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Title: Genome sequencing and transcriptome analysis of Trichoderma reesei QM9978 strain reveals a distal chromosome translocation to be responsible for loss of vib1 expression and loss of cellulase induction

Abstract

Background: The hydrolysis of biomass to simple sugars used for the production of biofuels in biorefneries requires the action of cellulolytic enzyme mixtures. During the last 50 years, the ascomycete Trichoderma reesei, the main source of industrial cellulase and hemicellulase cocktails, has been subjected to several rounds of classical mutagenesis with the aim to obtain higher production levels. During these random genetic events, strains unable to produce cellulases were generated. Here, whole genome sequencing and transcriptomic analyses of the cellulase-negative strain QM9978 were used for the identifcation of mutations underlying this cellulase-negative phenotype. Results: Sequence comparison of the cellulase-negative strain QM9978 to the reference strain QM6a identifed a total of 43 mutations, of which 33 were located either close to or in coding regions. From those, we identifed 23 single-nucleotide variants, nine InDels, and one translocation. The translocation occurred between chromosomes V and VII, is located upstream of the putative transcription factor vib1, and abolishes its expression in QM9978 as detected during the transcriptomic analyses. Ectopic expression of vib1 under the control of its native promoter as well as overexpression of vib1 under the control of a strong constitutive promoter restored cellulase expression in QM9978, thus confrming that the translocationmore » event is the reason for the cellulase-negative phenotype. Gene deletion of vib1 in the moderate producer strain QM9414 and in the high producer strain Rut-C30 reduced cellulase expression in both cases. Overexpression of vib1 in QM9414 and Rut-C30 had no efect on cellulase production, most likely because vib1 is already expressed at an optimal level under normal conditions. Conclusion: We were able to establish a link between a chromosomal translocation in QM9978 and the cellulasenegative phenotype of the strain. We identifed the transcription factor vib1 as a key regulator of cellulases in T. reesei whose expression is absent in QM9978. We propose that in T. reesei, as in Neurospora crassa, vib1 is involved in cellulase induction, although the exact mechanism remains to be elucidated. The data presented here show an example of a combined genome sequencing and transcriptomic approach to explain a specifc trait, in this case the QM9978 cellulase-negative phenotype, and how it helps to better understand the mechanisms during cellulase gene regulation. When focusing on mutations on the single base-pair level, changes on the chromosome level can be easily overlooked and through this work we provide an example that stresses the importance of the big picture of the genomic landscape during analysis of sequencing data.« less

Authors:
ORCiD logo [1];  [2];  [3];  [2];  [2];  [4];  [5];  [6];  [3];  [3]
+ Show Author Affiliations
  1. IFP Energies Nouvelles, Rueil-Malmaison (France); Institut Pasteur, Paris (France). Genetics of Biofilms. Dept. of Microbiology
  2. Technische Univ. Wien (Austria). Inst. of Chemical Engineering. Research Division Biochemical Technology. Molecular Biotechnology
  3. IFP Energies Nouvelles, Rueil-Malmaison (France)
  4. Pacific Northwest National Lab. (PNNL), Richland, WA (United States). Earth and Biological Sciences Directorate
  5. Sorbonne Univ., Paris (France). Evolution Paris Seine-Institut de Biologie Paris Seine (EPS-IBPS).
  6. Ecole Normale Superieure, Paris (France). PSL Research Univ. CNRS. Inserm. Institut de Biologie de l’École normale supérieure (IBENS). Plateforme Génomique
Publication Date:
Research Org.:
Pacific Northwest National Laboratory (PNNL), Richland, WA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER)
OSTI Identifier:
1626985
Grant/Contract Number:  
AC05-76RL01830
Resource Type:
Accepted Manuscript
Journal Name:
Biotechnology for Biofuels
Additional Journal Information:
Journal Volume: 10; Journal Issue: 1; Journal ID: ISSN 1754-6834
Publisher:
BioMed Central
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; 09 BIOMASS FUELS; Biotechnology & Applied Microbiology; Energy & Fuels; Trichoderma reesei; Genome analysis; Transcriptome; vib1; Cellulase production; Promoter; Translocation

