Ronald P de Vries1,2, Robert Riley3, Ad Wiebenga4,5, Guillermo Aguilar-Osorio6, Sotiris Amillis7, Cristiane Akemi Uchima8,9, Gregor Anderluh10, Mojtaba Asadollahi11, Marion Askin12,13, Kerrie Barry3, Evy Battaglia4,5, Özgür Bayram14,15, Tiziano Benocci4,5, Susanna A Braus-Stromeyer14, Camila Caldana8,16, David Cánovas17,18, Gustavo C Cerqueira19, Fusheng Chen20, Wanping Chen20, Cindy Choi3, Alicia Clum3, Renato Augusto Corrêa Dos Santos8, André Ricardo de Lima Damásio8,21, George Diallinas7, Tamás Emri22, Erzsébet Fekete11, Michel Flipphi11, Susanne Freyberg14, Antonia Gallo23, Christos Gournas24,25, Rob Habgood26, Matthieu Hainaut27, María Laura Harispe28,29, Bernard Henrissat27,30,31, Kristiina S Hildén32, Ryan Hope26, Abeer Hossain33,34, Eugenia Karabika35,36, Levente Karaffa11, Zsolt Karányi37, Nada Kraševec10, Alan Kuo3, Harald Kusch14,38,39, Kurt LaButti3, Ellen L Lagendijk12, Alla Lapidus3,40, Anthony Levasseur41,42, Erika Lindquist3, Anna Lipzen3, Antonio F Logrieco43, Andrew MacCabe44, Miia R Mäkelä32, Iran Malavazi45, Petter Melin46,47, Vera Meyer48, Natalia Mielnichuk17,49, Márton Miskei22,50, Ákos P Molnár11, Giuseppina Mulé43, Chew Yee Ngan3, Margarita Orejas44, Erzsébet Orosz4,22, Jean Paul Ouedraogo12,51, Karin M Overkamp33, Hee-Soo Park52, Giancarlo Perrone43, Francois Piumi41,53, Peter J Punt12,33, Arthur F J Ram12, Ana Ramón54, Stefan Rauscher55, Eric Record41, Diego Mauricio Riaño-Pachón8, Vincent Robert4, Julian Röhrig55, Roberto Ruller8, Asaf Salamov3, Nadhira S Salih26,56, Rob A Samson4, Erzsébet Sándor57, Manuel Sanguinetti54, Tabea Schütze12,58, Kristina Sepčić59, Ekaterina Shelest60, Gavin Sherlock61, Vicky Sophianopoulou24, Fabio M Squina8, Hui Sun3, Antonia Susca43, Richard B Todd62, Adrian Tsang63, Shiela E Unkles35, Nathalie van de Wiele4, Diana van Rossen-Uffink12,64, Juliana Velasco de Castro Oliveira8, Tammi C Vesth65, Jaap Visser4, Jae-Hyuk Yu66, Miaomiao Zhou4,5, Mikael R Andersen65, David B Archer26, Scott E Baker67, Isabelle Benoit4,5,68, Axel A Brakhage69, Gerhard H Braus14, Reinhard Fischer55, Jens C Frisvad65, Gustavo H Goldman70, Jos Houbraken4, Berl Oakley71, István Pócsi22, Claudio Scazzocchio72,73, Bernhard Seiboth74, Patricia A vanKuyk4,12, Jennifer Wortman75,76, Paul S Dyer26, Igor V Grigoriev3. 1. Westerdijk Fungal Biodiversity Institute, Uppsalalaan 8, 3584 CT, Utrecht, The Netherlands. r.devries@cbs.knaw.nl. 2. Fungal Molecular Physiology, Utrecht University, Uppsalalaan 8, 3584 CT, Utrecht, The Netherlands. r.devries@cbs.knaw.nl. 3. US Department of Energy Joint Genome Institute, 2800 Mitchell Drive, Walnut Creek, CA, 94598, USA. 4. Westerdijk Fungal Biodiversity Institute, Uppsalalaan 8, 3584 CT, Utrecht, The Netherlands. 5. Fungal Molecular Physiology, Utrecht University, Uppsalalaan 8, 3584 CT, Utrecht, The Netherlands. 6. Department of Food Science and Biotechnology, Faculty of Chemistry, National University of Mexico, Ciudad Universitaria, D.F., C.P. 04510, Mexico. 7. Department of Biology, National and Kapodistrian University of Athens, Panepistimioupolis, 15781, Athens, Greece. 8. Laboratório Nacional de Ciência e Tecnologia do Bioetanol (CTBE), Centro Nacional de Pesquisa em Energia e Materiais (CNPEM), Caixa Postal 6192, CEP 13083-970, Campinas, São Paulo, Brasil. 9. Present address: VTT Brasil, Alameda Inajá, 123, CEP 06460-055, Barueri, São Paulo, Brazil. 10. Laboratory for Molecular Biology and Nanobiotechnology, National Institute of Chemistry, Hajdrihova 19, 1000, Ljubljana, Slovenia. 11. Department of Biochemical Engineering, Faculty of Science and Technology, University of Debrecen, 4032, Debrecen, Hungary. 12. Institute of Biology Leiden, Molecular Microbiology and Biotechnology, Leiden University, Sylviusweg 72, 2333, BE, Leiden, The Netherlands. 13. Present address: CSIRO Publishing, Unipark, Building 1 Level 1, 195 Wellington Road, Clayton, VIC, 3168, Australia. 