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

Ronald P. de Vries (Corresponding Author), Robert Riley, Ad Wiebenga, Guillermo Aguilar-Osorio, Sotiris Amillis, Christiane Akemi Uchima, Gregor Anderluh, Mojtaba Asadollahi, Marion Askin, Kerrie Barry, Evy Battaglia, Özgür Bayram, Tiziano Benocci, Susann A. Braus-Stromeyer, Camila Caldana, David Cánovas, Gustavo C. Cerqueira, Fusheng Chen, Wanping Chen, Cindy ChoiAlicia 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, Erszébet 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, Erszébet 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

    Research output: Contribution to journalArticleScientificpeer-review

    101 Citations (Scopus)

    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.
    Original languageEnglish
    Article number28
    Number of pages45
    JournalGenome Biology
    Volume18
    Issue number1
    DOIs
    Publication statusPublished - 2017
    MoE publication typeA1 Journal article-refereed

    Fingerprint

    Biodiversity
    Aspergillus
    Genomics
    genomics
    genome
    Genome
    biodiversity
    Biomass
    stress response
    experimental study
    Secondary Metabolism
    Biological Sciences
    Genetic Models
    industrial applications
    biomass
    food contamination
    organic acid
    organic acids and salts
    signal transduction
    phenotype

    Keywords

    • aspergillus
    • comparative genomics
    • fungal biology
    • genome sequencing

