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Title: Identification and manipulation of Neurospora crassa genes involved in sensitivity to furfural

Abstract

Background: Biofuels derived from lignocellulosic biomass are a viable alternative to fossil fuels required for transportation. Following plant biomass pretreatment, the furan derivative furfural is present at concentrations which are inhibitory to yeasts. Detoxification of furfural is thus important for efficient fermentation. Here, we searched for new genetic attributes in the fungus Neurospora crassa that may be linked to furfural tolerance. The fact that furfural is involved in the natural process of sexual spore germination of N. crassa and that this fungus is highly amenable to genetic manipulations makes it a rational candidate for this study. Results: Both hypothesis-based and unbiased (random promotor mutagenesis) approaches were performed to identify N. crassa genes associated with the response to furfural. Changes in the transcriptional profile following exposure to furfural revealed that the affected processes were, overall, similar to those observed in Saccharomyces cerevisiae. N. crassa was more tolerant (by ~ 30%) to furfural when carboxymethyl cellulose was the main carbon source as opposed to sucrose, indicative of a link between carbohydrate metabolism and furfural tolerance. We also observed increased tolerance in a Δcre-1 mutant (CRE-1 is a key transcription factor that regulates the ability of fungi to utilize non-preferred carbon sources). Inmore » addition, analysis of aldehyde dehydrogenase mutants showed that ahd-2 (NCU00378) was involved in tolerance to furfural as well as the predicted membrane transporter NCU05580 (flr-1), a homolog of FLR1 in S. cerevisiae. Further to the rational screening, an unbiased approach revealed additional genes whose inactivation conferred increased tolerance to furfural: (i) NCU02488, which affected the abundance of the non-anchored cell wall protein NCW-1 (NCU05137), and (ii) the zinc finger protein NCU01407. Conclusions:We identified attributes in N. crassa associated with tolerance or degradation of furfural, using complementary research approaches. The manipulation of the genes involved in furan sensitivity can provide a means for improving the production of biofuel producing strains. Similar research approaches can be utilized in N. crassa and other filamentous fungi to identify additional attributes relevant to other furans or toxic chemicals.« less

Authors:
 [1];  [2];  [1];  [3];  [1]; ORCiD logo [1]
  1. Hebrew Univ. of Jerusalem, Rehovot (Israel). Dept. of Plant Pathology and Microbiology
  2. Univ. of California, Berkeley, CA (United States). Dept. of Plant and Microbial Biology
  3. Univ. of California, Berkeley, CA (United States). Dept. of Plant and Microbial Biology; Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Environmental Genomics and Systems Biology Division
Publication Date:
Research Org.:
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC)
OSTI Identifier:
1571949
Grant/Contract Number:  
AC02-05CH11231
Resource Type:
Accepted Manuscript
Journal Name:
Biotechnology for Biofuels
Additional Journal Information:
Journal Volume: 12; Journal Issue: 1; Journal ID: ISSN 1754-6834
Publisher:
BioMed Central
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES

