Heterotrimeric G-Protein Signaling Is Required for Cellulose Degradation in <named-content content-type="genus-species">Neurospora crassa</named-content>

ABSTRACT The filamentous fungus Neurospora crassa decomposes lignocellulosic biomass to generate soluble sugars as carbon sources. In this study, we investigated a role for heterotrimeric G-protein signaling in cellulose degradation. Loss of the Gα subunit genes gna-1 and gna-3, the Gβ subunit genes...

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Autores principales:	Logan A. Collier, Arit Ghosh, Katherine A. Borkovich
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2020
Materias:	G proteins cell signaling cellulolytic enzymes cyclic AMP filamentous fungi lignocellulose Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/cad0450f8a834cb2ac4ffcd534f9d676
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spelling	oai:doaj.org-article:cad0450f8a834cb2ac4ffcd534f9d6762021-11-15T15:55:43ZHeterotrimeric G-Protein Signaling Is Required for Cellulose Degradation in <named-content content-type="genus-species">Neurospora crassa</named-content>10.1128/mBio.02419-202150-7511https://doaj.org/article/cad0450f8a834cb2ac4ffcd534f9d6762020-12-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.02419-20https://doaj.org/toc/2150-7511ABSTRACT The filamentous fungus Neurospora crassa decomposes lignocellulosic biomass to generate soluble sugars as carbon sources. In this study, we investigated a role for heterotrimeric G-protein signaling in cellulose degradation. Loss of the Gα subunit genes gna-1 and gna-3, the Gβ subunit genes gnb-1 and cpc-2, the Gγ gene gng-1, or the gene for downstream effector adenylyl cyclase (cr-1) resulted in loss of detectable cellulase activity. This defect was also observed in strains expressing a constitutively active version of gna-3 (gna-3Q208L). We found that GNA-1 levels are greatly reduced in Δgna-3, Δgnb-1, and Δgng-1 strains, likely contributing to cellulase defects in these genetic backgrounds. The observation that gna-3Q208L Δgnb-1 strains exhibit cellulase activity, despite greatly reduced levels of GNA-1 protein, is consistent with positive control of cellulase production by GNA-3 that is manifested in the absence of gnb-1. Expression patterns for five cellulase genes showed that Δgna-1, Δgnb-1, and Δgna-3 mutants produce less cellulase mRNA than the wild type, consistent with transcriptional regulation. Δcpc-2 mutants had wild-type levels of cellulase transcripts, suggesting posttranscriptional control. In contrast, results for Δcr-1 mutants support both transcriptional and posttranscriptional control of cellulase activity by cAMP signaling. Cellulase activity defects in Δgna-3 mutants were fully remediated by cAMP supplementation, consistent with GNA-3 operating upstream of cAMP signaling. In contrast, cAMP addition only partially corrected cellulase activity defects in Δgna-1 and Δgnb-1 mutants, suggesting participation of GNA-1 and GNB-1 in additional cAMP-independent pathways that control cellulase activity. IMPORTANCE Filamentous fungi are critical for the recycling of plant litter in the biosphere by degrading lignocellulosic biomass into simpler compounds for metabolism. Both saprophytic and pathogenic fungi utilize plant cell wall-degrading enzymes to liberate carbon for metabolism. Several studies have demonstrated a role for cellulase enzymes during infection of economically relevant crops by fungal pathogens. Especially in developing countries, severe plant disease means loss of entire crops, sometimes leading to starvation. In this study, we demonstrate that G-protein signaling is a key component of cellulase production. Therefore, understanding the role of G-protein signaling in the regulation of the unique metabolism of cellulose by these organisms can inform innovations in strain engineering of industrially relevant species for biofuel production and in combatting food shortages caused by plant pathogens.Logan A. CollierArit GhoshKatherine A. BorkovichAmerican Society for MicrobiologyarticleG proteinscell signalingcellulolytic enzymescyclic AMPfilamentous fungilignocelluloseMicrobiologyQR1-502ENmBio, Vol 11, Iss 6 (2020)
institution	DOAJ
collection	DOAJ
language	EN
topic	G proteins cell signaling cellulolytic enzymes cyclic AMP filamentous fungi lignocellulose Microbiology QR1-502
