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Genome Biol. 2017 Feb 14;18(1):28. doi: 10.1186/s13059-017-1151-0.

Comparative genomics reveals high biological diversity and specific adaptations in the industrially and medically important fungal genus Aspergillus.

de Vries RP1,2, Riley R3, Wiebenga A4,5, Aguilar-Osorio G6, Amillis S7, Uchima CA8,9, Anderluh G10, Asadollahi M11, Askin M12,13, Barry K3, Battaglia E4,5, Bayram Ö14,15, Benocci T4,5, Braus-Stromeyer SA14, Caldana C8,16, Cánovas D17,18, Cerqueira GC19, Chen F20, Chen W20, Choi C3, Clum A3, Dos Santos RA8, Damásio AR8,21, Diallinas G7, Emri T22, Fekete E11, Flipphi M11, Freyberg S14, Gallo A23, Gournas C24,25, Habgood R26, Hainaut M27, Harispe ML28,29, Henrissat B27,30,31, Hildén KS32, Hope R26, Hossain A33,34, Karabika E35,36, Karaffa L11, Karányi Z37, Kraševec N10, Kuo A3, Kusch H14,38,39, LaButti K3, Lagendijk EL12, Lapidus A3,40, Levasseur A41,42, Lindquist E3, Lipzen A3, Logrieco AF43, MacCabe A44, Mäkelä MR32, Malavazi I45, Melin P46,47, Meyer V48, Mielnichuk N17,49, Miskei M22,50, Molnár ÁP11, Mulé G43, Ngan CY3, Orejas M44, Orosz E4,22, Ouedraogo JP12,51, Overkamp KM33, Park HS52, Perrone G43, Piumi F41,53, Punt PJ12,33, Ram AF12, Ramón A54, Rauscher S55, Record E41, Riaño-Pachón DM8, Robert V4, Röhrig J55, Ruller R8, Salamov A3, Salih NS26,56, Samson RA4, Sándor E57, Sanguinetti M54, Schütze T12,58, Sepčić K59, Shelest E60, Sherlock G61, Sophianopoulou V24, Squina FM8, Sun H3, Susca A43, Todd RB62, Tsang A63, Unkles SE35, van de Wiele N4, van Rossen-Uffink D12,64, Oliveira JV8, Vesth TC65, Visser J4, Yu JH66, Zhou M4,5, Andersen MR65, Archer DB26, Baker SE67, Benoit I4,5,68, Brakhage AA69, Braus GH14, Fischer R55, Frisvad JC65, Goldman GH70, Houbraken J4, Oakley B71, Pócsi I22, Scazzocchio C72,73, Seiboth B74, vanKuyk PA4,12, Wortman J75,76, Dyer PS26, Grigoriev IV3.

Author information

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.

KEYWORDS:

Aspergillus; Comparative genomics; Fungal biology; Genome sequencing

PMID:
28196534
PMCID:
PMC5307856
DOI:
10.1186/s13059-017-1151-0
[Indexed for MEDLINE]
Free PMC Article

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