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Title: Succession of physiological stages hallmarks the transcriptomic response of the fungus Aspergillus niger to lignocellulose

Abstract

Background: Understanding how fungi degrade lignocellulose is a cornerstone of improving renewables-based biotechnology, in particular for the production of hydrolytic enzymes. Considerable progress has been made in investigating fungal degradation during time-points where CAZyme expression peaks. However, a robust understanding of the fungal survival strategies over its life time on lignocellulose is thereby missed. Here we aimed to uncover the physiological responses of the biotechnological workhorse and enzyme producer Aspergillus niger over its life time to six substrates important for biofuel production. Results: We analysed the response of A. niger to the feedstock Miscanthus and compared it with our previous study on wheat straw, alone or in combination with hydrothermal or ionic liquid feedstock pretreatments. Conserved (substrate-independent) metabolic responses as well as those affected by pretreatment and feedstock were identified via multivariate analysis of genome-wide transcriptomics combined with targeted transcript and protein analyses and mapping to a metabolic model. Initial exposure to all substrates increased fatty acid beta-oxidation and lipid metabolism transcripts. In a strain carrying a deletion of the ortholog of the Aspergillus nidulans fatty acid beta-oxidation transcriptional regulator farA, there was a reduction in expression of selected lignocellulose degradative CAZyme-encoding genes suggesting that beta-oxidation contributes to adaptation tomore » lignocellulose. Mannan degradation expression was wheat straw feedstock-dependent and pectin degradation was higher on the untreated substrates. In the later life stages, known and novel secondary metabolite gene clusters were activated, which are of high interest due to their potential to synthesize bioactive compounds. Conclusion: In this study, which includes the first transcriptional response of Aspergilli to Miscanthus, we highlighted that life time as well as substrate composition and structure (via variations in pretreatment and feedstock) influence the fungal responses to lignocellulose. We also demonstrated that the fungal response contains physiological stages that are conserved across substrates and are typically found outside of the conditions with high CAZyme expression, as exemplified by the stages that are dominated by lipid and secondary metabolism.« less

Authors:
ORCiD logo; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; more »; « less
Publication Date:
Research Org.:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC); Netherlands Scientific Organization
OSTI Identifier:
1618778
Alternate Identifier(s):
OSTI ID: 1619151
Grant/Contract Number:  
AC02-05CH11231; NWO 824.15.023
Resource Type:
Published Article
Journal Name:
Biotechnology for Biofuels
Additional Journal Information:
Journal Name: Biotechnology for Biofuels Journal Volume: 13 Journal Issue: 1; Journal ID: ISSN 1754-6834
Publisher:
BioMed Central
Country of Publication:
Netherlands
Language:
English
Subject:
09 BIOMASS FUELS; Aspergillys niger; Lignocellulose; pretreatment; system analysis; CASymes; metabolism; fatty acids beta-oxidation; forA; secondary metabolism