Citation Formats

Ivanova, Christa, Ramoni, Jonas, Aouam, Thiziri, Frischmann, Alexa, Seiboth, Bernhard, Baker, Scott E., Le Crom, Stéphane, Lemoine, Sophie, Margeot, Antoine, and Bidard, Frédérique. Genome sequencing and transcriptome analysis of Trichoderma reesei QM9978 strain reveals a distal chromosome translocation to be responsible for loss of vib1 expression and loss of cellulase induction. United States: N. p., 2017. Web. doi:10.1186/s13068-017-0897-7.
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Ivanova, Christa, Ramoni, Jonas, Aouam, Thiziri, Frischmann, Alexa, Seiboth, Bernhard, Baker, Scott E., Le Crom, Stéphane, Lemoine, Sophie, Margeot, Antoine, & Bidard, Frédérique. Genome sequencing and transcriptome analysis of Trichoderma reesei QM9978 strain reveals a distal chromosome translocation to be responsible for loss of vib1 expression and loss of cellulase induction. United States. https://doi.org/10.1186/s13068-017-0897-7
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Ivanova, Christa, Ramoni, Jonas, Aouam, Thiziri, Frischmann, Alexa, Seiboth, Bernhard, Baker, Scott E., Le Crom, Stéphane, Lemoine, Sophie, Margeot, Antoine, and Bidard, Frédérique. Thu . "Genome sequencing and transcriptome analysis of Trichoderma reesei QM9978 strain reveals a distal chromosome translocation to be responsible for loss of vib1 expression and loss of cellulase induction". United States. https://doi.org/10.1186/s13068-017-0897-7. https://www.osti.gov/servlets/purl/1626985.
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@article{osti_1626985,
title = {Genome sequencing and transcriptome analysis of Trichoderma reesei QM9978 strain reveals a distal chromosome translocation to be responsible for loss of vib1 expression and loss of cellulase induction},
author = {Ivanova, Christa and Ramoni, Jonas and Aouam, Thiziri and Frischmann, Alexa and Seiboth, Bernhard and Baker, Scott E. and Le Crom, Stéphane and Lemoine, Sophie and Margeot, Antoine and Bidard, Frédérique},
abstractNote = {Background: The hydrolysis of biomass to simple sugars used for the production of biofuels in biorefneries requires the action of cellulolytic enzyme mixtures. During the last 50 years, the ascomycete Trichoderma reesei, the main source of industrial cellulase and hemicellulase cocktails, has been subjected to several rounds of classical mutagenesis with the aim to obtain higher production levels. During these random genetic events, strains unable to produce cellulases were generated. Here, whole genome sequencing and transcriptomic analyses of the cellulase-negative strain QM9978 were used for the identifcation of mutations underlying this cellulase-negative phenotype. Results: Sequence comparison of the cellulase-negative strain QM9978 to the reference strain QM6a identifed a total of 43 mutations, of which 33 were located either close to or in coding regions. From those, we identifed 23 single-nucleotide variants, nine InDels, and one translocation. The translocation occurred between chromosomes V and VII, is located upstream of the putative transcription factor vib1, and abolishes its expression in QM9978 as detected during the transcriptomic analyses. Ectopic expression of vib1 under the control of its native promoter as well as overexpression of vib1 under the control of a strong constitutive promoter restored cellulase expression in QM9978, thus confrming that the translocation event is the reason for the cellulase-negative phenotype. Gene deletion of vib1 in the moderate producer strain QM9414 and in the high producer strain Rut-C30 reduced cellulase expression in both cases. Overexpression of vib1 in QM9414 and Rut-C30 had no efect on cellulase production, most likely because vib1 is already expressed at an optimal level under normal conditions. Conclusion: We were able to establish a link between a chromosomal translocation in QM9978 and the cellulasenegative phenotype of the strain. We identifed the transcription factor vib1 as a key regulator of cellulases in T. reesei whose expression is absent in QM9978. We propose that in T. reesei, as in Neurospora crassa, vib1 is involved in cellulase induction, although the exact mechanism remains to be elucidated. The data presented here show an example of a combined genome sequencing and transcriptomic approach to explain a specifc trait, in this case the QM9978 cellulase-negative phenotype, and how it helps to better understand the mechanisms during cellulase gene regulation. When focusing on mutations on the single base-pair level, changes on the chromosome level can be easily overlooked and through this work we provide an example that stresses the importance of the big picture of the genomic landscape during analysis of sequencing data.},
doi = {10.1186/s13068-017-0897-7},
journal = {Biotechnology for Biofuels},
number = 1,
volume = 10,
place = {United States},
year = {Thu Sep 07 00:00:00 EDT 2017},
month = {Thu Sep 07 00:00:00 EDT 2017}
}
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Genetic improvement of Trichoderma reesei for large scale cellulase production
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The Lipid Body Protein, PpoA, Coordinates Sexual and Asexual Sporulation in Aspergillus nidulans
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DNA Damage, Homology-Directed Repair, and DNA Methylation
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The CRE1 carbon catabolite repressor of the fungus Trichoderma reesei: a master regulator of carbon assimilation
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Expression of Biomass-Degrading Enzymes Is a Major Event during Conidium Development in Trichoderma reesei
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Induction of cellulase in trichoderma reesei grown on lactose: Induction of Cellulase
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Conserved and essential transcription factors for cellulase gene expression in ascomycete fungi
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Cloning of genes expressed early during cellulase induction in Hypocrea jecorina by a rapid subtraction hybridization approach
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Comparative Genomics Analysis of Trichoderma reesei Strains
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A new Zn(II)2Cys6-type transcription factor BglR regulates β-glucosidase expression in Trichoderma reesei
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Suppressor of fusion, a Fusarium oxysporum homolog of Ndt80, is required for nutrient-dependent regulation of anastomosis
journal, October 2016

