Re-routing of Sugar Catabolism Provides a Better Insight Into Fungal Flexibility in Using Plant Biomass-Derived Monomers as Substrates
Abstract
The filamentous ascomycete Aspergillus niger has received increasing interest as a cell factory, being able to efficiently degrade plant cell wall polysaccharides as well as having an extensive metabolism to convert the released monosaccharides into value added compounds. The pentoses D-xylose and L-arabinose are the most abundant monosaccharides in plant biomass after the hexose D-glucose, being major constituents of xylan, pectin and xyloglucan. In this study, the influence of selected pentose catabolic pathway (PCP) deletion strains on growth on plant biomass and re-routing of sugar catabolism was addressed to gain a better understanding of the flexibility of this fungus in using plant biomass-derived monomers. The transcriptome, metabolome and proteome response of three PCP mutant strains, ΔlarAΔxyrAΔxyrB, ΔladAΔxdhAΔsdhA and ΔxkiA, grown on wheat bran (WB) and sugar beet pulp (SBP), was evaluated. Our results showed that despite the absolute impact of these PCP mutations on pure pentose sugars, they are not as critical for growth of A. niger on more complex biomass substrates, such as WB and SBP. However, significant phenotypic variation was observed between the two biomass substrates, but also between the different PCP mutants. This shows that the high sugar heterogeneity of these substrates in combination with the highmore »
- Authors:
-
- Univ. of Utrecht (Netherlands)
- Pacific Northwest National Lab. (PNNL), Richland, WA (United States)
- Univ. of Utrecht (Netherlands); Univ. of Helsinki (Finland)
- Publication Date:
- Research Org.:
- Pacific Northwest National Lab. (PNNL), Richland, WA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER); Academy of Finland
- OSTI Identifier:
- 1785530
- Report Number(s):
- PNNL-SA-158642
Journal ID: ISSN 2296-4185
- Grant/Contract Number:
- AC05-76RL01830; 308284
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Frontiers in Bioengineering and Biotechnology
- Additional Journal Information:
- Journal Volume: 9; Journal ID: ISSN 2296-4185
- Publisher:
- Frontiers Research Foundation
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; lignocellulosic substrates; pentose catabolic pathway; D-galacturonic acid catabolic pathway; L-rhamnose catabolic pathway; wheat bran; sugar beet pulp; CAZymes; Aspergillus niger
Citation Formats
Chroumpi, Tania, Peng, Mao, Markillie, Lye Meng, Mitchell, Hugh D., Nicora, Carrie D., Hutchinson, Chelsea M., Paurus, Vanessa L., Tolic, Nikola, Clendinen, Chaevien S., Orr, Galya, Baker, Scott E., Makela, Miia, and de Vries, Ronald P. Re-routing of Sugar Catabolism Provides a Better Insight Into Fungal Flexibility in Using Plant Biomass-Derived Monomers as Substrates. United States: N. p., 2021.
Web. doi:10.3389/fbioe.2021.644216.
Chroumpi, Tania, Peng, Mao, Markillie, Lye Meng, Mitchell, Hugh D., Nicora, Carrie D., Hutchinson, Chelsea M., Paurus, Vanessa L., Tolic, Nikola, Clendinen, Chaevien S., Orr, Galya, Baker, Scott E., Makela, Miia, & de Vries, Ronald P. Re-routing of Sugar Catabolism Provides a Better Insight Into Fungal Flexibility in Using Plant Biomass-Derived Monomers as Substrates. United States. https://doi.org/10.3389/fbioe.2021.644216
Chroumpi, Tania, Peng, Mao, Markillie, Lye Meng, Mitchell, Hugh D., Nicora, Carrie D., Hutchinson, Chelsea M., Paurus, Vanessa L., Tolic, Nikola, Clendinen, Chaevien S., Orr, Galya, Baker, Scott E., Makela, Miia, and de Vries, Ronald P. Mon .
"Re-routing of Sugar Catabolism Provides a Better Insight Into Fungal Flexibility in Using Plant Biomass-Derived Monomers as Substrates". United States. https://doi.org/10.3389/fbioe.2021.644216. https://www.osti.gov/servlets/purl/1785530.
