Publicação
Bringing up to date the toolkit for the catabolism of aromatic compounds in fungi
| Resumo: | Saprophytic fungi are able to catabolize many plant-derived aromatics, including, for example, gallate. The catabolism of gallate in fungi is assumed to depend on the five main central pathways, i.e., of the central intermediates' catechol, protocatechuate, hydroxyquinol, homogentisate and gentisate, but a definitive demonstration is lacking. To shed light on this process, we analysed the transcriptional reprogramming of the growth of Aspergillus terreus on gallate compared with acetate as the control condition. Surprisingly, the results revealed that the five main central pathways did not exhibit significant positive regulation. Instead, an in-depth analysis identified four highly expressed and upregulated genes that are part of a conserved gene cluster found in numerous species of fungi, though not in Aspergilli. The cluster comprises a monooxygenase gene and a fumarylacetoacetate hydrolase-like gene, which are recognized as key components of catabolic pathways responsible for aromatic compound degradation. The other two genes encode proteins with no reported enzymatic activities. Through functional analyses of gene deletion mutants in Aspergillus nidulans, the conserved short protein with no known domains could be linked to the conversion of the novel metabolite 5-hydroxydienelatone, whereas the DUF3500 gene likely encodes a ring-cleavage enzyme for 1,2,3,5-tetrahydroxybenzene. These significant findings establish the existence of a new 1,2,3,5-tetrahydroxybenzene central pathway for the catabolism of gallate and related compounds (e.g. 2,4,6-trihydroxybenzoate) in numerous fungi where this catabolic gene cluster was observed. |
|---|---|
| Autores principais: | Martins, Tiago M. |
| Outros Autores: | Bento, Artur; Martins, Celso; Tomé, Ana S.; Moreira, Carlos J.S.; Silva Pereira, Cristina |
| Assunto: | Biotechnology Bioengineering Biochemistry Applied Microbiology and Biotechnology |
| Ano: | 2024 |
| País: | Portugal |
| Tipo de documento: | artigo |
| Tipo de acesso: | acesso aberto |
| Instituição associada: | Universidade Nova de Lisboa |
| Idioma: | inglês |
| Origem: | Repositório Institucional da UNL |
| _version_ | 1879446136230510592 |
|---|---|
| author | Martins, Tiago M. |
| author2 | Bento, Artur Martins, Celso Tomé, Ana S. Moreira, Carlos J.S. Silva Pereira, Cristina |
| author2_role | author author author author author |
| author_facet | Martins, Tiago M. Bento, Artur Martins, Celso Tomé, Ana S. Moreira, Carlos J.S. Silva Pereira, Cristina |
| author_role | author |
| contributor_name_str_mv | Instituto de Tecnologia Química e Biológica António Xavier (ITQB) Blackwell RUN |
| country_str | PT |
| creators_json_txt | [{\"Person.name\":\"Martins, Tiago M.\"},{\"Person.name\":\"Bento, Artur\"},{\"Person.name\":\"Martins, Celso\"},{\"Person.name\":\"Tomé, Ana S.\"},{\"Person.name\":\"Moreira, Carlos J.S.\"},{\"Person.name\":\"Silva Pereira, Cristina\"}] |
| datacite.contributors.contributor.contributorName.fl_str_mv | Instituto de Tecnologia Química e Biológica António Xavier (ITQB) Blackwell RUN |
| datacite.creators.creator.creatorName.fl_str_mv | Martins, Tiago M. Bento, Artur Martins, Celso Tomé, Ana S. Moreira, Carlos J.S. Silva Pereira, Cristina |
| datacite.date.Accepted.fl_str_mv | 2024-01-01T00:00:00Z |
| datacite.date.available.fl_str_mv | 2024-09-30T22:25:32Z |
| datacite.date.embargoed.fl_str_mv | 2024-09-30T22:25:32Z |
| datacite.rights.fl_str_mv | http://purl.org/coar/access_right/c_abf2 |
| datacite.subjects.subject.fl_str_mv | Biotechnology Bioengineering Biochemistry Applied Microbiology and Biotechnology |