    Cite this

    de Vries, R. P., Riley, R., Wiebenga, A., Aguilar-Osorio, G., Amillis, S., Uchima, C. A., ... Grigoriev, I. V. (2017). Comparative genomics reveals high biological diversity and specific adaptations in the industrially and medically important fungal genus Aspergillus. Genome Biology, 18(1), [28]. https://doi.org/10.1186/s13059-017-1151-0
    de Vries, Ronald P. ; Riley, Robert ; Wiebenga, Ad ; Aguilar-Osorio, Guillermo ; Amillis, Sotiris ; Uchima, Christiane Akemi ; Anderluh, Gregor ; Asadollahi, Mojtaba ; Askin, Marion ; Barry, Kerrie ; Battaglia, Evy ; Bayram, Özgür ; Benocci, Tiziano ; Braus-Stromeyer, Susann A. ; Caldana, Camila ; Cánovas, David ; Cerqueira, Gustavo C. ; Chen, Fusheng ; Chen, Wanping ; Choi, Cindy ; Clum, Alicia ; dos Santos, Renato Augusto Corrêa ; de Lima Damásio, André Ricardo ; Diallinas, George ; Emri, Tamás ; Fekete, Erzsébet ; Flipphi, Michel ; Freyberg, Susanne ; Gallo, Antonia ; Gournas, Christos ; Habgood, Rob ; Hainaut, Matthieu ; Harispe, María Laura ; Henrissat, Bernard ; Hildén, Kristiina S. ; Hope, Ryan ; Hossain, Abeer ; Karabika, Eugenia ; Karaffa, Levente ; Karányi, Zsolt ; Kraševec, Nada ; Kuo, Alan ; Kusch, Harald ; LaButti, Kurt ; Lagendijk, Ellen L. ; Lapidus, Alla ; Levasseur, Anthony ; Lindquist, Erika ; Lipzen, Anna ; Logrieco, Antonio F. ; MacCabe, Andrew ; Mäkelä, Miia R. ; Malavazi, Iran ; Melin, Petter ; Meyer, Vera ; Mielnichuk, Natalia ; Miskei, Márton ; Molnár, Ákos P. ; Mulé, Giuseppina ; Ngan, Chew Yee ; Orejas, Margarita ; Orosz, Erszébet ; Ouedraogo, Jean Paul ; Overkamp, Karin M. ; Park, Hee-Soo ; Perrone, Giancarlo ; Piumi, Francois ; Punt, Peter J. ; Ram, Arthur F.J. ; Ramón, Ana ; Rauscher, Stefan ; Record, Eric ; Riaño-Pachón, Diego Mauricio ; Robert, Vincent ; Röhrig, Julian ; Ruller, Roberto ; Salamov, Asaf ; Salih, Nadhira S. ; Samson, Rob A. ; Sándor, Erszébet ; Sanguinetti, Manuel ; Schütze, Tabea ; Sepčić, Kristina ; Shelest, Ekaterina ; Sherlock, Gavin ; Sophianopoulou, Vicky ; Squina, Fabio M. ; Sun, Hui ; Susca, Antonia ; Todd, Richard B. ; Tsang, Adrian ; Unkles, Shiela E. ; van de Wiele, Nathalie ; van Rossen-Uffink, Diana ; de Castro Oliveira, Juliana Velasco ; Vesth, Tammi C. ; Visser, Jaap ; Yu, Jae-Hyuk ; Zhou, Miaomiao ; Andersen, Mikael R. ; Archer, David B. ; Baker, Scott E. ; Benoit, Isabelle ; Brakhage, Axel A. ; Braus, Gerhard H. ; Fischer, Reinhard ; Frisvad, Jens C. ; Goldman, Gustavo H. ; Houbraken, Jos ; Oakley, Berl ; Pócsi, István ; Scazzocchio, Claudio ; Seiboth, Bernhard ; vanKuyk, Patricia A. ; Wortman, Jennifer ; Dyer, Paul S. ; Grigoriev, Igor V. / Comparative genomics reveals high biological diversity and specific adaptations in the industrially and medically important fungal genus Aspergillus. In: Genome Biology. 2017 ; Vol. 18, No. 1.
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    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.",
