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Title: High resolution visualization and exo-proteomics reveal the physiological role of XlnR and AraR in plant biomass colonization and degradation by Aspergillus niger: Visualizing plant biomass degradation by A. niger

Abstract

In A. niger, two transcription factors, AraR and XlnR, regulate the production of enzymes involved in degradation of arabinoxylan and catabolism of the released L-arabinose and D-xylose. Deletion of both araR and xlnR in leads to reduced production of (hemi)cellulolytic enzymes and reduced growth on arabinan, arabinogalactan and xylan. In this study, we investigated the colonization and degradation of wheat bran by the A. niger reference strain CBS 137562 and araR/xlnR regulatory mutants using highresolution microscopy and exo-proteomics. We discovered that wheat bran flakes have a ‘rough’ and ‘smooth’ surface with substantially different affinity towards fungal hyphae. While colonization of the rough side was possible for all strains, the xlnR mutants struggled to survive on the smooth side of the wheat bran particles after 20 and 40 h post inoculation. Impaired colonization ability of the smooth surface of wheat bran was linked to reduced potential of DxlnR to secrete arabinoxylan and cellulosedegrading enzymes and indicates that XlnR is the major regulator that drives colonization of wheat bran in A. niger.

Authors:
 [1];  [1];  [2];  [2];  [2];  [2];  [2];  [2];  [1];  [1];  [1];  [2];  [1]
  1. Fungal Physiology, Westerdijk Fungal Biodiversity Institute & Fungal Molecular Physiology, Utrecht University, Utrecht, the Netherlands
  2. Department of Energy, Environmental Molecular Sciences Laboratory, Richland WA USA
Publication Date:
Research Org.:
Pacific Northwest National Lab. (PNNL), Richland, WA (United States)
Sponsoring Org.:
USDOE
OSTI Identifier:
1439702
Report Number(s):
PNNL-SA-134692
Journal ID: ISSN 1462-2912; KP1704020
DOE Contract Number:  
AC05-76RL01830
Resource Type:
Journal Article
Journal Name:
Environmental Microbiology
Additional Journal Information:
Journal Volume: 19; Journal Issue: 11; Journal ID: ISSN 1462-2912
Publisher:
Wiley
Country of Publication:
United States
Language:
English

Citation Formats

Kowalczyk, Joanna E., Khosravi, Claire, Purvine, Samuel, Dohnalkova, Alice, Chrisler, William B., Orr, Galya, Robinson, Errol, Zink, Erika, Wiebenga, Ad, Peng, Mao, Battaglia, Evy, Baker, Scott, and de Vries, Ronald P. High resolution visualization and exo-proteomics reveal the physiological role of XlnR and AraR in plant biomass colonization and degradation by Aspergillus niger: Visualizing plant biomass degradation by A. niger. United States: N. p., 2017. Web. doi:10.1111/1462-2920.13923.
Kowalczyk, Joanna E., Khosravi, Claire, Purvine, Samuel, Dohnalkova, Alice, Chrisler, William B., Orr, Galya, Robinson, Errol, Zink, Erika, Wiebenga, Ad, Peng, Mao, Battaglia, Evy, Baker, Scott, & de Vries, Ronald P. High resolution visualization and exo-proteomics reveal the physiological role of XlnR and AraR in plant biomass colonization and degradation by Aspergillus niger: Visualizing plant biomass degradation by A. niger. United States. doi:10.1111/1462-2920.13923.
Kowalczyk, Joanna E., Khosravi, Claire, Purvine, Samuel, Dohnalkova, Alice, Chrisler, William B., Orr, Galya, Robinson, Errol, Zink, Erika, Wiebenga, Ad, Peng, Mao, Battaglia, Evy, Baker, Scott, and de Vries, Ronald P. Fri . "High resolution visualization and exo-proteomics reveal the physiological role of XlnR and AraR in plant biomass colonization and degradation by Aspergillus niger: Visualizing plant biomass degradation by A. niger". United States. doi:10.1111/1462-2920.13923.
@article{osti_1439702,
title = {High resolution visualization and exo-proteomics reveal the physiological role of XlnR and AraR in plant biomass colonization and degradation by Aspergillus niger: Visualizing plant biomass degradation by A. niger},
author = {Kowalczyk, Joanna E. and Khosravi, Claire and Purvine, Samuel and Dohnalkova, Alice and Chrisler, William B. and Orr, Galya and Robinson, Errol and Zink, Erika and Wiebenga, Ad and Peng, Mao and Battaglia, Evy and Baker, Scott and de Vries, Ronald P.},
abstractNote = {In A. niger, two transcription factors, AraR and XlnR, regulate the production of enzymes involved in degradation of arabinoxylan and catabolism of the released L-arabinose and D-xylose. Deletion of both araR and xlnR in leads to reduced production of (hemi)cellulolytic enzymes and reduced growth on arabinan, arabinogalactan and xylan. In this study, we investigated the colonization and degradation of wheat bran by the A. niger reference strain CBS 137562 and araR/xlnR regulatory mutants using highresolution microscopy and exo-proteomics. We discovered that wheat bran flakes have a ‘rough’ and ‘smooth’ surface with substantially different affinity towards fungal hyphae. While colonization of the rough side was possible for all strains, the xlnR mutants struggled to survive on the smooth side of the wheat bran particles after 20 and 40 h post inoculation. Impaired colonization ability of the smooth surface of wheat bran was linked to reduced potential of DxlnR to secrete arabinoxylan and cellulosedegrading enzymes and indicates that XlnR is the major regulator that drives colonization of wheat bran in A. niger.},
doi = {10.1111/1462-2920.13923},
journal = {Environmental Microbiology},
issn = {1462-2912},
number = 11,
volume = 19,
place = {United States},
year = {2017},
month = {10}
}