14. Department of Molecular Microbiology and Genetics, Institute for Microbiology and Genetics, Georg August University Göttingen, Grisebachstr. 8, 37077, Göttingen, Germany. 15. Department of Biology, Maynooth University, Maynooth, Co. Kildare, Ireland. 16. Max Planck Partner Group, Brazilian Bioethanol Science and Technology Laboratory, CEP 13083-100, Campinas, Sao Paulo, Brazil. 17. Department of Genetics, Faculty of Biology, University of Seville, Avda de Reina Mercedes 6, 41012, Sevilla, Spain. 18. Fungal Genetics and Genomics Unit, Department of Applied Genetics and Cell Biology, University of Natural Resources and Life Sciences (BOKU) Vienna, Vienna, Austria. 19. Broad Institute of Harvard and MIT, 75 Ames St, Cambridge, MA, 02142, USA. 20. College of Food Science and Technology, Huazhong Agricultural University, Wuhan, 430070, China. 21. Department of Biochemistry and Tissue Biology, Institute of Biology, University of Campinas, CEP 13083-862, Campinas, SP, Brazil. 22. Department of Biotechnology and Microbiology, Faculty of Science and Technology, University of Debrecen, Egyetem tér 1, 4032, Debrecen, Hungary. 23. Institute of Sciences of Food Production (ISPA), National Research Council (CNR), via Provinciale Lecce-Monteroni, 73100, Lecce, Italy. 24. Institute of Biosciences and Applications, Microbial Molecular Genetics Laboratory, National Center for Scientific Research, Demokritos (NCSRD), Athens, Greece. 25. Present address: Université Libre de Bruxelles Institute of Molecular Biology and Medicine (IBMM), Brussels, Belgium. 26. School of Life Sciences, University of Nottingham, University Park, Nottingham, NG7 2RD, UK. 27. CNRS, Aix-Marseille Université, Marseille, France. 28. Institut Pasteur de Montevideo, Unidad Mixta INIA-IPMont, Mataojo 2020, CP11400, Montevideo, Uruguay. 29. Present address: Instituto de Profesores Artigas, Consejo de Formación en Educación, ANEP, CP 11800, Av. del Libertador 2025, Montevideo, Uruguay. 30. INRA, USC 1408 AFMB, 13288, Marseille, France. 31. Department of Biological Sciences, King Abdulaziz University, Jeddah, Saudi Arabia. 32. Department of Food and Environmental Sciences, University of Helsinki, Viikinkaari 9, Helsinki, Finland. 33. Dutch DNA Biotech BV, Utrechtseweg 48, 3703AJ, Zeist, The Netherlands. 34. Swammerdam Institute for Life Sciences, University of Amsterdam, Amsterdam, The Netherlands. 35. School of Biology, University of St Andrews, St Andrews, Fife, KY16 9TH, UK. 36. Present Address: Department of Chemistry, University of Ioannina, Ioannina, 45110, Greece. 37. Department of Medicine, Faculty of Medicine, University of Debrecen, Nagyerdei krt. 98, 4032, Debrecen, Hungary. 38. Department of Medical Informatics, University Medical Centre, Robert-Koch-Str.40, 37075, Göttingen, Germany. 39. Department of Molecular Biology, Universitätsmedizin Göttingen, Humboldtallee 23, Göttingen, 37073, Germany. 40. Present address: Center for Algorithmic Biotechnology, St.Petersburg State University, St. Petersburg, Russia. 41. INRA, Aix-Marseille Univ, BBF, Biodiversité et Biotechnologie Fongiques, Marseille, France. 42. Present address: Aix-Marseille Université, Unité de Recherche sur les Maladies Infectieuses et Tropicales Emergentes (URMITE), UM63, CNRS 7278, IRD 198, INSERM U1095, IHU Méditerranée Infection, Pôle des Maladies Infectieuses, Assistance Publique-Hôpitaux de Marseille, Faculté de Médecine, 27 Bd Jean Moulin, 13005, Marseille, France. 43. Institute of Sciences of Food Production (ISPA), National Research Council (CNR), Via Amendola 122/O, 70126, Bari, Italy. 44. Departamento de Biotecnología, Instituto de Agroquímica y Tecnología de Alimentos, Consejo Superior de Investigaciones Científicas (CSIC), Paterna, Valencia, Spain. 45. Departamento de Genética e Evolução, Centro de Ciências Biológicas e da Saúde, Universidade Federal de São Carlos, São Carlos, São Paulo, Brazil. 46. Uppsala BioCenter, Department of Microbiology, Swedish University of Agricultural Sciences, P.O. Box 7025, 750 07, Uppsala, Sweden. 