@article{osti_1785530,
title = {Re-routing of Sugar Catabolism Provides a Better Insight Into Fungal Flexibility in Using Plant Biomass-Derived Monomers as Substrates},
author = {Chroumpi, Tania and Peng, Mao and Markillie, Lye Meng and Mitchell, Hugh D. and Nicora, Carrie D. and Hutchinson, Chelsea M. and Paurus, Vanessa L. and Tolic, Nikola and Clendinen, Chaevien S. and Orr, Galya and Baker, Scott E. and Makela, Miia and de Vries, Ronald P.},
abstractNote = {The filamentous ascomycete Aspergillus niger has received increasing interest as a cell factory, being able to efficiently degrade plant cell wall polysaccharides as well as having an extensive metabolism to convert the released monosaccharides into value added compounds. The pentoses D-xylose and L-arabinose are the most abundant monosaccharides in plant biomass after the hexose D-glucose, being major constituents of xylan, pectin and xyloglucan. In this study, the influence of selected pentose catabolic pathway (PCP) deletion strains on growth on plant biomass and re-routing of sugar catabolism was addressed to gain a better understanding of the flexibility of this fungus in using plant biomass-derived monomers. The transcriptome, metabolome and proteome response of three PCP mutant strains, ΔlarAΔxyrAΔxyrB, ΔladAΔxdhAΔsdhA and ΔxkiA, grown on wheat bran (WB) and sugar beet pulp (SBP), was evaluated. Our results showed that despite the absolute impact of these PCP mutations on pure pentose sugars, they are not as critical for growth of A. niger on more complex biomass substrates, such as WB and SBP. However, significant phenotypic variation was observed between the two biomass substrates, but also between the different PCP mutants. This shows that the high sugar heterogeneity of these substrates in combination with the high complexity and adaptability of the fungal sugar metabolism allow for activation of alternative strategies to support growth.},
doi = {10.3389/fbioe.2021.644216},
journal = {Frontiers in Bioengineering and Biotechnology},
number = ,
volume = 9,
place = {United States},
year = {Mon Mar 08 00:00:00 EST 2021},
month = {Mon Mar 08 00:00:00 EST 2021}
}
Works referenced in this record:
L-Arabinose and D-Xylose Catabolism in Aspergillus niger
journal, August 1989
- Witteveen, C. F. B.; Busink, R.; Van De Vondervoort, P.
- Microbiology, Vol. 135, Issue 8
Two Cellobiohydrolase-Encoding Genes from Aspergillus niger Require d-Xylose and the Xylanolytic Transcriptional Activator XlnR for Their Expression
journal, January 1999
- Gielkens, Marco M. C.; Dekkers, Ester; Visser, Jaap
- Applied and Environmental Microbiology, Vol. 65, Issue 10
Hemicelluloses
journal, June 2010
- Scheller, Henrik Vibe; Ulvskov, Peter
- Annual Review of Plant Biology, Vol. 61, Issue 1
Expression-based clustering of CAZyme-encoding genes of Aspergillus niger
journal, November 2017
- Gruben, Birgit S.; Mäkelä, Miia R.; Kowalczyk, Joanna E.
- BMC Genomics, Vol. 18, Issue 1
DAnTE: a statistical tool for quantitative analysis of -omics data
journal, May 2008
- Polpitiya, A. D.; Qian, W. -J.; Jaitly, N.
- Bioinformatics, Vol. 24, Issue 13
Identification of a gene encoding the last step of the L-rhamnose catabolic pathway in Aspergillus niger revealed the inducer of the pathway regulator
journal, April 2020
- Chroumpi, Tania; Aguilar-Pontes, Maria Victoria; Peng, Mao
- Microbiological Research, Vol. 234
CreA modulates the XlnR-induced expression on xylose of Aspergillus niger genes involved in xylan degradation
journal, May 1999
- P. de Vries, Ronald; Visser, Jaap; de Graaff, Leo H.
- Research in Microbiology, Vol. 150, Issue 4
HTSeq--a Python framework to work with high-throughput sequencing data
journal, September 2014
- Anders, S.; Pyl, P. T.; Huber, W.
- Bioinformatics, Vol. 31, Issue 2
Analysis of regulation of pentose utilisation in Aspergillus niger reveals evolutionary adaptations in Eurotiales
journal, June 2011
- Battaglia, E.; Visser, L.; Nijssen, A.
