better discriminatory power than ITS. With a clustering quality value of 80 %, LSU outperformed ITS in identifying filamentous fungi at the ordinal level. At the generic level, the clustering quality values produced by both genetic markers were low, indicating the necessity for taxonomic revisions at genus level and, likely, for applying more conserved genetic markers or even whole genomes. The taxonomic thresholds predicted for filamentous fungal identification at the genus, family, order and class levels were 94.3 %, 88.5 %, 81.2 % and 80.9 % based on ITS barcodes, and 98.2 %, 96.2 %, 94.7 % and 92.7 % based on LSU barcodes. The DNA barcodes used in this study have been deposited to GenBank and will also be publicly available at the Westerdijk Institute's website as reference sequences for fungal identification, marking an unprecedented data release event in global fungal barcoding efforts to date.

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          Most cited references41

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          A DNA barcode for land plants.

          DNA barcoding involves sequencing a standard region of DNA as a tool for species identification. However, there has been no agreement on which region(s) should be used for barcoding land plants. To provide a community recommendation on a standard plant barcode, we have compared the performance of 7 leading candidate plastid DNA regions (atpF-atpH spacer, matK gene, rbcL gene, rpoB gene, rpoC1 gene, psbK-psbI spacer, and trnH-psbA spacer). Based on assessments of recoverability, sequence quality, and levels of species discrimination, we recommend the 2-locus combination of rbcL+matK as the plant barcode. This core 2-locus barcode will provide a universal framework for the routine use of DNA sequence data to identify specimens and contribute toward the discovery of overlooked species of land plants.
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            Metagenomics: application of genomics to uncultured microorganisms.

            Metagenomics (also referred to as environmental and community genomics) is the genomic analysis of microorganisms by direct extraction and cloning of DNA from an assemblage of microorganisms. The development of metagenomics stemmed from the ineluctable evidence that as-yet-uncultured microorganisms represent the vast majority of organisms in most environments on earth. This evidence was derived from analyses of 16S rRNA gene sequences amplified directly from the environment, an approach that avoided the bias imposed by culturing and led to the discovery of vast new lineages of microbial life. Although the portrait of the microbial world was revolutionized by analysis of 16S rRNA genes, such studies yielded only a phylogenetic description of community membership, providing little insight into the genetics, physiology, and biochemistry of the members. Metagenomics provides a second tier of technical innovation that facilitates study of the physiology and ecology of environmental microorganisms. Novel genes and gene products discovered through metagenomics include the first bacteriorhodopsin of bacterial origin; novel small molecules with antimicrobial activity; and new members of families of known proteins, such as an Na(+)(Li(+))/H(+) antiporter, RecA, DNA polymerase, and antibiotic resistance determinants. Reassembly of multiple genomes has provided insight into energy and nutrient cycling within the community, genome structure, gene function, population genetics and microheterogeneity, and lateral gene transfer among members of an uncultured community. The application of metagenomic sequence information will facilitate the design of better culturing strategies to link genomic analysis with pure culture studies.
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              Fungal Diversity Revisited: 2.2 to 3.8 Million Species.

              The question of how many species of Fungi there are has occasioned much speculation, with figures mostly posited from around half a million to 10 million, and in one extreme case even a sizable portion of the spectacular number of 1 trillion. Here we examine new evidence from various sources to derive an updated estimate of global fungal diversity. The rates and patterns in the description of new species from the 1750s show no sign of approaching an asymptote and even accelerated in the 2010s after the advent of molecular approaches to species delimitation. Species recognition studies of (semi-)cryptic species hidden in morpho-species complexes suggest a weighted average ratio of about an order of magnitude for the number of species recognized after and before such studies. New evidence also comes from extrapolations of plant:fungus ratios, with information now being generated from environmental sequence studies, including comparisons of molecular and fieldwork data from the same sites. We further draw attention to undescribed species awaiting discovery in biodiversity hot spots in the tropics, little-explored habitats (such as lichen-inhabiting fungi), and material in collections awaiting study. We conclude that the commonly cited estimate of 1.5 million species is conservative and that the actual range is properly estimated at 2.2 to 3.8 million. With 120,000 currently accepted species, it appears that at best just 8%, and in the worst case scenario just 3%, are named so far. Improved estimates hinge particularly on reliable statistical and phylogenetic approaches to analyze the rapidly increasing amount of environmental sequence data.

                Author and article information

                Contributors
                Journal
                Stud Mycol
                Stud. Mycol
                Studies in Mycology
                CBS Fungal Biodiversity Centre
                0166-0616
                1872-9797
                30 May 2018
                March 2019
                30 May 2018
                : 92
                : 135-154
                Affiliations
                [1 ]Westerdijk Fungal Biodiversity Institute, Uppsalalaan 8, 3584 CT Utrecht, The Netherlands
                [2 ]Staatliches Museum f. Naturkunde Stuttgart, Abt. Botanik, Rosenstein 1, D-70191 Stuttgart, Germany
                [3 ]University of Perugia, Dept. of Pharmaceutical Sciences, Via Borgo 20 Giugno 74, I 06121 Perugia, Italy
                [4 ]Institute for Biodiversity and Ecosystem Dynamics, University of Amsterdam, The Netherlands
                [5 ]Wageningen University and Research Centre (WUR), Laboratory of Phytopathology, Droevendaalsesteeg 1, 6708 PB Wageningen, The Netherlands
                [6 ]Department of Genetics, Biochemistry and Microbiology, Forestry and Agricultural Biotechnology Institute (FABI), University of Pretoria, Pretoria 0028, South Africa
                Author notes
                Article
                S0166-0616(18)30027-7
                10.1016/j.simyco.2018.05.001
                6020082
                29955203
                7f694f2f-dab6-4593-ba26-86b9be025104
                © 2018 Westerdijk Fungal Biodiversity Institute. Production and hosting by ELSEVIER B.V.

                This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

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                Categories
                Research Paper

                Plant science & Botany
                automated curation,biological resource centre,fungi,its,lsu,taxonomic thresholds

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