47. Present address: Swedish Chemicals Agency, Box 2, 172 13, Sundbyberg, Sweden. 48. Institute of Biotechnology, Department Applied and Molecular Microbiology, Berlin University of Technology, Gustav-Meyer-Allee 25, 13355, Berlin, Germany. 49. Present address: Instituto de Ciencia y Tecnología Dr. César Milstein, Fundación Pablo Cassará, CONICET, Saladillo 2468 C1440FFX, Ciudad de Buenos Aires, Argentina. 50. MTA-DE Momentum, Laboratory of Protein Dynamics, Department of Biochemistry and Molecular Biology, University of Debrecen, Nagyerdei krt.98., 4032, Debrecen, Hungary. 51. Present address: Centre for Structural and Functional Genomics, Concordia University, 7141 Sherbrooke Street West, Montreal, QC, H4B 1R6, Canada. 52. School of Food Science and Biotechnology, Kyungpook National University, Daegu, 702-701, Republic of Korea. 53. Present address: INRA UMR1198 Biologie du Développement et de la Reproduction - Domaine de Vilvert, Jouy en Josas, 78352, Cedex, France. 54. Sección Bioquímica, Departamento de Biología Celular y Molecular, Facultad de Ciencias, Universidad de la República, Montevideo, Uruguay. 55. Department of Microbiology, Karlsruhe Institute of Technology, Institute for Applied Biosciences, Hertzstrasse 16,, 76187, Karlsruhe, Germany. 56. Department of Biology, School of Science, University of Sulaimani, Al Sulaymaneyah, Iraq. 57. Institute of Food Science, Faculty of Agricultural and Food Sciences and Environmental Management, University of Debrecen, 4032, Debrecen, Hungary. 58. Present address: Department Applied and Molecular Microbiology, Institute of Biotechnology, Berlin University of Technology, Gustav-Meyer-Allee 25, 13355, Berlin, Germany. 59. Department of Biology, Biotechnical Faculty, University of Ljubljana, Jamnikarjeva 101, 1000, Ljubljana, Slovenia. 60. Systems Biology/Bioinformatics group, Leibniz Institute for Natural Product Research and Infection Biology, Hans Knoell Institute, (HKI), Beutenbergstr. 11a, 07745, Jena, Germany. 61. Department of Genetics, Stanford University, Stanford, CA, 94305-5120, USA. 62. Department of Plant Pathology, Kansas State University, Manhattan, KS, 66506, USA. 63. Centre for Structural and Functional Genomics, Concordia University, 7141 Sherbrooke Street West, Montreal, QC, H4B 1R6, Canada. 64. Present address: BaseClear B.V., Einsteinweg 5, 2333, CC, Leiden, The Netherlands. 65. Department of Biotechnology and Biomedicine, Technical University of Denmark, Søltofts Plads 223, 2800, Kongens Lyngby, Denmark. 66. Departments of Bacteriology and Genetics, University of Wisconsin-Madison, 1550 Linden Drive, Madison, WI, 53706, USA. 67. Fungal Biotechnology Team, Pacific Northwest National Laboratory, Richland, Washington, 99352, USA. 68. Present address: Centre of Functional and Structure Genomics Biology Department Concordia University, 7141 Sherbrooke St. W., Montreal, QC, H4B 1R6, Canada. 69. Department of Molecular and Applied Microbiology, Leibniz-Institute for Natural Product Research and Infection Biology - Hans Knoell Institute (HKI) and Institute for Microbiology, Friedrich Schiller University Jena, Beutenbergstr. 11a, 07745, Jena, Germany. 70. Faculdade de Ciências Farmacêuticas de Ribeirão Preto, Universidade de São Paulo, Av. do Café S/N, CEP 14040-903, Ribeirão Preto, São Paulo, Brazil. 71. Department of Molecular Biosciences, University of Kansas, Lawrence, Kansas, 66045, USA. 72. Department of Microbiology, Imperial College, London, SW7 2AZ, UK. 73. Institute for Integrative Biology of the Cell (I2BC), CEA, CNRS, University Paris-Sud, Université Paris-Saclay, 91198, Gif-sur-Yvette cedex, France. 74. Research Division Biochemical Technology, Institute of Chemical Engineering, TU Wien, Gumpendorferstraße 1a, 1060, Vienna, Austria. 75. Broad Institute, 415 Main St, Cambridge, MA, 02142, USA. 76. Present address: Seres Therapeutics, 200 Sidney St, Cambridge, MA, 02139, USA.