spellingShingle	G proteins cell signaling cellulolytic enzymes cyclic AMP filamentous fungi lignocellulose Microbiology QR1-502 Logan A. Collier Arit Ghosh Katherine A. Borkovich Heterotrimeric G-Protein Signaling Is Required for Cellulose Degradation in <named-content content-type="genus-species">Neurospora crassa</named-content>
description	ABSTRACT The filamentous fungus Neurospora crassa decomposes lignocellulosic biomass to generate soluble sugars as carbon sources. In this study, we investigated a role for heterotrimeric G-protein signaling in cellulose degradation. Loss of the Gα subunit genes gna-1 and gna-3, the Gβ subunit genes gnb-1 and cpc-2, the Gγ gene gng-1, or the gene for downstream effector adenylyl cyclase (cr-1) resulted in loss of detectable cellulase activity. This defect was also observed in strains expressing a constitutively active version of gna-3 (gna-3Q208L). We found that GNA-1 levels are greatly reduced in Δgna-3, Δgnb-1, and Δgng-1 strains, likely contributing to cellulase defects in these genetic backgrounds. The observation that gna-3Q208L Δgnb-1 strains exhibit cellulase activity, despite greatly reduced levels of GNA-1 protein, is consistent with positive control of cellulase production by GNA-3 that is manifested in the absence of gnb-1. Expression patterns for five cellulase genes showed that Δgna-1, Δgnb-1, and Δgna-3 mutants produce less cellulase mRNA than the wild type, consistent with transcriptional regulation. Δcpc-2 mutants had wild-type levels of cellulase transcripts, suggesting posttranscriptional control. In contrast, results for Δcr-1 mutants support both transcriptional and posttranscriptional control of cellulase activity by cAMP signaling. Cellulase activity defects in Δgna-3 mutants were fully remediated by cAMP supplementation, consistent with GNA-3 operating upstream of cAMP signaling. In contrast, cAMP addition only partially corrected cellulase activity defects in Δgna-1 and Δgnb-1 mutants, suggesting participation of GNA-1 and GNB-1 in additional cAMP-independent pathways that control cellulase activity. IMPORTANCE Filamentous fungi are critical for the recycling of plant litter in the biosphere by degrading lignocellulosic biomass into simpler compounds for metabolism. Both saprophytic and pathogenic fungi utilize plant cell wall-degrading enzymes to liberate carbon for metabolism. Several studies have demonstrated a role for cellulase enzymes during infection of economically relevant crops by fungal pathogens. Especially in developing countries, severe plant disease means loss of entire crops, sometimes leading to starvation. In this study, we demonstrate that G-protein signaling is a key component of cellulase production. Therefore, understanding the role of G-protein signaling in the regulation of the unique metabolism of cellulose by these organisms can inform innovations in strain engineering of industrially relevant species for biofuel production and in combatting food shortages caused by plant pathogens.
format	article
author	Logan A. Collier Arit Ghosh Katherine A. Borkovich
author_facet	Logan A. Collier Arit Ghosh Katherine A. Borkovich
author_sort	Logan A. Collier
title	Heterotrimeric G-Protein Signaling Is Required for Cellulose Degradation in <named-content content-type="genus-species">Neurospora crassa</named-content>
title_short	Heterotrimeric G-Protein Signaling Is Required for Cellulose Degradation in <named-content content-type="genus-species">Neurospora crassa</named-content>
title_full	Heterotrimeric G-Protein Signaling Is Required for Cellulose Degradation in <named-content content-type="genus-species">Neurospora crassa</named-content>
title_fullStr	Heterotrimeric G-Protein Signaling Is Required for Cellulose Degradation in <named-content content-type="genus-species">Neurospora crassa</named-content>
title_full_unstemmed	Heterotrimeric G-Protein Signaling Is Required for Cellulose Degradation in <named-content content-type="genus-species">Neurospora crassa</named-content>
title_sort	heterotrimeric g-protein signaling is required for cellulose degradation in <named-content content-type="genus-species">neurospora crassa</named-content>
publisher	American Society for Microbiology
publishDate	2020
url	https://doaj.org/article/cad0450f8a834cb2ac4ffcd534f9d676
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Heterotrimeric G-Protein Signaling Is Required for Cellulose Degradation in <named-content content-type="genus-species">Neurospora crassa</named-content>

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