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

Ronald P. de Vries, Robert Riley, Ad Wiebenga, Guillermo Aguilar-Osorio, Sotiris Amillis, Cristiane Akemi Uchima, Gregor Anderluh, Mojtaba Asadollahi, Marion Askin, Kerrie Barry, Evy Battaglia, Özgür Bayram, Tiziano Benocci, Susanna A. Braus-Stromeyer, Camila Caldana, David Cánovas, Gustavo C. Cerqueira, Fusheng Chen, Wanping Chen, Cindy Choi, Alicia Clum, Renato Augusto Corrêa dos Santos, André Ricardo de Lima Damásio, George Diallinas, Tamás Emri, Erzsébet Fekete, Michel Flipphi, Susanne Freyberg, Antonia Gallo, Christos Gournas, Rob Habgood, Matthieu Hainaut, María Laura Harispe, Bernard Henrissat, Kristiina S. Hildén, Ryan Hope, Abeer Hossain, Eugenia Karabika, Levente Karaffa, Zsolt Karányi, Nada Kraševec, Alan Kuo, Harald Kusch, Kurt LaButti, Ellen L. Lagendijk, Alla Lapidus, Anthony Levasseur, Erika Lindquist, Anna Lipzen, Antonio F. Logrieco, Andrew MacCabe, Miia R. Mäkelä, Iran Malavazi, Petter Melin, Vera Meyer, Natalia Mielnichuk, Márton Miskei, Ákos P. Molnár, Giuseppina Mulé, Chew Yee Ngan, Margarita Orejas, Erzsébet Orosz, Jean Paul Ouedraogo, Karin M. Overkamp, Hee-Soo Park, Giancarlo Perrone, Francois Piumi, Peter J. Punt, Arthur F. J. Ram, Ana Ramón, Stefan Rauscher, Eric Record, Diego Mauricio Riaño-Pachón, Vincent Robert, Julian Röhrig, Roberto Ruller, Asaf Salamov, Nadhira S. Salih, Rob A. Samson, Erzsébet Sándor, Manuel Sanguinetti, Tabea Schütze, Kristina Sepčić, Ekaterina Shelest, Gavin Sherlock, Vicky Sophianopoulou, Fabio M. Squina, Hui Sun, Antonia Susca, Richard B. Todd, Adrian Tsang, Shiela E. Unkles, Nathalie van de Wiele, Diana van Rossen-Uffink, Juliana Velasco de Castro Oliveira, Tammi C. Vesth, Jaap Visser, Jae-Hyuk Yu, Miaomiao Zhou, Mikael R. Andersen, David B. Archer, Scott E. Baker, Isabelle Benoit, Axel A. Brakhage, Gerhard H. Braus, Reinhard Fischer, Jens C. Frisvad, Gustavo H. Goldman, Jos Houbraken, Berl Oakley, István Pócsi, Claudio Scazzocchio, Bernhard Seiboth, Patricia A. vanKuyk, Jennifer Wortman, Paul S. Dyer, Igor V. Grigoriev

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. 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. 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.