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    de Vries, RP, Riley, R, Wiebenga, A, Aguilar-Osorio, G, Amillis, S, Uchima, CA, Anderluh, G, Asadollahi, M, Askin, M, Barry, K, Battaglia, E, Bayram, Ö, Benocci, T, Braus-Stromeyer, SA, Caldana, C, Cánovas, D, Cerqueira, GC, Chen, F, Chen, W, Choi, C, Clum, A, dos Santos, RAC, de Lima Damásio, AR, Diallinas, G, Emri, T, Fekete, E, Flipphi, M, Freyberg, S, Gallo, A, Gournas, C, Habgood, R, Hainaut, M, Harispe, ML, Henrissat, B, Hildén, KS, Hope, R, Hossain, A, Karabika, E, Karaffa, L, Karányi, Z, Kraševec, N, Kuo, A, Kusch, H, LaButti, K, Lagendijk, EL, Lapidus, A, Levasseur, A, Lindquist, E, Lipzen, A, Logrieco, AF, MacCabe, A, Mäkelä, MR, Malavazi, I, Melin, P, Meyer, V, Mielnichuk, N, Miskei, M, Molnár, ÁP, Mulé, G, Ngan, CY, Orejas, M, Orosz, E, Ouedraogo, JP, Overkamp, KM, Park, H-S, Perrone, G, Piumi, F, Punt, PJ, Ram, AFJ, Ramón, A, Rauscher, S, Record, E, Riaño-Pachón, DM, Robert, V, Röhrig, J, Ruller, R, Salamov, A, Salih, NS, Samson, RA, Sándor, E, Sanguinetti, M, Schütze, T, Sepčić, K, Shelest, E, Sherlock, G, Sophianopoulou, V, Squina, FM, Sun, H, Susca, A, Todd, RB, Tsang, A, Unkles, SE, van de Wiele, N, van Rossen-Uffink, D, de Castro Oliveira, JV, Vesth, TC, Visser, J, Yu, J-H, Zhou, M, Andersen, MR, Archer, DB, Baker, SE, Benoit, I, Brakhage, AA, Braus, GH, Fischer, R, Frisvad, JC, Goldman, GH, Houbraken, J, Oakley, B, Pócsi, I, Scazzocchio, C, Seiboth, B, vanKuyk, PA, Wortman, J, Dyer, PS & Grigoriev, IV 2017, 'Comparative genomics reveals high biological diversity and specific adaptations in the industrially and medically important fungal genus Aspergillus', Genome Biology, vol. 18, no. 1, 28. https://doi.org/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, Ronald P. (Corresponding Author); Riley, Robert; Wiebenga, Ad; Aguilar-Osorio, Guillermo; Amillis, Sotiris; Uchima, Christiane Akemi; Anderluh, Gregor; Asadollahi, Mojtaba; Askin, Marion; Barry, Kerrie; Battaglia, Evy; Bayram, Özgür; Benocci, Tiziano; Braus-Stromeyer, Susann A.; Caldana, Camila; Cánovas, David; Cerqueira, Gustavo C.; Chen, Fusheng; Chen, Wanping; Choi, Cindy; Clum, Alicia; dos Santos, Renato Augusto Corrêa; de Lima Damásio, André Ricardo; Diallinas, George; Emri, Tamás; Fekete, Erzsébet; Flipphi, Michel; Freyberg, Susanne; Gallo, Antonia; Gournas, Christos; Habgood, Rob; Hainaut, Matthieu; Harispe, María Laura; Henrissat, Bernard; Hildén, Kristiina S.; Hope, Ryan; Hossain, Abeer; Karabika, Eugenia; Karaffa, Levente; Karányi, Zsolt; Kraševec, Nada; Kuo, Alan; Kusch, Harald; LaButti, Kurt; Lagendijk, Ellen L.; Lapidus, Alla; Levasseur, Anthony; Lindquist, Erika; Lipzen, Anna; Logrieco, Antonio F.; MacCabe, Andrew; Mäkelä, Miia R.; Malavazi, Iran; Melin, Petter; Meyer, Vera; Mielnichuk, Natalia; Miskei, Márton; Molnár, Ákos P.; Mulé, Giuseppina; Ngan, Chew Yee; Orejas, Margarita; Orosz, Erszébet; Ouedraogo, Jean Paul; Overkamp, Karin M.; Park, Hee-Soo; Perrone, Giancarlo; Piumi, Francois; Punt, Peter J.; Ram, Arthur F.J.; Ramón, Ana; Rauscher, Stefan; Record, Eric; Riaño-Pachón, Diego Mauricio; Robert, Vincent; Röhrig, Julian; Ruller, Roberto; Salamov, Asaf; Salih, Nadhira S.; Samson, Rob A.; Sándor, Erszébet; Sanguinetti, Manuel; Schütze, Tabea; Sepčić, Kristina; Shelest, Ekaterina; Sherlock, Gavin; Sophianopoulou, Vicky; Squina, Fabio M.; Sun, Hui; Susca, Antonia; Todd, Richard B.; Tsang, Adrian; Unkles, Shiela E.; van de Wiele, Nathalie; van Rossen-Uffink, Diana; de Castro Oliveira, Juliana Velasco; Vesth, Tammi C.; Visser, Jaap; Yu, Jae-Hyuk; Zhou, Miaomiao; Andersen, Mikael R. ; Archer, David B.; Baker, Scott E.; Benoit, Isabelle; Brakhage, Axel A.; Braus, Gerhard H.; Fischer, Reinhard; Frisvad, Jens C.; Goldman, Gustavo H.; Houbraken, Jos; Oakley, Berl; Pócsi, István; Scazzocchio, Claudio; Seiboth, Bernhard; vanKuyk, Patricia A.; Wortman, Jennifer; Dyer, Paul S.; Grigoriev, Igor V.

