Twists and Turns in the Salicylate Catabolism of <italic toggle="yes">Aspergillus terreus</italic>, Revealing New Roles of the 3-Hydroxyanthranilate Pathway

ABSTRACT In fungi, salicylate catabolism was believed to proceed only through the catechol branch of the 3-oxoadipate pathway, as shown, e.g., in Aspergillus nidulans. However, the observation of a transient accumulation of gentisate upon the cultivation of Aspergillus terreus in salicylate medium q...

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Autores principales:	Tiago M. Martins, Celso Martins, Paula Guedes, Cristina Silva Pereira
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2021
Materias:	RNA-seq aromatic compound catabolism Aspergillus nidulans Aspergillus terreus 3-oxoadipate pathway gentisate Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/a38d1dfd845448fcb07334bce5fec955
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spelling	oai:doaj.org-article:a38d1dfd845448fcb07334bce5fec9552021-12-02T18:20:19ZTwists and Turns in the Salicylate Catabolism of <italic toggle="yes">Aspergillus terreus</italic>, Revealing New Roles of the 3-Hydroxyanthranilate Pathway10.1128/mSystems.00230-202379-5077https://doaj.org/article/a38d1dfd845448fcb07334bce5fec9552021-02-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.00230-20https://doaj.org/toc/2379-5077ABSTRACT In fungi, salicylate catabolism was believed to proceed only through the catechol branch of the 3-oxoadipate pathway, as shown, e.g., in Aspergillus nidulans. However, the observation of a transient accumulation of gentisate upon the cultivation of Aspergillus terreus in salicylate medium questions this concept. To address this, we have run a comparative analysis of the transcriptome of these two species after growth in salicylate using acetate as a control condition. The results revealed the high complexity of the salicylate metabolism in A. terreus with the concomitant positive regulation of several pathways for the catabolism of aromatic compounds. This included the unexpected joint action of two pathways—3-hydroxyanthranilate and nicotinate—possibly crucial for the catabolism of aromatics in this fungus. Importantly, the 3-hydroxyanthranilate catabolic pathway in fungi is described here for the first time, whereas new genes participating in the nicotinate metabolism are also proposed. The transcriptome analysis showed also for the two species an intimate relationship between salicylate catabolism and secondary metabolism. This study emphasizes that the central pathways for the catabolism of aromatic hydrocarbons in fungi hold many mysteries yet to be discovered. IMPORTANCE Aspergilli are versatile cell factories used in industry for the production of organic acids, enzymes, and pharmaceutical drugs. To date, bio-based production of organic acids relies on food substrates. These processes are currently being challenged to switch to renewable nonfood raw materials—a reality that should inspire the use of lignin-derived aromatic monomers. In this context, aspergilli emerge at the forefront of future bio-based approaches due to their industrial relevance and recognized prolific catabolism of aromatic compounds. Notwithstanding considerable advances in the field, there are still important knowledge gaps in the central catabolism of aromatic hydrocarbons in fungi. Here, we disclose a novel central pathway, 3-hydroxyanthranilate, defying previously established ideas on the central metabolism of the aromatic amino acid tryptophan in Ascomycota. We also observe that the catabolism of the aromatic salicylate greatly activated the secondary metabolism, furthering the significance of using lignin-derived aromatic hydrocarbons as a distinctive biomass source.Tiago M. MartinsCelso MartinsPaula GuedesCristina Silva PereiraAmerican Society for MicrobiologyarticleRNA-seqaromatic compound catabolismAspergillus nidulansAspergillus terreus3-oxoadipate pathwaygentisateMicrobiologyQR1-502ENmSystems, Vol 6, Iss 1 (2021)
institution	DOAJ
collection	DOAJ
language	EN
topic	RNA-seq aromatic compound catabolism Aspergillus nidulans Aspergillus terreus 3-oxoadipate pathway gentisate Microbiology QR1-502
