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Twists and turns in the salicylate catabolism of aspergillus terreus, revealing new roles of the 3-hydroxyanthranilate pathway

2021-01-26Artigo científico Acesso aberto
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dc.contributor.authorMartins, Tiago M.
dc.contributor.authorMartins, Celso
dc.contributor.authorGuedes, Paula
dc.contributor.authorPereira, Cristina Silva
dc.contributor.institutionInstituto de Tecnologia Química e Biológica António Xavier (ITQB)
dc.contributor.institutionCENSE - Centro de Investigação em Ambiente e Sustentabilidade
dc.contributor.institutionDCEA - Departamento de Ciências e Engenharia do Ambiente
dc.contributor.pblAmerican Society for Microbiology
dc.date.accessioned2022-02-01T03:28:27Z
dc.date.available2022-02-01T03:28:27Z
dc.date.issued2021-01-26
dc.descriptionThis work was financially supported by Fundacao para a Ciencia e a Tecnologia (FCT), project MOSTMICRO ITQB with reference no. UIDB/04612/2020 and UIDP/04612/2020, and by project "PinusResina" no. PDR2020-101-031905, funded by PDR2020 through Portugal2020. This research was carried out through a partnership with the RESOLUTION LAB, an infrastructure at NOVA School of Science and Technology. The authors acknowledge and thank the support given by the Portuguese Foundation for Science and Technology (FCT) to CENSE through the strategic project UIDB/04085/2020. T.M. and C.M. are grateful to FCT for the working contract financed by national funds under Norma Transitoria D.L. no. 57/2016 and the fellowship SFRH/BD/118377/2016, respectively.
dc.description.abstractIn 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.en
dc.description.versionpublishersversion
dc.description.versionpublished
dc.format.extent3207123
dc.identifier.doi10.1128/mSystems.00230-20
dc.identifier.issn2379-5077
dc.identifier.otherPURE: 28050934
dc.identifier.otherPURE UUID: 96ffbcb1-56d7-445d-999c-2d880330d5f2
dc.identifier.otherScopus: 85100307414
dc.identifier.otherPubMed: 33500329
dc.identifier.otherPubMedCentral: PMC7842363
dc.identifier.otherWOS: 000647691000025
dc.identifier.urihttp://hdl.handle.net/10362/131972
dc.identifier.urlhttps://www.scopus.com/pages/publications/85100307414
dc.language.isoeng
dc.peerreviewedyes
dc.subject3-oxoadipate pathway
dc.subjectAromatic compound catabolism
dc.subjectAspergillus nidulans
dc.subjectAspergillus terreus
dc.subjectGentisate
dc.subjectNicotinate catabolism
dc.subjectRNA-seq
dc.subjectSaprophytic Ascomycota
dc.subjectSecondary metabolism
dc.subjectTryptophan kynurenine pathway
dc.subjectMicrobiology
dc.subjectPhysiology
dc.subjectBiochemistry
dc.subjectEcology, Evolution, Behavior and Systematics
dc.subjectModelling and Simulation
dc.subjectMolecular Biology
dc.subjectGenetics
dc.subjectComputer Science Applications
dc.subjectSDG 7 - Affordable and Clean Energy
dc.titleTwists and turns in the salicylate catabolism of aspergillus terreus, revealing new roles of the 3-hydroxyanthranilate pathwayen
dc.typejournal article
degois.publication.issue1
degois.publication.titlemSystems
degois.publication.volume6
dspace.entity.typePublication
rcaap.rightsopenAccess

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