Abstract
BACKGROUND: The fungal genus Aspergillus is of critical importance to humankind. Species include those with industrial applications, important pathogens of humans, animals and crops, a source of potent carcinogenic contaminants of food, and an important genetic model. The genome sequences of eight aspergilli have already been explored to investigate aspects of fungal biology, raising questions about evolution and specialization within this genus. RESULTS: We have generated genome sequences for ten novel, highly diverse Aspergillus species and compared these in detail to sister and more distant genera. Comparative studies of key aspects of fungal biology, including primary and secondary metabolism, stress response, biomass degradation, and signal transduction, revealed both conservation and diversity among the species. Observed genomic differences were validated with experimental studies. This revealed several highlights, such as the potential for sex in asexual species, organic acid production genes being a key feature of black aspergilli, alternative approaches for degrading plant biomass, and indications for the genetic basis of stress response. A genome-wide phylogenetic analysis demonstrated in detail the relationship of the newly genome sequenced species with other aspergilli. CONCLUSIONS: Many aspects of biological differences between fungal species cannot be explained by current knowledge obtained from genome sequences. The comparative genomics and experimental study, presented here, allows for the first time a genus-wide view of the biological diversity of the aspergilli and in many, but not all, cases linked genome differences to phenotype. Insights gained could be exploited for biotechnological and medical applications of fungi.
BACKGROUND: The fungal genus Aspergillus is of critical importance to humankind. Species include those with industrial applications, important pathogens of humans, animals and crops, a source of potent carcinogenic contaminants of food, and an important genetic model. The genome sequences of eight aspergilli have already been explored to investigate aspects of fungal biology, raising questions about evolution and specialization within this genus. RESULTS: We have generated genome sequences for ten novel, highly diverse Aspergillus species and compared these in detail to sister and more distant genera. Comparative studies of key aspects of fungal biology, including primary and secondary metabolism, stress response, biomass degradation, and signal transduction, revealed both conservation and diversity among the species. Observed genomic differences were validated with experimental studies. This revealed several highlights, such as the potential for sex in asexual species, organic acid production genes being a key feature of black aspergilli, alternative approaches for degrading plant biomass, and indications for the genetic basis of stress response. A genome-wide phylogenetic analysis demonstrated in detail the relationship of the newly genome sequenced species with other aspergilli. CONCLUSIONS: Many aspects of biological differences between fungal species cannot be explained by current knowledge obtained from genome sequences. The comparative genomics and experimental study, presented here, allows for the first time a genus-wide view of the biological diversity of the aspergilli and in many, but not all, cases linked genome differences to phenotype. Insights gained could be exploited for biotechnological and medical applications of fungi.
Authors: M Ashburner; C A Ball; J A Blake; D Botstein; H Butler; J M Cherry; A P Davis; K Dolinski; S S Dwight; J T Eppig; M A Harris; D P Hill; L Issel-Tarver; A Kasarskis; S Lewis; J C Matese; J E Richardson; M Ringwald; G M Rubin; G Sherlock Journal: Nat Genet Date: 2000-05 Impact factor: 38.330
Authors: Jacob L Steenwyk; Abigail L Lind; Laure N A Ries; Thaila F Dos Reis; Lilian P Silva; Fausto Almeida; Rafael W Bastos; Thais Fernanda de Campos Fraga da Silva; Vania L D Bonato; André Moreira Pessoni; Fernando Rodrigues; Huzefa A Raja; Sonja L Knowles; Nicholas H Oberlies; Katrien Lagrou; Gustavo H Goldman; Antonis Rokas Journal: Curr Biol Date: 2020-06-04 Impact factor: 10.834
Authors: Lorna M Y Mitchison-Field; José M Vargas-Muñiz; Benjamin M Stormo; Ellysa J D Vogt; Sarah Van Dierdonck; James F Pelletier; Christoph Ehrlich; Daniel J Lew; Christine M Field; Amy S Gladfelter Journal: Curr Biol Date: 2019-10-10 Impact factor: 10.834
Authors: Michelle F Grau; Ruth Entwistle; Yi-Ming Chiang; Manmeet Ahuja; C Elizabeth Oakley; Tomohiro Akashi; Clay C C Wang; Richard B Todd; Berl R Oakley Journal: ACS Chem Biol Date: 2018-10-29 Impact factor: 5.100
Authors: Matthew E Mead; Sonja L Knowles; Jacob L Steenwyk; Huzefa A Raja; Christopher D Roberts; Oliver Bader; Jos Houbraken; Gustavo H Goldman; Nicholas H Oberlies; Antonis Rokas Journal: Genetics Date: 2020-08-17 Impact factor: 4.562