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A Comparative Genomics Study of 23 Aspergillus Species from Section Flavi

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ARTICLE https://doi.org/10.1038/s41467-019-14051-y OPEN A comparative genomics study of 23 Aspergillus species from section Flavi Inge Kjærbølling1, Tammi Vesth1, Jens C. Frisvad 1, Jane L. Nybo1, Sebastian Theobald1, Sara Kildgaard1, Thomas Isbrandt Petersen1, Alan Kuo2, Atsushi Sato3, Ellen K. Lyhne1, Martin E. Kogle1, Ad Wiebenga4, Roland S. Kun4, Ronnie J.M. Lubbers4, Miia R. Mäkelä 5, Kerrie Barry2, Mansi Chovatia2, Alicia Clum2, Chris Daum2, Sajeet Haridas 2, Guifen He2, Kurt LaButti 2, Anna Lipzen2, Stephen Mondo2, Jasmyn Pangilinan2, Robert Riley2, Asaf Salamov2, Blake A. Simmons 6, Jon K. Magnuson 6, Bernard Henrissat7, Uffe H. Mortensen 1, Thomas O. Larsen 1, Ronald P. de Vries 4, Igor V. Grigoriev 2,8, 9 6,10 1 1234567890():,; Masayuki Machida , Scott E. Baker & Mikael R. Andersen * Section Flavi encompasses both harmful and beneficial Aspergillus species, such as Aspergillus oryzae, used in food fermentation and enzyme production, and Aspergillus flavus, food spoiler and mycotoxin producer. Here, we sequence 19 genomes spanning section Flavi and compare 31 fungal genomes including 23 Flavi species. We reassess their phylogenetic relationships and show that the closest relative of A. oryzae is not A. flavus, but A. minisclerotigenes or A. aflatoxiformans and identify high genome diversity, especially in sub-telomeric regions. We predict abundant CAZymes (598 per species) and prolific secondary metabolite gene clus- ters (73 per species) in section Flavi. However, the observed phenotypes (growth char- acteristics, polysaccharide degradation) do not necessarily correlate with inferences made from the predicted CAZyme content. Our work, including genomic analyses, phenotypic assays, and identification of secondary metabolites, highlights the genetic and metabolic diversity within section Flavi. 1 Department of Biotechnology and Bioengineering, Technical University of Denmark, Søltoft Plads 223, 2800 Kongens Lyngby, Denmark. 2 US Department of Energy Joint Genome Institute, 2800 Mitchell Drive, Walnut Creek, CA 94598, USA. 3 Kikkoman Corporation, 250 Noda, 278-0037 Noda, Japan. 4 Fungal Physiology, Westerdijk Fungal Biodiversity Institute & Fungal Molecular Physiology, Utrecht University, Uppsalalaan 8, 3584 CT Utrecht, The Netherlands. 5 Department of Microbiology, Faculty of Agriculture and Forestry, University of Helsinki, Viikinkaari 9, Helsinki, Finland. 6 US Department of Energy Joint BioEnergy Institute, 5885 Hollis St., Emeryville, CA 94608, USA. 7 Architecture et Fonction des Macromolécules Biologiques, (CNRS UMR 7257, Aix- Marseille University, 163 Avenue de Luminy, Parc Scientifique et Technologique de Luminy, 13288 Marseille, France. 8 Department of Plant and Microbial Biology, University of California, 111 Koshland Hall, Berkeley, CA 94720, USA. 9 Kanazawa Institute of Technology, 3 Chome-1, 924-0838 Yatsukaho, Hakusan-shi, Ishikawa-ken, Japan. 10 Environmental Molecular Sciences Division, Earth and Biological Sciences Directorate, Pacific Northwest National Laboratory, 902 Battelle Blvd, Richland, WA 99354, USA. *email: [email protected] NATURE COMMUNICATIONS | (2020) 11:1106 | https://doi.org/10.1038/s41467-019-14051-y | www.nature.com/naturecommunications 1 ARTICLE NATURE COMMUNICATIONS | https://doi.org/10.1038/s41467-019-14051-y spergillus section Flavi encompasses a large number of alternative species for industrial use, combat pathogenicity, find A species, many of which have a significant impact on novel bioactives, and to identify useful enzymes. Prior to this human life: some species (e.g., A. oryzae and A. sojae) are project, whole-genome sequences were only available for five routinely used in production of sake, miso, soy sauce, and other