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Comparative Genomics Reveals High Biological Diversity and Specific Adaptations in the Industrially and Medically Important Fungal Genus Aspergillus Ronald P

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Comparative Genomics Reveals High Biological Diversity and Specific Adaptations in the Industrially and Medically Important Fungal Genus Aspergillus Ronald P de Vries et al. Genome Biology (2017) 18:28 DOI 10.1186/s13059-017-1151-0 RESEARCH Open Access Comparative genomics reveals high biological diversity and specific adaptations in the industrially and medically important fungal genus Aspergillus Ronald P. de Vries1,2*, Robert Riley3, Ad Wiebenga1,2, Guillermo Aguilar-Osorio4, Sotiris Amillis5, Cristiane Akemi Uchima6,60, Gregor Anderluh7, Mojtaba Asadollahi8, Marion Askin9,61, Kerrie Barry3, Evy Battaglia1,2, Özgür Bayram10,11, Tiziano Benocci1,2, Susanna A. Braus-Stromeyer10, Camila Caldana6,12, David Cánovas13,14, Gustavo C. Cerqueira15,FushengChen16,WanpingChen16,CindyChoi3, Alicia Clum3, Renato Augusto Corrêa dos Santos6, André Ricardo de Lima Damásio6,17, George Diallinas5,TamásEmri18,ErzsébetFekete8, Michel Flipphi8, Susanne Freyberg10, Antonia Gallo19,ChristosGournas20,62,RobHabgood21, Matthieu Hainaut22, María Laura Harispe23,63, Bernard Henrissat22,24,25, Kristiina S. Hildén26,RyanHope21,AbeerHossain27,28,EugeniaKarabika29,64, Levente Karaffa8, Zsolt Karányi30,NadaKraševec7,AlanKuo3,HaraldKusch10,31,32, Kurt LaButti3, Ellen L. Lagendijk9, Alla Lapidus3,65, Anthony Levasseur33,66, Erika Lindquist3,AnnaLipzen3, Antonio F. Logrieco34,AndrewMacCabe35, Miia R. Mäkelä26, Iran Malavazi36, Petter Melin37,67, Vera Meyer38, Natalia Mielnichuk13,68,MártonMiskei18,39,ÁkosP.Molnár8, Giuseppina Mulé34,ChewYeeNgan3, Margarita Orejas35, Erzsébet Orosz1,18, Jean Paul Ouedraogo9,69, Karin M. Overkamp27, Hee-Soo Park40, Giancarlo Perrone34,FrancoisPiumi33,70, Peter J. Punt9,27,ArthurF.J.Ram9, Ana Ramón41,StefanRauscher42,EricRecord33, Diego Mauricio Riaño-Pachón6,VincentRobert1, Julian Röhrig42, Roberto Ruller6,AsafSalamov3, Nadhira S. Salih21,43,RobA.Samson1, Erzsébet Sándor44, Manuel Sanguinetti41, Tabea Schütze9,71,KristinaSepčić45, Ekaterina Shelest46, Gavin Sherlock47, Vicky Sophianopoulou20,FabioM.Squina6, Hui Sun3ˆ,AntoniaSusca34,RichardB.Todd48,AdrianTsang49,ShielaE.Unkles29, Nathalie van de Wiele1, Diana van Rossen-Uffink9,72, Juliana Velasco de Castro Oliveira6,TammiC.Vesth50, Jaap Visser1,Jae-HyukYu51, Miaomiao Zhou1,2,MikaelR.Andersen50, David B. Archer21,ScottE.Baker52, Isabelle Benoit1,2,74,AxelA.Brakhage53, Gerhard H. Braus10,ReinhardFischer42, Jens C. Frisvad50, Gustavo H. Goldman54,JosHoubraken1,BerlOakley55, István Pócsi18, Claudio Scazzocchio56,57, Bernhard Seiboth58, Patricia A. vanKuyk1,9, Jennifer Wortman59,73, Paul S. Dyer21 and Igor V. Grigoriev3 * Correspondence: [email protected] ˆDeceased 1Westerdijk Fungal Biodiversity Institute, Uppsalalaan 8, 3584 CT Utrecht, The Netherlands 2Fungal Molecular Physiology, Utrecht University, Uppsalalaan 8, 3584 CT Utrecht, The Netherlands Full list of author information is available at the end of the article © The Author(s). 2017 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. de Vries et al. Genome Biology (2017) 18:28 Page 2 of 45 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, Genome sequencing, Comparative genomics, Fungal biology Background combined with synteny and orthology analysis. The in- The genus Aspergillus is one of the best studied genera clusion of these genomes in MycoCosm [15, 16] enabled of filamentous fungi, largely because of the medical comparison to sister and more distant genera. These (A. fumigatus, A. terreus), food spoilage (A. flavus, A. studies also revealed substantial genomic variations parasiticus), and industrial (A. niger, A. aculeatus, A. between these species and