Citation Formats

Feldman, Daria, Kowbel, David J., Cohen, Adi, Glass, N. Louise, Hadar, Yitzhak, and Yarden, Oded. Identification and manipulation of Neurospora crassa genes involved in sensitivity to furfural. United States: N. p., 2019. Web. doi:10.1186/s13068-019-1550-4.
Feldman, Daria, Kowbel, David J., Cohen, Adi, Glass, N. Louise, Hadar, Yitzhak, & Yarden, Oded. Identification and manipulation of Neurospora crassa genes involved in sensitivity to furfural. United States. doi:10.1186/s13068-019-1550-4.
Feldman, Daria, Kowbel, David J., Cohen, Adi, Glass, N. Louise, Hadar, Yitzhak, and Yarden, Oded. Wed . "Identification and manipulation of Neurospora crassa genes involved in sensitivity to furfural". United States. doi:10.1186/s13068-019-1550-4. https://www.osti.gov/servlets/purl/1571949.
@article{osti_1571949,
title = {Identification and manipulation of Neurospora crassa genes involved in sensitivity to furfural},
author = {Feldman, Daria and Kowbel, David J. and Cohen, Adi and Glass, N. Louise and Hadar, Yitzhak and Yarden, Oded},
abstractNote = {Background: Biofuels derived from lignocellulosic biomass are a viable alternative to fossil fuels required for transportation. Following plant biomass pretreatment, the furan derivative furfural is present at concentrations which are inhibitory to yeasts. Detoxification of furfural is thus important for efficient fermentation. Here, we searched for new genetic attributes in the fungus Neurospora crassa that may be linked to furfural tolerance. The fact that furfural is involved in the natural process of sexual spore germination of N. crassa and that this fungus is highly amenable to genetic manipulations makes it a rational candidate for this study. Results: Both hypothesis-based and unbiased (random promotor mutagenesis) approaches were performed to identify N. crassa genes associated with the response to furfural. Changes in the transcriptional profile following exposure to furfural revealed that the affected processes were, overall, similar to those observed in Saccharomyces cerevisiae. N. crassa was more tolerant (by ~ 30%) to furfural when carboxymethyl cellulose was the main carbon source as opposed to sucrose, indicative of a link between carbohydrate metabolism and furfural tolerance. We also observed increased tolerance in a Δcre-1 mutant (CRE-1 is a key transcription factor that regulates the ability of fungi to utilize non-preferred carbon sources). In addition, analysis of aldehyde dehydrogenase mutants showed that ahd-2 (NCU00378) was involved in tolerance to furfural as well as the predicted membrane transporter NCU05580 (flr-1), a homolog of FLR1 in S. cerevisiae. Further to the rational screening, an unbiased approach revealed additional genes whose inactivation conferred increased tolerance to furfural: (i) NCU02488, which affected the abundance of the non-anchored cell wall protein NCW-1 (NCU05137), and (ii) the zinc finger protein NCU01407. Conclusions:We identified attributes in N. crassa associated with tolerance or degradation of furfural, using complementary research approaches. The manipulation of the genes involved in furan sensitivity can provide a means for improving the production of biofuel producing strains. Similar research approaches can be utilized in N. crassa and other filamentous fungi to identify additional attributes relevant to other furans or toxic chemicals.},
doi = {10.1186/s13068-019-1550-4},
journal = {Biotechnology for Biofuels},
number = 1,
volume = 12,
place = {United States},
year = {2019},
month = {9}
}

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    Works referencing / citing this record:

    Detoxification of 5-hydroxymethylfurfural by the Pleurotus ostreatus lignolytic enzymes aryl alcohol oxidase and dehydrogenase
    journal, April 2015

    • Feldman, Daria; Kowbel, David J.; Glass, N. Louise
    • Biotechnology for Biofuels, Vol. 8, Issue 1
    • DOI: 10.1186/s13068-015-0244-9

    MindTheGap: integrated detection and assembly of short and long insertions
    journal, August 2014


    Biotechnological strategies to overcome inhibitors in lignocellulose hydrolysates for ethanol production: review
    journal, May 2010


    Transcriptome shifts in response to furfural and acetic acid in Saccharomyces cerevisiae
    journal, March 2010


    The genome sequence of the filamentous fungus Neurospora crassa
    journal, April 2003

    • Galagan, James E.; Calvo, Sarah E.; Borkovich, Katherine A.
    • Nature, Vol. 422, Issue 6934
    • DOI: 10.1038/nature01554

    High-throughput chromatin immunoprecipitation for genome-wide mapping of in vivo protein-DNA interactions and epigenomic states
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    • Blecher-Gonen, Ronnie; Barnett-Itzhaki, Zohar; Jaitin, Diego
    • Nature Protocols, Vol. 8, Issue 3
    • DOI: 10.1038/nprot.2013.023

    The generation of fermentation inhibitors during dilute acid hydrolysis of softwood
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    • Larsson, Simona; Palmqvist, Eva; Hahn-Hägerdal, Bärbel
    • Enzyme and Microbial Technology, Vol. 24, Issue 3-4
    • DOI: 10.1016/s0141-0229(98)00101-x

    Chitin synthase 1 plays a major role in cell wall biogenesis in Neurospora crassa.
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    Identification and characterization of the furfural and 5-(hydroxymethyl)furfural degradation pathways of Cupriavidus basilensis HMF14
    journal, March 2010

    • Koopman, F.; Wierckx, N.; de Winde, J. H.
    • Proceedings of the National Academy of Sciences, Vol. 107, Issue 11
    • DOI: 10.1073/pnas.0913039107

