Unraveling the regulation of sugar beet pulp utilization in the industrially relevant fungus Aspergillus niger

Sandra Garrigues; Roland S. Kun; Mao Peng; Diane Bauer; Keykhosrow Keymanesh; Anna Lipzen; Vivian Ng; Igor V. Grigoriev; Ronald P. de Vries

doi:10.1016/j.isci.2022.104065

Unraveling the regulation of sugar beet pulp utilization in the industrially relevant fungus Aspergillus niger

Sandra Garrigues, Roland S. Kun, Mao Peng, Diane Bauer, Keykhosrow Keymanesh, Anna Lipzen, Vivian Ng, Igor V. Grigoriev, Ronald P. de Vries^*

^*Corresponding author for this work

Molecular Plant Physiology

Research output: Contribution to journal › Article › Academic › peer-review

Abstract

Efficient utilization of agro-industrial waste, such as sugar beet pulp, is crucial for the bio-based economy. The fungus Aspergillus niger possesses a wide array of enzymes that degrade complex plant biomass substrates, and several regulators have been reported to play a role in their production. The role of the regulators GaaR, AraR, and RhaR in sugar beet pectin degradation has previously been reported. However, genetic regulation of the degradation of sugar beet pulp has not been assessed in detail. In this study, we generated a set of single and combinatorial deletion mutants targeting the pectinolytic regulators GaaR, AraR, RhaR, and GalX as well as the (hemi-)cellulolytic regulators XlnR and ClrB to address their relative contribution to the utilization of sugar beet pulp. We show that A. niger has a flexible regulatory network, adapting to the utilization of (hemi-)cellulose at early timepoints when pectin degradation is impaired.

Original language	English
Article number	104065
Number of pages	20
Journal	iScience
Volume	25
Issue number	4
DOIs	https://doi.org/10.1016/j.isci.2022.104065
Publication status	Published - 15 Apr 2022

Bibliographical note

Funding Information:
The authors acknowledge Prof. Adrian Tsang (Concordia University, Montreal, Canada) who provided the ANEp8-Cas9-pyrG plasmid. RSK and SG were supported by a grant of the Applied Science Division (TTW) of NWO and the Biotechnology and Safety Program of the Ministry of Infrastructure and Water Management 15807 to R.P.dV. The work (proposal: 10.46936/fics.proj.2018.50379/60006403) conducted by the U.S. Department of Energy Joint Genome Institute (https://ror.org/04xm1d337), a DOE Office of Science User Facility, is supported by the Office of Science of the U.S. Department of Energy operated under Contract No. DE-AC02-05CH11231. S.G. and R.S.K. performed the experiments, analyzed the data, and wrote the original manuscript. D.B. K.K. A.L. and V.N. performed the RNA sequencing and initial analysis. I.V.G. supervised the RNA sequencing. M.P. contributed to the bioinformatics analysis. R.P.dV. designed the experiments, supervised the research, and reviewed and edited the manuscript. All authors commented on and approved the submitted manuscript. The authors declare no competing interests.

Funding Information:
The authors acknowledge Prof. Adrian Tsang (Concordia University, Montreal, Canada) who provided the ANEp8-Cas9-pyrG plasmid. RSK and SG were supported by a grant of the Applied Science Division (TTW) of NWO and the Biotechnology and Safety Program of the Ministry of Infrastructure and Water Management 15807 to R.P.dV.

Funding Information:
The work (proposal: 10.46936/fics.proj.2018.50379/60006403) conducted by the U.S. Department of Energy Joint Genome Institute ( https://ror.org/04xm1d337 ), a DOE Office of Science User Facility, is supported by the Office of Science of the U.S. Department of Energy operated under Contract No. DE-AC02-05CH11231 .

Publisher Copyright:
© 2022 The Author(s)