species from section Flavi (A. oryzae, A. flavus, A. sojae, A. fermented foods. Moreover, A. oryzae is used industrially for luteovirescens (formerly A. bombycis), and A. parasiticus3,12–15). production of enzymes and secondary metabolite production1–4. They all belong to a closely related clade within the section and In contrast, other Flavi species (e.g., A. flavus and A. parasiticus) thus cover only a small part of the diversity. are notorious for producing highly toxic fungal compounds (e.g., In this study, as part of the Aspergillus genus-sequencing aflatoxins), in addition to infecting and damaging crops5–7. project16,17, we have generated genome sequences for 18 addi- Furthermore, A. flavus has been shown to infect immunocom- tional species plus an additional A. parasiticus isolate, permitting promised humans, and is currently the second most common genomic comparisons across 23 members of section Flavi con- cause of human aspergillosis8,9. taining at least 29 species10. We apply these sequences in tandem In addition, the section includes less known species that, with experimental and phenotypic data on secondary metabolite similar to their (in)famous relatives, display both beneficial and production, growth characteristics, and plant polysaccharide harmful properties. The benefits are found in producers of degradation to link phenotypes to genotypes and quantify the bioactive compounds (such as the anti-insectant N-alkoxypyr- genetic potential of the section. Our analysis is useful for (1) idone metabolite, leporin A, from A. leporis; an antibiotic with exploring novel enzymes and secondary metabolites, (2) opti- antifungal activity, avenaciolide, from A. avenaceus) and enzyme mizing food fermentation and industrial use, and (3) improving producers (including amylases, proteases, and xylanolytic food and feed protection and control. enzymes in A. tamarii and pectin-degrading enzymes in A. alliaceus). On the harmful side, plant pathogens (A. alliaceus on onion bulb, A. nomius on nuts, seeds, and grains) and toxin Results and discussion producers (ochratoxin from A. alliaceus,aflatoxin from A. Assessment of 19 newly sequenced section Flavi genomes.In nomius) are also found among these less studied Flavi spe- this study, we present the whole-genome sequences of 19 species cies10,11, for which no genome sequences have previously been from Aspergillus section Flavi (Fig. 1b). Two of these (A. nomius available. and A. arachidicola18,19) were also published by other groups in Given the importance of section Flavi, it is highly valuable to parallel to this work. We compare these 19 to previously examine the full genetic potential of the section in order to assess sequenced section Flavi species (A. oryzae, A. flavus, A. sojae, and abc Legend for A A. parasiticus 38.4 13,752 75 48.1 270 354,721 34 Unresolved 100 * 100 A. transmontanensis 39.3 14,216 74 48 293 342,792 36 Legend for B 99 A. arachidicola 39.8 13,895 74 48.1 451 349,923 34 A. flavus clade 100 A. tamarii clade A. novoparasiticus 40.9 14,182 73 48 870 276,844 48 A. nomius clade A. sergii 38.3 13,713 75 48.2 262 382,883 33 A. alliaceus clade A. flavus 36.8 12,604 69 48.3 138 2,388,123 6 A. togoensis clade 100 72 A. sojae – 12,738 – – – – – A. leporis clade 81 * A. avenaceus clade A. aflatoxiformans 37.6 13,595 73 48.2 385 240,665 47 This project 94 A. oryzae 37.9 12,030 70 47.2 11 4,887,096 4 100 95 A. minisclerotigenes 37.1 13,415 75 48.3 296 298,536 37 72 A. caelatus 40 13,916 75 47.6 729 115,961 102 * 100 81 A. aflatoxi... A. pseudocaelatus 39.7 13,895 75 47.6 466 210,129 58 100 97 94 A. pseudotamarii 38.2 13,428 74 47.9 249 410,003 29 95 A. oryzae 100 A. minisclerotigenes A. tamarii 38.5 13,331 75 47.5 448 214,496 51 100 A. pseudonomius 37.8 13,384 74 48.4 374 271,263 40 100 100 A. nomius 36.7 12,897 76 48.6 290 332,018 32 A. luteovirescens 37.5 12,265 81 48.8 450 240,792 46 100 