- Studies in Mycology, Vol. 69
The carbohydrate-active enzymes database (CAZy) in 2013
journal, November 2013
- Lombard, Vincent; Golaconda Ramulu, Hemalatha; Drula, Elodie
- Nucleic Acids Research, Vol. 42, Issue D1
NCBI GEO: archive for functional genomics data sets—update
journal, November 2012
- Barrett, Tanya; Wilhite, Stephen E.; Ledoux, Pierre
- Nucleic Acids Research, Vol. 41, Issue D1
Regulation of Aspergillus genes encoding plant cell wall polysaccharide-degrading enzymes; relevance for industrial production
journal, March 2003
- de Vries, R.
- Applied Microbiology and Biotechnology, Vol. 61, Issue 1
Regulation of the α-glucuronidase-encoding gene ( aguA ) from Aspergillus niger
journal, September 2002
- Vries, R. de; Vondervoort, P. van de; L., Hendriks
- Molecular Genetics and Genomics, Vol. 268, Issue 1
Differential Expression of Three α-Galactosidase Genes and a Single β-Galactosidase Gene from Aspergillus niger
journal, June 1999
- de Vries, Ronald P.; van den Broeck, Hetty C.; Dekkers, Ester
- Applied and Environmental Microbiology, Vol. 65, Issue 6
FiehnLib: Mass Spectral and Retention Index Libraries for Metabolomics Based on Quadrupole and Time-of-Flight Gas Chromatography/Mass Spectrometry
journal, December 2009
- Kind, Tobias; Wohlgemuth, Gert; Lee, Do Yup
- Analytical Chemistry, Vol. 81, Issue 24
MPLEx: a Robust and Universal Protocol for Single-Sample Integrative Proteomic, Metabolomic, and Lipidomic Analyses
journal, May 2016
- Nakayasu, Ernesto S.; Nicora, Carrie D.; Sims, Amy C.
- mSystems, Vol. 1, Issue 3
Aspergillus Enzymes Involved in Degradation of Plant Cell Wall Polysaccharides
journal, December 2001
- de Vries, R. P.; Visser, J.
- Microbiology and Molecular Biology Reviews, Vol. 65, Issue 4
Closely related fungi employ diverse enzymatic strategies to degrade plant biomass
journal, August 2015
- Benoit, Isabelle; Culleton, Helena; Zhou, Miaomiao
- Biotechnology for Biofuels, Vol. 8, Issue 1
Revisiting a ‘simple’ fungal metabolic pathway reveals redundancy, complexity and diversity
journal, March 2021
- Chroumpi, Tania; Peng, Mao; Aguilar‐Pontes, Maria Victoria
- Microbial Biotechnology
Chemically Etched Open Tubular and Monolithic Emitters for Nanoelectrospray Ionization Mass Spectrometry
journal, November 2006
- Kelly, Ryan T.; Page, Jason S.; Luo, Quanzhou
- Analytical Chemistry, Vol. 78, Issue 22, p. 7796-7801
The gold-standard genome of Aspergillus niger NRRL 3 enables a detailed view of the diversity of sugar catabolism in fungi
journal, September 2018
- Aguilar-Pontes, M. V.; Brandl, J.; McDonnell, E.
- Studies in Mycology, Vol. 91
Metabolomics by Gas Chromatography–Mass Spectrometry: Combined Targeted and Untargeted Profiling
journal, April 2016
- Fiehn, Oliver
- Current Protocols in Molecular Biology, Vol. 114, Issue 1
Cellulose Synthesis in Higher Plants
journal, November 2006
- Somerville, Chris
- Annual Review of Cell and Developmental Biology, Vol. 22, Issue 1
Spectral Probabilities and Generating Functions of Tandem Mass Spectra: A Strike against Decoy Databases
journal, August 2008
- Kim, Sangtae; Gupta, Nitin; Pevzner, Pavel A.
- Journal of Proteome Research, Vol. 7, Issue 8
Regulation of pentose utilisation by AraR, but not XlnR, differs in Aspergillus nidulans and Aspergillus niger
journal, April 2011
- Battaglia, Evy; Hansen, Sara Fasmer; Leendertse, Anne
- Applied Microbiology and Biotechnology, Vol. 91, Issue 2
An evolutionary conserved d-galacturonic acid metabolic pathway operates across filamentous fungi capable of pectin degradation
journal, November 2008
- Martens-Uzunova, Elena S.; Schaap, Peter J.
