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Title: Glucose-Mediated Repression of Plant Biomass Utilization in the White-Rot Fungus Dichomitus squalens

Abstract

The extent of carbon catabolite repression (CCR) at a global level is unknown in wood-rotting fungi, which are critical to the carbon cycle and are a source of biotechnological enzymes. CCR occurs in the presence of sufficient concentrations of easily metabolizable carbon sources (e.g., glucose) and involves downregulation of the expression of genes encoding enzymes involved in the breakdown of complex carbon sources. We investigated this phenomenon in the white-rot fungusDichomitus squalensusing transcriptomics and exoproteomics. InD. squalenscultures, approximately 7% of genes were repressed in the presence of glucose compared to Avicel or xylan alone. The glucose-repressed genes included the essential components for utilization of plant biomass—carbohydrate-active enzyme(CAZyme) and carbon catabolic genes. The majority of polysaccharide-degrading CAZyme genes were repressed and included activities toward all major carbohydrate polymers present in plant cell walls, while repression of ligninolytic genes also occurred. The transcriptome-level repression of the CAZyme genes observed on the Avicel cultures was strongly supported by exoproteomics. Protease-encoding genes were generally not glucose repressed, indicating their likely dominant role in scavenging for nitrogen rather than carbon. The extent of CCR is surprising, given thatD. squalensrarely experiences high free sugar concentrations in its woody environment, and it indicates that biotechnological use ofD.more » squalensfor modification of plant biomass would benefit from derepressed or constitutively CAZyme-expressing strains. White-rot fungi are critical to the carbon cycle because they can mineralize all wood components using enzymes that also have biotechnological potential. The occurrence of carbon catabolite repression (CCR) in white-rot fungi is poorly understood. Previously, CCR in wood-rotting fungi has only been demonstrated for a small number of genes. We demonstrated widespread glucose-mediated CCR of plant biomass utilization in the white-rot fungusDichomitus squalens. This indicates that the CCR mechanism has been largely retained even though wood-rotting fungi rarely experience commonly considered CCR conditions in their woody environment. The general lack of repression of genes encoding proteases along with the reduction in secreted CAZymes during CCR suggested that the retention of CCR may be connected with the need to conserve nitrogen use during growth on nitrogen-scarce wood. Finally the widespread repression indicates that derepressed strains could be beneficial for enzyme production.« less

Authors:
ORCiD logo [1];  [1];  [2];  [3];  [3];  [3];  [3];  [2]; ORCiD logo [4]; ORCiD logo [5]
  1. Utrecht Univ. (Netherlands)
  2. Concordia Univ., Montrael, QB (Canada)
  3. USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
  4. Univ. of Helsinki (Finland)
  5. Utrecht Univ. (Netherlands); Univ. of Helsinki (Finland)
Publication Date:
Research Org.:
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC); Netherlands Scientific Organization; Academy of Finland
OSTI Identifier:
1619143
Grant/Contract Number:  
AC02-05CH11231; NWO 824.15.023; 308284
Resource Type:
Accepted Manuscript
Journal Name:
Applied and Environmental Microbiology
Additional Journal Information:
Journal Volume: 85; Journal Issue: 23; Journal ID: ISSN 0099-2240
Publisher:
American Society for Microbiology
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; dichomitus; carbon catabolite repression; CAZymes; regulation

Citation Formats

Daly, Paul, Peng, Mao, Di Falco, Marcos, Lipzen, Anna, Wang, Mei, Ng, Vivian, Grigoriev, Igor V., Tsang, Adrian, Mäkelä, Miia R., and de Vries, Ronald P.. Glucose-Mediated Repression of Plant Biomass Utilization in the White-Rot Fungus Dichomitus squalens. United States: N. p., 2019. Web. https://doi.org/10.1128/aem.01828-19.
Daly, Paul, Peng, Mao, Di Falco, Marcos, Lipzen, Anna, Wang, Mei, Ng, Vivian, Grigoriev, Igor V., Tsang, Adrian, Mäkelä, Miia R., & de Vries, Ronald P.. Glucose-Mediated Repression of Plant Biomass Utilization in the White-Rot Fungus Dichomitus squalens. United States. https://doi.org/10.1128/aem.01828-19
Daly, Paul, Peng, Mao, Di Falco, Marcos, Lipzen, Anna, Wang, Mei, Ng, Vivian, Grigoriev, Igor V., Tsang, Adrian, Mäkelä, Miia R., and de Vries, Ronald P.. Mon . "Glucose-Mediated Repression of Plant Biomass Utilization in the White-Rot Fungus Dichomitus squalens". United States. https://doi.org/10.1128/aem.01828-19. https://www.osti.gov/servlets/purl/1619143.
@article{osti_1619143,
title = {Glucose-Mediated Repression of Plant Biomass Utilization in the White-Rot Fungus Dichomitus squalens},
author = {Daly, Paul and Peng, Mao and Di Falco, Marcos and Lipzen, Anna and Wang, Mei and Ng, Vivian and Grigoriev, Igor V. and Tsang, Adrian and Mäkelä, Miia R. and de Vries, Ronald P.},
abstractNote = {The extent of carbon catabolite repression (CCR) at a global level is unknown in wood-rotting fungi, which are critical to the carbon cycle and are a source of biotechnological enzymes. CCR occurs in the presence of sufficient concentrations of easily metabolizable carbon sources (e.g., glucose) and involves downregulation of the expression of genes encoding enzymes involved in the breakdown of complex carbon sources. We investigated this phenomenon in the white-rot fungusDichomitus squalensusing transcriptomics and exoproteomics. InD. squalenscultures, approximately 7% of genes were repressed in the presence of glucose compared to Avicel or xylan alone. The glucose-repressed genes included the essential components for utilization of plant biomass—carbohydrate-active enzyme(CAZyme) and carbon catabolic genes. The majority of polysaccharide-degrading CAZyme genes were repressed and included activities toward all major carbohydrate polymers present in plant cell walls, while repression of ligninolytic genes also occurred. The transcriptome-level repression of the CAZyme genes observed on the Avicel cultures was strongly supported by exoproteomics. Protease-encoding genes were generally not glucose repressed, indicating their likely dominant role in scavenging for nitrogen rather than carbon. The extent of CCR is surprising, given thatD. squalensrarely experiences high free sugar concentrations in its woody environment, and it indicates that biotechnological use ofD. squalensfor modification of plant biomass would benefit from derepressed or constitutively CAZyme-expressing strains. White-rot fungi are critical to the carbon cycle because they can mineralize all wood components using enzymes that also have biotechnological potential. The occurrence of carbon catabolite repression (CCR) in white-rot fungi is poorly understood. Previously, CCR in wood-rotting fungi has only been demonstrated for a small number of genes. We demonstrated widespread glucose-mediated CCR of plant biomass utilization in the white-rot fungusDichomitus squalens. This indicates that the CCR mechanism has been largely retained even though wood-rotting fungi rarely experience commonly considered CCR conditions in their woody environment. The general lack of repression of genes encoding proteases along with the reduction in secreted CAZymes during CCR suggested that the retention of CCR may be connected with the need to conserve nitrogen use during growth on nitrogen-scarce wood. Finally the widespread repression indicates that derepressed strains could be beneficial for enzyme production.},
doi = {10.1128/aem.01828-19},
journal = {Applied and Environmental Microbiology},
number = 23,
volume = 85,
place = {United States},
year = {2019},
month = {11}
}

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