A. bertholletius 37 12,948 74 48.2 443 173,958 72 A. alliaceus 40.2 13,099 72 47.1 331 499,171 24 100 100 100 A. albertensis 40.1 12,816 74 47.1 473 296,126 44 100 A. coremiiformis 30.1 9078 75 43 2728 58,658 135 A. leporis 39.4 12,745 74 47.5 615 157,399 82 100 A. avenaceus 33.8 11,293 76 45.6 1528 79,000 112 A. steynii 37.8 13,211 66 49.1 37 3,921,250 4 66 28.3 9764 68 51.2 62 1,703,432 6 90 56 A. campestris A. terreus 29.3 10,406 72 52.7 26 1,912,493 7 100 A. nidulans 30.5 10,680 72 49.3 8 3,759,208 4 80 A. niger ATCC 1015 34.9 11,910 70 50.3 24 1,937,564 6 A. fumigatus Af293 29.4 9781 72 48.8 8 3,948,441 4 P. digitatum 26 9118 67 48.2 100 878,909 8 100 N. crassa 41 10,785 64 48.2 20 6,000,761 3 0.2 Genome Predicted InterPro GC Scaffolds Scaffold L50 Scaffold N50 size (MB) proteins (#) (%) (%) (#) (bp) (#) Fig. 1 Phylogeny and genome statistics of section Flavi plus eight other Aspergillus, Penicillium, and Neurospora species. a Phylogenetic tree constructed using RAxML, MUSCLE, and Gblocks based on 200 monocore genes (a single homolog in each of the species). The red star indicates an uncertain leaf most likely caused by a different gene calling method98–100, and the arrow shows where A. sojae should be placed in the phylogenetic tree. The zoom shows the branching in a clade around A. oryzae. b The colors illustrate the clades found within section Flavi and X indicates species sequenced in this study. Earlier sequenced genomes such as A. oryzae and A. fumigatus were assembled using optical mapping and genetic maps. c Seven bubble plots illustrating key genome numbers and sequencing quality parameter. The bubble sizes have been scaled to each panel and are not comparable across panels. 2 NATURE COMMUNICATIONS | (2020) 11:1106 | https://doi.org/10.1038/s41467-019-14051-y | www.nature.com/naturecommunications NATURE COMMUNICATIONS | https://doi.org/10.1038/s41467-019-14051-y ARTICLE A.
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  • Sequencing Abstracts Msa Annual Meeting Berkeley, California 7-11 August 2016

    Sequencing Abstracts Msa Annual Meeting Berkeley, California 7-11 August 2016

    M S A 2 0 1 6 SEQUENCING ABSTRACTS MSA ANNUAL MEETING BERKELEY, CALIFORNIA 7-11 AUGUST 2016 MSA Special Addresses Presidential Address Kerry O’Donnell MSA President 2015–2016 Who do you love? Karling Lecture Arturo Casadevall Johns Hopkins Bloomberg School of Public Health Thoughts on virulence, melanin and the rise of mammals Workshops Nomenclature UNITE Student Workshop on Professional Development Abstracts for Symposia, Contributed formats for downloading and using locally or in a Talks, and Poster Sessions arranged by range of applications (e.g. QIIME, Mothur, SCATA). 4. Analysis tools - UNITE provides variety of analysis last name of primary author. Presenting tools including, for example, massBLASTer for author in *bold. blasting hundreds of sequences in one batch, ITSx for detecting and extracting ITS1 and ITS2 regions of ITS 1. UNITE - Unified system for the DNA based sequences from environmental communities, or fungal species linked to the classification ATOSH for assigning your unknown sequences to *Abarenkov, Kessy (1), Kõljalg, Urmas (1,2), SHs. 5. Custom search functions and unique views to Nilsson, R. Henrik (3), Taylor, Andy F. S. (4), fungal barcode sequences - these include extended Larsson, Karl-Hnerik (5), UNITE Community (6) search filters (e.g. source, locality, habitat, traits) for 1.Natural History Museum, University of Tartu, sequences and SHs, interactive maps and graphs, and Vanemuise 46, Tartu 51014; 2.Institute of Ecology views to the largest unidentified sequence clusters and Earth Sciences, University of Tartu, Lai 40, Tartu formed by sequences from multiple independent 51005, Estonia; 3.Department of Biological and ecological studies, and for which no metadata Environmental Sciences, University of Gothenburg, currently exists.