raised questions about the oryzae) relevance of some of its species, in addition to evolution of various aspects of fungal biology within the the fundamental studies in the model fungus A. nidu- genus. lans that have contributed broadly to our understand- In this study, ten novel genome sequences of the ing of eukaryotic cell biology and molecular processes. genus Aspergillus were generated, namely A. luchuensis, Aspergilli can grow in a wide range of niches, mainly A. aculeatus, A. brasiliensis, A. carbonarius, A. glaucus, in soils and on dead matter, and some are also capable A. sydowii, A. tubingensis, A. versicolor, A. wentii, and A. of colonizing living animal or plant hosts and, in total, zonatus. These species were chosen primarily to provide approximately 350 species have been identified in this better coverage of the whole genus, to complement the genus [1]. The broad relevance and economic import- already available genome sequences of A. clavatus, A. ance of the genus has pushed it to the forefront of fischeri, A. flavus, A. fumigatus, A. nidulans, A. niger, A. fungal research, with one of the largest academic and oryzae, and A. terreus, and to allow more detailed data industrial research communities [2]. mining of the industrially relevant section Nigri (A. Aspergillus species are characterized by the unifying luchuensis, A. aculeatus, A. brasiliensis, A. carbonarius, feature of the “aspergillum,” an asexual reproductive A. niger, A. tubingensis). Additional species from the structure. The aspergilli form a broad monophyletic section Nidulantes were included because of the high di- group, but show large taxonomic divergence with re- vergence of the genome sequence of A. nidulans from spect to morphology [3] and phylogenetic distance [4]. the other Aspergillus genomes, and A. sydowii because Genome sequences for three aspergilli [4–6] were of its marine life-style and being a pathogen of Gorgon- among the first to be reported from filamentous fungi ian corals [17]. We demonstrate that this combined set and were soon followed by an additional five genomes of genomes provides a highly valuable dataset for [7–10]. This has resulted in many genomic, comparative comparative and functional genomics. This study was genomic, and post-genomic studies covering a wide performed as a global consortium effort with different variety of topics [11, 12], largely due to the size of the researchers addressing different topics as subgroups of Aspergillus research community. These studies were the consortium. Where possible, experimental data were facilitated by genome resources for this genus, such as generated to examine inferences from the genomic dif- CADRE [13] and AspGD [14], in which gene curation ferences and to provide an unprecedented comparative and functional annotation of reference species were analysis of variation and functional specialization within de Vries et al. Genome Biology (2017) 18:28 Page 3 of 45 a fungal genus. The paper is organized in topic based A genome-wide phylogenetic analysis was conducted sections, covering: to determine the relationship between the newly se- quenced genomes and other related species present in – General comparison of the genomes and MycoCosm. This resulted in a highly supported phy- phylogenomics logram providing insights into taxonomic relation- – Asexual and sexual reproduction ships within Aspergillus and between Aspergillus and – Primary carbon catabolism related genera. With the introduction of the single – Plant biomass degradation name nomenclature for fungal anamorph and teleo- – Secondary metabolism morph forms, there is discussion over whether to split – Stress response Aspergillus or to maintain the genus as one. One ar- – Transporters gument for splitting is the indication that the genus – Flavohemoglobins and nitric oxide
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