- Fungal Genetics and Biology, Vol. 45, Issue 11
The pathway intermediate 2-keto-3-deoxy-L-galactonate mediates the induction of genes involved in D-galacturonic acid utilization in Aspergillus niger
journal, May 2017
- Alazi, Ebru; Khosravi, Claire; Homan, Tim G.
- FEBS Letters, Vol. 591, Issue 10
Blocking hexose entry into glycolysis activates alternative metabolic conversion of these sugars and upregulates pentose metabolism in Aspergillus nidulans
journal, March 2018
- Khosravi, Claire; Battaglia, Evy; Kun, Roland S.
- BMC Genomics, Vol. 19, Issue 1
In vivo functional analysis of L-rhamnose metabolic pathway in Aspergillus niger: a tool to identify the potential inducer of RhaR
journal, November 2017
- Khosravi, Claire; Kun, Roland Sándor; Visser, Jaap
- BMC Microbiology, Vol. 17, Issue 1
Highly efficient gene targeting in the Aspergillus niger kusA mutant
journal, March 2007
- Meyer, Vera; Arentshorst, Mark; El-Ghezal, Aymen
- Journal of Biotechnology, Vol. 128, Issue 4
Fungal arabinan and l-arabinose metabolism
journal, January 2011
- Seiboth, Bernhard; Metz, Benjamin
- Applied Microbiology and Biotechnology, Vol. 89, Issue 6
Improving cellulase production by Aspergillus niger using adaptive evolution
journal, February 2016
- Patyshakuliyeva, Aleksandrina; Arentshorst, Mark; Allijn, Iris E.
- Biotechnology Letters, Vol. 38, Issue 6
MetaboliteDetector: Comprehensive Analysis Tool for Targeted and Nontargeted GC/MS Based Metabolome Analysis
journal, May 2009
- Hiller, Karsten; Hangebrauk, Jasper; Jäger, Christian
- Analytical Chemistry, Vol. 81, Issue 9
Identification of an l-Arabinose Reductase Gene in Aspergillus niger and Its Role in l-Arabinose Catabolism
journal, May 2010
- Mojzita, Dominik; Penttilä, Merja; Richard, Peter
- Journal of Biological Chemistry, Vol. 285, Issue 31
A New Black Aspergillus Species, A. vadensis, Is a Promising Host for Homologous and Heterologous Protein Production
journal, July 2004
- de Vries, R. P.; Burgers, K.; van de Vondervoort, P. J. I.
- Applied and Environmental Microbiology, Vol. 70, Issue 7
The fungus Aspergillus niger consumes sugars in a sequential manner that is not mediated by the carbon catabolite repressor CreA
journal, April 2018
- Mäkelä, Miia R.; Aguilar-Pontes, María Victoria; van Rossen-Uffink, Diana
- Scientific Reports, Vol. 8, Issue 1
Pectin structure and biosynthesis
journal, June 2008
- Mohnen, D.
- Current Opinion in Plant Biology, Vol. 11, Issue 3
Isolation and analysis of xln R, encoding a transcriptional activator co-ordinating xylanolytic expression in Aspergillus niger
journal, January 1998
- van Peij, Noël N. M. E.; Visser, Jaap; de Graaff, Leo H.
- Molecular Microbiology, Vol. 27, Issue 1
MS-GF+ makes progress towards a universal database search tool for proteomics
journal, October 2014
- Kim, Sangtae; Pevzner, Pavel A.
- Nature Communications, Vol. 5, Issue 1
MASIC: A software program for fast quantitation and flexible visualization of chromatographic profiles from detected LC–MS(/MS) features
journal, June 2008
- Monroe, Matthew E.; Shaw, Jason L.; Daly, Don S.
- Computational Biology and Chemistry, Vol. 32, Issue 3
Sorbitol dehydrogenase of Aspergillus niger , SdhA, is part of the oxido-reductive d -galactose pathway and essential for d -sorbitol catabolism
journal, January 2012
- Koivistoinen, Outi M.; Richard, Peter; Penttilä, Merja
- FEBS Letters, Vol. 586, Issue 4
Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2
journal, December 2014
- Love, Michael I.; Huber, Wolfgang; Anders, Simon
- Genome Biology, Vol. 15, Issue 12