Works referenced in this record:

The phenolic acid and polysaccharide composition of cell walls of bran layers of mature wheat (Triticum aestivum L. cv. Avalon) grains
journal, January 2005

  • Parker, Mary L.; Ng, Annie; Waldron, Keith W.
  • Journal of the Science of Food and Agriculture, Vol. 85, Issue 15
  • DOI: 10.1002/jsfa.2304

Advances in proteomics data analysis and display using an accurate mass and time tag approach
journal, January 2006

  • Zimmer, Jennifer S. D.; Monroe, Matthew E.; Qian, Wei-Jun
  • Mass Spectrometry Reviews, Vol. 25, Issue 3
  • DOI: 10.1002/mas.20071

DAnTE: a statistical tool for quantitative analysis of -omics data
journal, May 2008


Analysis of regulation of pentose utilisation in Aspergillus niger reveals evolutionary adaptations in Eurotiales
journal, June 2011


The roles of the zinc finger transcription factors XlnR, ClrA and ClrB in the breakdown of lignocellulose by Aspergillus niger
journal, January 2016


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
  • DOI: 10.1093/nar/gkt1178

d-Xylose Concentration-Dependent Hydrolase Expression Profiles and the Function of CreA and XlnR in Aspergillus niger
journal, February 2012

  • Mach-Aigner, Astrid R.; Omony, Jimmy; Jovanovic, Birgit
  • Applied and Environmental Microbiology, Vol. 78, Issue 9
  • DOI: 10.1128/AEM.07772-11

How a fungus escapes the water to grow into the air
journal, January 1999


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
  • DOI: 10.1007/s00438-002-0729-7

DeconMSn: a software tool for accurate parent ion monoisotopic mass determination for tandem mass spectra
journal, February 2008


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
  • DOI: 10.1186/s13068-015-0285-0

Hydrophobins: Multipurpose Proteins
journal, October 2001


RNAseq reveals hydrophobins that are involved in the adaptation of Aspergillus nidulans to lignocellulose
journal, July 2016

  • Brown, Neil Andrew; Ries, Laure N. A.; Reis, Thaila F.
  • Biotechnology for Biofuels, Vol. 9, Issue 1
  • DOI: 10.1186/s13068-016-0558-2

The role of carbon starvation in the induction of enzymes that degrade plant-derived carbohydrates in Aspergillus niger
journal, November 2014


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
  • DOI: 10.1007/s00253-011-3242-2

Comparative Secretome Analysis of Trichoderma reesei and Aspergillus niger during Growth on Sugarcane Biomass
journal, June 2015


Improved Peptide Elution Time Prediction for Reversed-Phase Liquid Chromatography-MS by Incorporating Peptide Sequence Information
journal, July 2006

  • Petritis, Konstantinos; Kangas, Lars J.; Yan, Bo
  • Analytical Chemistry, Vol. 78, Issue 14
  • DOI: 10.1021/ac060143p

The influence of Aspergillus niger transcription factors AraR and XlnR in the gene expression during growth in d-xylose, l-arabinose and steam-exploded sugarcane bagasse
journal, November 2013

  • de Souza, Wagner Rodrigo; Maitan-Alfenas, Gabriela Piccolo; de Gouvêa, Paula Fagundes
  • Fungal Genetics and Biology, Vol. 60
  • DOI: 10.1016/j.fgb.2013.07.007

A New Black Aspergillus Species, A. vadensis, Is a Promising Host for Homologous and Heterologous Protein Production
journal, July 2004


VIPER: an advanced software package to support high-throughput LC-MS peptide identification
journal, June 2007


Isolation and analysis of xln R, encoding a transcriptional activator co-ordinating xylanolytic expression in Aspergillus niger
journal, January 1998


Uncovering the Genome-Wide Transcriptional Responses of the Filamentous Fungus Aspergillus niger to Lignocellulose Using RNA Sequencing
journal, August 2012


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
  • DOI: 10.1038/ncomms6277

Characterization of the Kexin-Like Maturase of Aspergillus niger
journal, January 2000

  • Jalving, R.; van de Vondervoort, P. J. I.; Visser, J.
  • Applied and Environmental Microbiology, Vol. 66, Issue 1
  • DOI: 10.1128/AEM.66.1.363-368.2000

Similar is not the same: Differences in the function of the (hemi-)cellulolytic regulator XlnR (Xlr1/Xyr1) in filamentous fungi
journal, November 2014