Funding

The authors acknowledge Prof. Adrian Tsang (Concordia University, Montreal, Canada) who provided the ANEp8-Cas9-pyrG plasmid. RSK and SG were supported by a grant of the Applied Science Division (TTW) of NWO and the Biotechnology and Safety Program of the Ministry of Infrastructure and Water Management 15807 to R.P.dV. The work (proposal: 10.46936/fics.proj.2018.50379/60006403) conducted by the U.S. Department of Energy Joint Genome Institute (https://ror.org/04xm1d337), a DOE Office of Science User Facility, is supported by the Office of Science of the U.S. Department of Energy operated under Contract No. DE-AC02-05CH11231. S.G. and R.S.K. performed the experiments, analyzed the data, and wrote the original manuscript. D.B. K.K. A.L. and V.N. performed the RNA sequencing and initial analysis. I.V.G. supervised the RNA sequencing. M.P. contributed to the bioinformatics analysis. R.P.dV. designed the experiments, supervised the research, and reviewed and edited the manuscript. All authors commented on and approved the submitted manuscript. The authors declare no competing interests. The authors acknowledge Prof. Adrian Tsang (Concordia University, Montreal, Canada) who provided the ANEp8-Cas9-pyrG plasmid. RSK and SG were supported by a grant of the Applied Science Division (TTW) of NWO and the Biotechnology and Safety Program of the Ministry of Infrastructure and Water Management 15807 to R.P.dV. The work (proposal: 10.46936/fics.proj.2018.50379/60006403) conducted by the U.S. Department of Energy Joint Genome Institute ( https://ror.org/04xm1d337 ), a DOE Office of Science User Facility, is supported by the Office of Science of the U.S. Department of Energy operated under Contract No. DE-AC02-05CH11231 .

Keywords

Microbial metabolism
Mycology

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PIIS2589004222003352Final published version, 5.18 MBLicence: CC BY

Cite this

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title = "Unraveling the regulation of sugar beet pulp utilization in the industrially relevant fungus Aspergillus niger",

abstract = "Efficient utilization of agro-industrial waste, such as sugar beet pulp, is crucial for the bio-based economy. The fungus Aspergillus niger possesses a wide array of enzymes that degrade complex plant biomass substrates, and several regulators have been reported to play a role in their production. The role of the regulators GaaR, AraR, and RhaR in sugar beet pectin degradation has previously been reported. However, genetic regulation of the degradation of sugar beet pulp has not been assessed in detail. In this study, we generated a set of single and combinatorial deletion mutants targeting the pectinolytic regulators GaaR, AraR, RhaR, and GalX as well as the (hemi-)cellulolytic regulators XlnR and ClrB to address their relative contribution to the utilization of sugar beet pulp. We show that A. niger has a flexible regulatory network, adapting to the utilization of (hemi-)cellulose at early timepoints when pectin degradation is impaired.",

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author = "Sandra Garrigues and Kun, {Roland S.} and Mao Peng and Diane Bauer and Keykhosrow Keymanesh and Anna Lipzen and Vivian Ng and Grigoriev, {Igor V.} and {de Vries}, {Ronald P.}",

note = "Funding Information: The authors acknowledge Prof. Adrian Tsang (Concordia University, Montreal, Canada) who provided the ANEp8-Cas9-pyrG plasmid. RSK and SG were supported by a grant of the Applied Science Division (TTW) of NWO and the Biotechnology and Safety Program of the Ministry of Infrastructure and Water Management 15807 to R.P.dV. The work (proposal: 10.46936/fics.proj.2018.50379/60006403) conducted by the U.S. Department of Energy Joint Genome Institute (https://ror.org/04xm1d337), a DOE Office of Science User Facility, is supported by the Office of Science of the U.S. Department of Energy operated under Contract No. DE-AC02-05CH11231. S.G. and R.S.K. performed the experiments, analyzed the data, and wrote the original manuscript. D.B. K.K. A.L. and V.N. performed the RNA sequencing and initial analysis. I.V.G. supervised the RNA sequencing. M.P. contributed to the bioinformatics analysis. R.P.dV. designed the experiments, supervised the research, and reviewed and edited the manuscript. All authors commented on and approved the submitted manuscript. The authors declare no competing interests. Funding Information: The authors acknowledge Prof. Adrian Tsang (Concordia University, Montreal, Canada) who provided the ANEp8-Cas9-pyrG plasmid. RSK and SG were supported by a grant of the Applied Science Division (TTW) of NWO and the Biotechnology and Safety Program of the Ministry of Infrastructure and Water Management 15807 to R.P.dV. Funding Information: The work (proposal: 10.46936/fics.proj.2018.50379/60006403) conducted by the U.S. Department of Energy Joint Genome Institute ( https://ror.org/04xm1d337 ), a DOE Office of Science User Facility, is supported by the Office of Science of the U.S. Department of Energy operated under Contract No. DE-AC02-05CH11231 . Publisher Copyright: {\textcopyright} 2022 The Author(s)",

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AU - Kun, Roland S.

AU - Peng, Mao

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AU - Keymanesh, Keykhosrow

AU - Lipzen, Anna

AU - Ng, Vivian

AU - Grigoriev, Igor V.

AU - de Vries, Ronald P.

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Unraveling the regulation of sugar beet pulp utilization in the industrially relevant fungus Aspergillus niger

Abstract

Bibliographical note

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Keywords

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