Citation Formats

van Munster, Jolanda M., Daly, Paul, Blythe, Martin J., Ibbett, Roger, Kokolski, Matt, Gaddipati, Sanyasi, Lindquist, Erika, Singan, Vasanth R., Barry, Kerrie W., Lipzen, Anna, Ngan, Chew Yee, Petzold, Christopher J., Chan, Leanne Jade G., Arvas, Mikko, Raulo, Roxane, Pullan, Steven T., Delmas, Stéphane, Grigoriev, Igor V., Tucker, Gregory A., Simmons, Blake A., and Archer, David B. Succession of physiological stages hallmarks the transcriptomic response of the fungus Aspergillus niger to lignocellulose. Netherlands: N. p., 2020. Web. doi:10.1186/s13068-020-01702-2.
van Munster, Jolanda M., Daly, Paul, Blythe, Martin J., Ibbett, Roger, Kokolski, Matt, Gaddipati, Sanyasi, Lindquist, Erika, Singan, Vasanth R., Barry, Kerrie W., Lipzen, Anna, Ngan, Chew Yee, Petzold, Christopher J., Chan, Leanne Jade G., Arvas, Mikko, Raulo, Roxane, Pullan, Steven T., Delmas, Stéphane, Grigoriev, Igor V., Tucker, Gregory A., Simmons, Blake A., & Archer, David B. Succession of physiological stages hallmarks the transcriptomic response of the fungus Aspergillus niger to lignocellulose. Netherlands. https://doi.org/10.1186/s13068-020-01702-2
van Munster, Jolanda M., Daly, Paul, Blythe, Martin J., Ibbett, Roger, Kokolski, Matt, Gaddipati, Sanyasi, Lindquist, Erika, Singan, Vasanth R., Barry, Kerrie W., Lipzen, Anna, Ngan, Chew Yee, Petzold, Christopher J., Chan, Leanne Jade G., Arvas, Mikko, Raulo, Roxane, Pullan, Steven T., Delmas, Stéphane, Grigoriev, Igor V., Tucker, Gregory A., Simmons, Blake A., and Archer, David B. Mon . "Succession of physiological stages hallmarks the transcriptomic response of the fungus Aspergillus niger to lignocellulose". Netherlands. https://doi.org/10.1186/s13068-020-01702-2.
@article{osti_1618778,
title = {Succession of physiological stages hallmarks the transcriptomic response of the fungus Aspergillus niger to lignocellulose},
author = {van Munster, Jolanda M. and Daly, Paul and Blythe, Martin J. and Ibbett, Roger and Kokolski, Matt and Gaddipati, Sanyasi and Lindquist, Erika and Singan, Vasanth R. and Barry, Kerrie W. and Lipzen, Anna and Ngan, Chew Yee and Petzold, Christopher J. and Chan, Leanne Jade G. and Arvas, Mikko and Raulo, Roxane and Pullan, Steven T. and Delmas, Stéphane and Grigoriev, Igor V. and Tucker, Gregory A. and Simmons, Blake A. and Archer, David B.},
abstractNote = {Background: Understanding how fungi degrade lignocellulose is a cornerstone of improving renewables-based biotechnology, in particular for the production of hydrolytic enzymes. Considerable progress has been made in investigating fungal degradation during time-points where CAZyme expression peaks. However, a robust understanding of the fungal survival strategies over its life time on lignocellulose is thereby missed. Here we aimed to uncover the physiological responses of the biotechnological workhorse and enzyme producer Aspergillus niger over its life time to six substrates important for biofuel production. Results: We analysed the response of A. niger to the feedstock Miscanthus and compared it with our previous study on wheat straw, alone or in combination with hydrothermal or ionic liquid feedstock pretreatments. Conserved (substrate-independent) metabolic responses as well as those affected by pretreatment and feedstock were identified via multivariate analysis of genome-wide transcriptomics combined with targeted transcript and protein analyses and mapping to a metabolic model. Initial exposure to all substrates increased fatty acid beta-oxidation and lipid metabolism transcripts. In a strain carrying a deletion of the ortholog of the Aspergillus nidulans fatty acid beta-oxidation transcriptional regulator farA, there was a reduction in expression of selected lignocellulose degradative CAZyme-encoding genes suggesting that beta-oxidation contributes to adaptation to lignocellulose. Mannan degradation expression was wheat straw feedstock-dependent and pectin degradation was higher on the untreated substrates. In the later life stages, known and novel secondary metabolite gene clusters were activated, which are of high interest due to their potential to synthesize bioactive compounds. Conclusion: In this study, which includes the first transcriptional response of Aspergilli to Miscanthus, we highlighted that life time as well as substrate composition and structure (via variations in pretreatment and feedstock) influence the fungal responses to lignocellulose. We also demonstrated that the fungal response contains physiological stages that are conserved across substrates and are typically found outside of the conditions with high CAZyme expression, as exemplified by the stages that are dominated by lipid and secondary metabolism.},
doi = {10.1186/s13068-020-01702-2},
journal = {Biotechnology for Biofuels},
number = 1,
volume = 13,
place = {Netherlands},
year = {Mon Apr 13 00:00:00 EDT 2020},
month = {Mon Apr 13 00:00:00 EDT 2020}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record
https://doi.org/10.1186/s13068-020-01702-2

Citation Metrics:
Cited by: 4 works
Citation information provided by
Web of Science

Figures / Tables:

Fig. 1 Fig. 1: Schematic representation of experimental setup. a A. niger was cultivated in shake flasks with glucose as carbon source, after which mycelium was transferred to shake flask containing either knife milled Miscanthus (KMM), or KMM pretreated with ionic liquid (ILM) or hydrothermal treatment (HTM). Mycelium was harvested at indicatedmore » time points after which RNA was isolated and sequenced. This dataset was compared to data obtained with a similar experiment b using knife milled wheat straw (KMS) and pretreated straw (ILS, HTS). b is reproduced from [31] under a CC BY ((https ://creat iveco mmons .org/licen ses/by/4.0/) license« less

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