spellingShingle	RNA-seq aromatic compound catabolism Aspergillus nidulans Aspergillus terreus 3-oxoadipate pathway gentisate Microbiology QR1-502 Tiago M. Martins Celso Martins Paula Guedes Cristina Silva Pereira Twists and Turns in the Salicylate Catabolism of <italic toggle="yes">Aspergillus terreus</italic>, Revealing New Roles of the 3-Hydroxyanthranilate Pathway
description	ABSTRACT In fungi, salicylate catabolism was believed to proceed only through the catechol branch of the 3-oxoadipate pathway, as shown, e.g., in Aspergillus nidulans. However, the observation of a transient accumulation of gentisate upon the cultivation of Aspergillus terreus in salicylate medium questions this concept. To address this, we have run a comparative analysis of the transcriptome of these two species after growth in salicylate using acetate as a control condition. The results revealed the high complexity of the salicylate metabolism in A. terreus with the concomitant positive regulation of several pathways for the catabolism of aromatic compounds. This included the unexpected joint action of two pathways—3-hydroxyanthranilate and nicotinate—possibly crucial for the catabolism of aromatics in this fungus. Importantly, the 3-hydroxyanthranilate catabolic pathway in fungi is described here for the first time, whereas new genes participating in the nicotinate metabolism are also proposed. The transcriptome analysis showed also for the two species an intimate relationship between salicylate catabolism and secondary metabolism. This study emphasizes that the central pathways for the catabolism of aromatic hydrocarbons in fungi hold many mysteries yet to be discovered. IMPORTANCE Aspergilli are versatile cell factories used in industry for the production of organic acids, enzymes, and pharmaceutical drugs. To date, bio-based production of organic acids relies on food substrates. These processes are currently being challenged to switch to renewable nonfood raw materials—a reality that should inspire the use of lignin-derived aromatic monomers. In this context, aspergilli emerge at the forefront of future bio-based approaches due to their industrial relevance and recognized prolific catabolism of aromatic compounds. Notwithstanding considerable advances in the field, there are still important knowledge gaps in the central catabolism of aromatic hydrocarbons in fungi. Here, we disclose a novel central pathway, 3-hydroxyanthranilate, defying previously established ideas on the central metabolism of the aromatic amino acid tryptophan in Ascomycota. We also observe that the catabolism of the aromatic salicylate greatly activated the secondary metabolism, furthering the significance of using lignin-derived aromatic hydrocarbons as a distinctive biomass source.
format	article
author	Tiago M. Martins Celso Martins Paula Guedes Cristina Silva Pereira
author_facet	Tiago M. Martins Celso Martins Paula Guedes Cristina Silva Pereira
author_sort	Tiago M. Martins
title	Twists and Turns in the Salicylate Catabolism of <italic toggle="yes">Aspergillus terreus</italic>, Revealing New Roles of the 3-Hydroxyanthranilate Pathway
title_short	Twists and Turns in the Salicylate Catabolism of <italic toggle="yes">Aspergillus terreus</italic>, Revealing New Roles of the 3-Hydroxyanthranilate Pathway
title_full	Twists and Turns in the Salicylate Catabolism of <italic toggle="yes">Aspergillus terreus</italic>, Revealing New Roles of the 3-Hydroxyanthranilate Pathway
title_fullStr	Twists and Turns in the Salicylate Catabolism of <italic toggle="yes">Aspergillus terreus</italic>, Revealing New Roles of the 3-Hydroxyanthranilate Pathway
title_full_unstemmed	Twists and Turns in the Salicylate Catabolism of <italic toggle="yes">Aspergillus terreus</italic>, Revealing New Roles of the 3-Hydroxyanthranilate Pathway
title_sort	twists and turns in the salicylate catabolism of <italic toggle="yes">aspergillus terreus</italic>, revealing new roles of the 3-hydroxyanthranilate pathway
publisher	American Society for Microbiology
publishDate	2021
url	https://doaj.org/article/a38d1dfd845448fcb07334bce5fec955
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Twists and Turns in the Salicylate Catabolism of <italic toggle="yes">Aspergillus terreus</italic>, Revealing New Roles of the 3-Hydroxyanthranilate Pathway

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