| datacite.titles.title.fl_str_mv | Bringing up to date the toolkit for the catabolism of aromatic compounds in fungi The unexpected 1,2,3,5-tetrahydroxybenzene central pathway |
| dc.contributor.none.fl_str_mv | Instituto de Tecnologia Química e Biológica António Xavier (ITQB) Blackwell RUN |
| dc.creator.none.fl_str_mv | Martins, Tiago M. Bento, Artur Martins, Celso Tomé, Ana S. Moreira, Carlos J.S. Silva Pereira, Cristina |
| dc.date.Accepted.fl_str_mv | 2024-01-01T00:00:00Z |
| dc.date.available.fl_str_mv | 2024-09-30T22:25:32Z |
| dc.date.embargoed.fl_str_mv | 2024-09-30T22:25:32Z |
| dc.format.none.fl_str_mv | application/pdf |
| dc.identifier.none.fl_str_mv | http://hdl.handle.net/10362/172691 |
| dc.language.none.fl_str_mv | eng |
| dc.rights.none.fl_str_mv | http://purl.org/coar/access_right/c_abf2 |
| dc.subject.none.fl_str_mv | Biotechnology Bioengineering Biochemistry Applied Microbiology and Biotechnology |
| dc.title.fl_str_mv | Bringing up to date the toolkit for the catabolism of aromatic compounds in fungi The unexpected 1,2,3,5-tetrahydroxybenzene central pathway |
| dc.type.none.fl_str_mv | http://purl.org/coar/resource_type/c_6501 |
| description | Saprophytic fungi are able to catabolize many plant-derived aromatics, including, for example, gallate. The catabolism of gallate in fungi is assumed to depend on the five main central pathways, i.e., of the central intermediates' catechol, protocatechuate, hydroxyquinol, homogentisate and gentisate, but a definitive demonstration is lacking. To shed light on this process, we analysed the transcriptional reprogramming of the growth of Aspergillus terreus on gallate compared with acetate as the control condition. Surprisingly, the results revealed that the five main central pathways did not exhibit significant positive regulation. Instead, an in-depth analysis identified four highly expressed and upregulated genes that are part of a conserved gene cluster found in numerous species of fungi, though not in Aspergilli. The cluster comprises a monooxygenase gene and a fumarylacetoacetate hydrolase-like gene, which are recognized as key components of catabolic pathways responsible for aromatic compound degradation. The other two genes encode proteins with no reported enzymatic activities. Through functional analyses of gene deletion mutants in Aspergillus nidulans, the conserved short protein with no known domains could be linked to the conversion of the novel metabolite 5-hydroxydienelatone, whereas the DUF3500 gene likely encodes a ring-cleavage enzyme for 1,2,3,5-tetrahydroxybenzene. These significant findings establish the existence of a new 1,2,3,5-tetrahydroxybenzene central pathway for the catabolism of gallate and related compounds (e.g. 2,4,6-trihydroxybenzoate) in numerous fungi where this catabolic gene cluster was observed. |
| dirty | 0 |
| eu_rights_str_mv | openAccess |
| format | article |
| fulltext.url.fl_str_mv | https://run.unl.pt/bitstreams/961a94eb-3dff-4b37-bd28-73c4167540fc/download |
| id | run_adbc8ed1f09e08f81d194e45ec3bf5b6 |
| identifier.url.fl_str_mv | http://hdl.handle.net/10362/172691 |
| inst_facet_str | urn:organizationAcronym:unl{{{_:::_}}}Universidade Nova de Lisboa |
| instacron_str | unl |
| institution | Universidade Nova de Lisboa |
| instname_str | Universidade Nova de Lisboa |
| language | eng |
| network_acronym_str | run |
| network_name_str | Repositório Institucional da UNL |
| oai_identifier_str | oai:run.unl.pt:10362/172691 |
| organization_str_mv | urn:organizationAcronym:unl |
| person_str_mv | Martins, Tiago M. Bento, Artur Martins, Celso Tomé, Ana S. Moreira, Carlos J.S. Silva Pereira, Cristina |
| publishDate | 2024 |
| repo_facet_str | urn:repositoryAcronym:run{{{_:::_}}}Repositório Institucional da UNL |
| reponame_str | Repositório Institucional da UNL |
