Crosstalk of Cellulose and Mannan Perception Pathways Leads to Inhibition of Cellulase Production in Several Filamentous Fungi

ABSTRACT It is essential for microbes to acquire information about their environment. Fungi use soluble degradation products of plant cell wall components to understand the substrate composition they grow on. Individual perception pathways have been well described. However, the interconnections betw...

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Autores principales:	Lara Hassan, Liangcai Lin, Hagit Sorek, Laura E. Sperl, Thomas Goudoulas, Franz Hagn, Natalie Germann, Chaoguang Tian, J. Philipp Benz
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2019
Materias:	Neurospora crassa cellulose/hemicellulose signaling competitive inhibition filamentous fungi plant cell wall degradation Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/b6dea3630057434590e8606a84909d21
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spelling	oai:doaj.org-article:b6dea3630057434590e8606a84909d212021-11-15T16:22:10ZCrosstalk of Cellulose and Mannan Perception Pathways Leads to Inhibition of Cellulase Production in Several Filamentous Fungi10.1128/mBio.00277-192150-7511https://doaj.org/article/b6dea3630057434590e8606a84909d212019-08-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00277-19https://doaj.org/toc/2150-7511ABSTRACT It is essential for microbes to acquire information about their environment. Fungi use soluble degradation products of plant cell wall components to understand the substrate composition they grow on. Individual perception pathways have been well described. However, the interconnections between pathways remain poorly understood. In the present work, we provide evidence of crosstalk between the perception pathways for cellulose and the hemicellulose mannan being conserved in several filamentous fungi and leading to the inhibition of cellulase expression. We used the functional genomics tools available for Neurospora crassa to investigate this overlap at the molecular level. Crosstalk and competitive inhibition could be identified both during uptake by cellodextrin transporters and intracellularly. Importantly, the overlap is independent of CRE-1-mediated catabolite repression. These results provide novel insights into the regulatory networks of lignocellulolytic fungi and will contribute to the rational optimization of fungal enzyme production for efficient plant biomass depolymerization and utilization. IMPORTANCE In fungi, the production of enzymes for polysaccharide degradation is controlled by complex signaling networks. Previously, these networks were studied in response to simple sugars or single polysaccharides. Here, we tackled for the first time the molecular interplay between two seemingly unrelated perception pathways: those for cellulose and the hemicellulose (gluco)mannan. We identified a so far unknown competitive inhibition between the respective degradation products acting as signaling molecules. Competition was detected both at the level of the uptake and intracellularly, upstream of the main transcriptional regulator CLR-2. Our findings provide novel insights into the molecular communication between perception pathways. Also, they present possible targets for the improvement of industrial strains for higher cellulase production through the engineering of mannan insensitivity.Lara HassanLiangcai LinHagit SorekLaura E. SperlThomas GoudoulasFranz HagnNatalie GermannChaoguang TianJ. Philipp BenzAmerican Society for MicrobiologyarticleNeurospora crassacellulose/hemicellulose signalingcompetitive inhibitionfilamentous fungiplant cell wall degradationMicrobiologyQR1-502ENmBio, Vol 10, Iss 4 (2019)
institution	DOAJ
collection	DOAJ
language	EN
topic	Neurospora crassa cellulose/hemicellulose signaling competitive inhibition filamentous fungi plant cell wall degradation Microbiology QR1-502
spellingShingle	Neurospora crassa cellulose/hemicellulose signaling competitive inhibition filamentous fungi plant cell wall degradation Microbiology QR1-502 Lara Hassan Liangcai Lin Hagit Sorek Laura E. Sperl Thomas Goudoulas Franz Hagn Natalie Germann Chaoguang Tian J. Philipp Benz Crosstalk of Cellulose and Mannan Perception Pathways Leads to Inhibition of Cellulase Production in Several Filamentous Fungi
description	ABSTRACT It is essential for microbes to acquire information about their environment. Fungi use soluble degradation products of plant cell wall components to understand the substrate composition they grow on. Individual perception pathways have been well described. However, the interconnections between pathways remain poorly understood. In the present work, we provide evidence of crosstalk between the perception pathways for cellulose and the hemicellulose mannan being conserved in several filamentous fungi and leading to the inhibition of cellulase expression. We used the functional genomics tools available for Neurospora crassa to investigate this overlap at the molecular level. Crosstalk and competitive inhibition could be identified both during uptake by cellodextrin transporters and intracellularly. Importantly, the overlap is independent of CRE-1-mediated catabolite repression. These results provide novel insights into the regulatory networks of lignocellulolytic fungi and will contribute to the rational optimization of fungal enzyme production for efficient plant biomass depolymerization and utilization. IMPORTANCE In fungi, the production of enzymes for polysaccharide degradation is controlled by complex signaling networks. Previously, these networks were studied in response to simple sugars or single polysaccharides. Here, we tackled for the first time the molecular interplay between two seemingly unrelated perception pathways: those for cellulose and the hemicellulose (gluco)mannan. We identified a so far unknown competitive inhibition between the respective degradation products acting as signaling molecules. Competition was detected both at the level of the uptake and intracellularly, upstream of the main transcriptional regulator CLR-2. Our findings provide novel insights into the molecular communication between perception pathways. Also, they present possible targets for the improvement of industrial strains for higher cellulase production through the engineering of mannan insensitivity.
format	article
author	Lara Hassan Liangcai Lin Hagit Sorek Laura E. Sperl Thomas Goudoulas Franz Hagn Natalie Germann Chaoguang Tian J. Philipp Benz
author_facet	Lara Hassan Liangcai Lin Hagit Sorek Laura E. Sperl Thomas Goudoulas Franz Hagn Natalie Germann Chaoguang Tian J. Philipp Benz
author_sort	Lara Hassan
title	Crosstalk of Cellulose and Mannan Perception Pathways Leads to Inhibition of Cellulase Production in Several Filamentous Fungi
title_short	Crosstalk of Cellulose and Mannan Perception Pathways Leads to Inhibition of Cellulase Production in Several Filamentous Fungi
title_full	Crosstalk of Cellulose and Mannan Perception Pathways Leads to Inhibition of Cellulase Production in Several Filamentous Fungi
title_fullStr	Crosstalk of Cellulose and Mannan Perception Pathways Leads to Inhibition of Cellulase Production in Several Filamentous Fungi
title_full_unstemmed	Crosstalk of Cellulose and Mannan Perception Pathways Leads to Inhibition of Cellulase Production in Several Filamentous Fungi
title_sort	crosstalk of cellulose and mannan perception pathways leads to inhibition of cellulase production in several filamentous fungi
publisher	American Society for Microbiology
publishDate	2019
url	https://doaj.org/article/b6dea3630057434590e8606a84909d21
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Crosstalk of Cellulose and Mannan Perception Pathways Leads to Inhibition of Cellulase Production in Several Filamentous Fungi

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