    TopHat: discovering splice junctions with RNA-Seq
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    Identification of the CRE-1 Cellulolytic Regulon in Neurospora crassa
    journal, September 2011


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    • Taherzadeh, Mohammad; Karimi, Keikhosro
    • International Journal of Molecular Sciences, Vol. 9, Issue 9, p. 1621-1651
    • DOI: 10.3390/ijms9091621

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    • Modig, Tobias; LidÉN, Gunnar; Taherzadeh, Mohammad J.
    • Biochemical Journal, Vol. 363, Issue 3
    • DOI: 10.1042/bj3630769

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    • Proceedings of the National Academy of Sciences, Vol. 109, Issue 19
    • DOI: 10.1073/pnas.1200785109

    Open source clustering software
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    Carbon source affects PKA-dependent polarity of Neurospora crassa in a CRE-1-dependent and independent manner
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    Analysis of a conserved cellulase transcriptional regulator reveals inducer-independent production of cellulolytic enzymes in Neurospora crassa
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    • Coradetti, Samuel T.; Xiong, Yi; Glass, N. Louise
    • MicrobiologyOpen, Vol. 2, Issue 4
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    Strains of Neurospora Collected from Nature
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    Multiple gene-mediated NAD(P)H-dependent aldehyde reduction is a mechanism of in situ detoxification of furfural and 5-hydroxymethylfurfural by Saccharomyces cerevisiae
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    • Lewis Liu, Z.; Moon, Jaewoong; Andersh, Brad J.
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    • DOI: 10.1007/s00253-008-1702-0

    Systems analysis of plant cell wall degradation by the model filamentous fungus Neurospora crassa
    journal, December 2009

    • Tian, Chaoguang; Beeson, William T.; Iavarone, Anthony T.
    • Proceedings of the National Academy of Sciences, Vol. 106, Issue 52
    • DOI: 10.1073/pnas.0906810106

    Understanding physiological responses to pre-treatment inhibitors in ethanologenic fermentations
    journal, February 2012

    • Taylor, Mark P.; Mulako, Inonge; Tuffin, Marla
    • Biotechnology Journal, Vol. 7, Issue 9, p. 1169-1181
    • DOI: 10.1002/biot.201100335

    Fungal pretreatment of lignocellulosic biomass
    journal, November 2012


    Life-history ofNeurospora intermedia in a sugar cane field
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    • Pandit, Alka; Maheshwari, Ramesh
    • Journal of Biosciences, Vol. 21, Issue 1
    • DOI: 10.1007/bf02716813

    Silencing of NADPH-Dependent Oxidoreductase Genes (yqhD and dkgA) in Furfural-Resistant Ethanologenic Escherichia coli
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    • Miller, E. N.; Jarboe, L. R.; Yomano, L. P.
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    • DOI: 10.1128/aem.00567-09

    Plant Cell Wall Deconstruction by Ascomycete Fungi
    journal, September 2013


    Exploring the tolerance of marine yeast to inhibitory compounds for improving bioethanol production
    journal, January 2019

    • Greetham, Darren; Zaky, Abdelrahman Saleh; Du, Chenyu
    • Sustainable Energy & Fuels, Vol. 3, Issue 6
    • DOI: 10.1039/c9se00029a

    ManR, a Transcriptional Regulator of the β-Mannan Utilization System, Controls the Cellulose Utilization System in <i>Aspergillus oryzae</i>
    journal, January 2013

    • Ogawa, Masahiro; Kobayashi, Tetsuo; Koyama, Yasuji
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    • DOI: 10.1271/bbb.120795

    Comparative proteomic analysis of a new adaptive Pichia Stipitis strain to furfural, a lignocellulosic inhibitory compound
    journal, January 2013

    • Hao, Xue-Cai; Yang, Xiu-Shan; Wan, Ping
    • Biotechnology for Biofuels, Vol. 6, Issue 1
    • DOI: 10.1186/1754-6834-6-34

    Mechanism of formation of 2-furaldehyde from d-xylose
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    Furfural Formation and Behavior
    journal, February 1948


    Lessons from the Genome Sequence of Neurospora crassa: Tracing the Path from Genomic Blueprint to Multicellular Organism
    journal, March 2004


    LUMPY: a probabilistic framework for structural variant discovery
    journal, January 2014


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