Kinetic transcriptome analysis reveals an essentially intact induction system in a cellulase hyper-producer Trichoderma reesei strain
journal, December 2014

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The Sequence Alignment/Map format and SAMtools
journal, June 2009

Consolidated bioprocessing of lignocellulose for production of glucaric acid by an artificial microbial consortium
journal, April 2021

Achieving efficient protein expression in Trichoderma reesei by using strong constitutive promoters
journal, January 2012

Directed evolution of industrial enzymes: an update
journal, August 2003

Comparative analysis of the Trichoderma reesei transcriptome during growth on the cellulase inducing substrates wheat straw and lactose
journal, January 2013

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  • Biotechnology for Biofuels, Vol. 6, Issue 1
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Systems analysis of plant cell wall degradation by the model filamentous fungus Neurospora crassa
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  • Tian, Chaoguang; Beeson, William T.; Iavarone, Anthony T.
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Identification of vib-1 , a Locus Involved in Vegetative Incompatibility Mediated by het-c in Neurospora crassa
journal, September 2002

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    Works referencing / citing this record:

    YPR2 is a regulator of light modulated carbon and secondary metabolism in Trichoderma reesei
    journal, March 2019

    Enhancement of cellulase production in Trichoderma reesei RUT-C30 by comparative genomic screening
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    Enhancement of cellulase production in Trichoderma reesei RUT-C30 by comparative genomic screening
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    The regulatory and transcriptional landscape associated with carbon utilization in a filamentous fungus
    journal, February 2020

    • Wu, Vincent W.; Thieme, Nils; Huberman, Lori B.
    • Proceedings of the National Academy of Sciences, Vol. 117, Issue 11
    • DOI: 10.1073/pnas.1915611117

    Metabolic Engineering of Fungal Strains for Efficient Production of Cellulolytic Enzymes
    book, January 2018

    The influence of feedstock characteristics on enzyme production in Trichoderma reesei: a review on productivity, gene regulation and secretion profiles
    journal, October 2019

    • Novy, Vera; Nielsen, Fredrik; Seiboth, Bernhard
    • Biotechnology for Biofuels, Vol. 12, Issue 1
    • DOI: 10.1186/s13068-019-1571-z

    The role of PKAc1 in gene regulation and trichodimerol production in Trichoderma reesei
    journal, September 2019

    • Hinterdobler, Wolfgang; Schuster, André; Tisch, Doris
    • Fungal Biology and Biotechnology, Vol. 6, Issue 1
    • DOI: 10.1186/s40694-019-0075-8

    Protein hyperproduction in fungi by design
    journal, August 2018

    Regulation of plant cell wall degradation by light in Trichoderma
    journal, April 2018

    Protein hyperproduction in fungi by design
    journal, August 2018

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