    In: Genome Biology, Vol. 18, No. 1, 28, 2017.

    Research output: Contribution to journalArticleScientificpeer-review

    TY - JOUR

    T1 - Comparative genomics reveals high biological diversity and specific adaptations in the industrially and medically important fungal genus Aspergillus

    AU - de Vries, Ronald P.

    AU - Riley, Robert

    AU - Wiebenga, Ad

    AU - Aguilar-Osorio, Guillermo

    AU - Amillis, Sotiris

    AU - Uchima, Christiane Akemi

    AU - Anderluh, Gregor

    AU - Asadollahi, Mojtaba

    AU - Askin, Marion

    AU - Barry, Kerrie

    AU - Battaglia, Evy

    AU - Bayram, Özgür

    AU - Benocci, Tiziano

    AU - Braus-Stromeyer, Susann A.

    AU - Caldana, Camila

    AU - Cánovas, David

    AU - Cerqueira, Gustavo C.

    AU - Chen, Fusheng

    AU - Chen, Wanping

    AU - Choi, Cindy

    AU - Clum, Alicia

    AU - dos Santos, Renato Augusto Corrêa

    AU - de Lima Damásio, André Ricardo

    AU - Diallinas, George

    AU - Emri, Tamás

    AU - Fekete, Erzsébet

    AU - Flipphi, Michel

    AU - Freyberg, Susanne

    AU - Gallo, Antonia

    AU - Gournas, Christos

    AU - Habgood, Rob

    AU - Hainaut, Matthieu

    AU - Harispe, María Laura

    AU - Henrissat, Bernard

    AU - Hildén, Kristiina S.

    AU - Hope, Ryan

    AU - Hossain, Abeer

    AU - Karabika, Eugenia

    AU - Karaffa, Levente

    AU - Karányi, Zsolt

    AU - Kraševec, Nada

    AU - Kuo, Alan

    AU - Kusch, Harald

    AU - LaButti, Kurt

    AU - Lagendijk, Ellen L.

    AU - Lapidus, Alla

    AU - Levasseur, Anthony

    AU - Lindquist, Erika

    AU - Lipzen, Anna

    AU - Logrieco, Antonio F.

    AU - MacCabe, Andrew

    AU - Mäkelä, Miia R.

    AU - Malavazi, Iran

    AU - Melin, Petter

    AU - Meyer, Vera

    AU - Mielnichuk, Natalia

    AU - Miskei, Márton

    AU - Molnár, Ákos P.

    AU - Mulé, Giuseppina

    AU - Ngan, Chew Yee

    AU - Orejas, Margarita

    AU - Orosz, Erszébet

    AU - Ouedraogo, Jean Paul

    AU - Overkamp, Karin M.

    AU - Park, Hee-Soo

    AU - Perrone, Giancarlo

    AU - Piumi, Francois

    AU - Punt, Peter J.

    AU - Ram, Arthur F.J.

    AU - Ramón, Ana

    AU - Rauscher, Stefan

    AU - Record, Eric

    AU - Riaño-Pachón, Diego Mauricio

    AU - Robert, Vincent

    AU - Röhrig, Julian

    AU - Ruller, Roberto

    AU - Salamov, Asaf

    AU - Salih, Nadhira S.

    AU - Samson, Rob A.

    AU - Sándor, Erszébet

    AU - Sanguinetti, Manuel

    AU - Schütze, Tabea

    AU - Sepčić, Kristina

    AU - Shelest, Ekaterina

    AU - Sherlock, Gavin

    AU - Sophianopoulou, Vicky

    AU - Squina, Fabio M.

    AU - Sun, Hui

    AU - Susca, Antonia

    AU - Todd, Richard B.

    AU - Tsang, Adrian

    AU - Unkles, Shiela E.

    AU - van de Wiele, Nathalie

    AU - van Rossen-Uffink, Diana

    AU - de Castro Oliveira, Juliana Velasco

    AU - Vesth, Tammi C.

    AU - Visser, Jaap

    AU - Yu, Jae-Hyuk

    AU - Zhou, Miaomiao

    AU - Andersen, Mikael R.

    AU - Archer, David B.

    AU - Baker, Scott E.

    AU - Benoit, Isabelle

    AU - Brakhage, Axel A.

    AU - Braus, Gerhard H.

    AU - Fischer, Reinhard

    AU - Frisvad, Jens C.

    AU - Goldman, Gustavo H.

    AU - Houbraken, Jos

    AU - Oakley, Berl

    AU - Pócsi, István

    AU - Scazzocchio, Claudio

    AU - Seiboth, Bernhard

    AU - vanKuyk, Patricia A.

    AU - Wortman, Jennifer

    AU - Dyer, Paul S.

    AU - Grigoriev, Igor V.

    PY - 2017

    Y1 - 2017

    N2 - 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.

    AB - 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.

    KW - aspergillus

    KW - comparative genomics

    KW - fungal biology

    KW - genome sequencing

    UR - http://www.scopus.com/inward/record.url?scp=85013301401&partnerID=8YFLogxK

    U2 - 10.1186/s13059-017-1151-0

    DO - 10.1186/s13059-017-1151-0

    M3 - Article

    VL - 18

    JO - Genome Biology

    JF - Genome Biology

    SN - 1474-7596

    IS - 1

    M1 - 28

    ER -