| repository_id_str | urn:repositoryAcronym:run |
| service_str_mv | urn:repositoryAcronym:run |
| spelling | engenSaprophytic fungi are able to catabolize many plant-derived aromatics, including, for example, gallate. The catabolism of gallate in fungi is assumed to depend on the five main central pathways, i.e., of the central intermediates' catechol, protocatechuate, hydroxyquinol, homogentisate and gentisate, but a definitive demonstration is lacking. To shed light on this process, we analysed the transcriptional reprogramming of the growth of Aspergillus terreus on gallate compared with acetate as the control condition. Surprisingly, the results revealed that the five main central pathways did not exhibit significant positive regulation. Instead, an in-depth analysis identified four highly expressed and upregulated genes that are part of a conserved gene cluster found in numerous species of fungi, though not in Aspergilli. The cluster comprises a monooxygenase gene and a fumarylacetoacetate hydrolase-like gene, which are recognized as key components of catabolic pathways responsible for aromatic compound degradation. The other two genes encode proteins with no reported enzymatic activities. Through functional analyses of gene deletion mutants in Aspergillus nidulans, the conserved short protein with no known domains could be linked to the conversion of the novel metabolite 5-hydroxydienelatone, whereas the DUF3500 gene likely encodes a ring-cleavage enzyme for 1,2,3,5-tetrahydroxybenzene. These significant findings establish the existence of a new 1,2,3,5-tetrahydroxybenzene central pathway for the catabolism of gallate and related compounds (e.g. 2,4,6-trihydroxybenzoate) in numerous fungi where this catabolic gene cluster was observed.application/pdfenBringing up to date the toolkit for the catabolism of aromatic compounds in fungiSubtitleenThe unexpected 1,2,3,5-tetrahydroxybenzene central pathwayMartins, Tiago M.Bento, ArturMartins, CelsoTomé, Ana S.Moreira, Carlos J.S.Silva Pereira, CristinaInstituto de Tecnologia Química e Biológica António Xavier (ITQB)BlackwellHostingInstitutionOrganizationalRUNe-mailmailto:run@unl.ptrun@unl.ptISSNIsPartOf1751-7907URNIsPartOfPURE: 90704476URNIsPartOfPURE UUID: 753cba88-5e49-4407-9e8d-48110b25d6ffURNIsPartOfScopus: 85179304989URNIsPartOfPubMed: 38064205DOIIsPartOf10.1111/1751-7915.143712024-09-30T22:25:32Z2024-012024-01-01T00:00:00ZHandlehttp://hdl.handle.net/10362/172691http://purl.org/coar/access_right/c_abf2open accessBiotechnologyBioengineeringBiochemistryApplied Microbiology and Biotechnology22224408 bytesliteraturehttp://purl.org/coar/resource_type/c_6501journal articlehttp://purl.org/coar/access_right/c_abf2application/pdffulltexthttps://run.unl.pt/bitstreams/961a94eb-3dff-4b37-bd28-73c4167540fc/download |
| spellingShingle | Bringing up to date the toolkit for the catabolism of aromatic compounds in fungi Martins, Tiago M. Biotechnology Bioengineering Biochemistry Applied Microbiology and Biotechnology |
| status | SINGLETON |
| subject.fl_str_mv | Biotechnology Bioengineering Biochemistry Applied Microbiology and Biotechnology |
| title | Bringing up to date the toolkit for the catabolism of aromatic compounds in fungi |
| title_full | Bringing up to date the toolkit for the catabolism of aromatic compounds in fungi |
| title_fullStr | Bringing up to date the toolkit for the catabolism of aromatic compounds in fungi |
| title_full_unstemmed | Bringing up to date the toolkit for the catabolism of aromatic compounds in fungi |
| title_short | Bringing up to date the toolkit for the catabolism of aromatic compounds in fungi |
| title_sort | Bringing up to date the toolkit for the catabolism of aromatic compounds in fungi |
| topic | Biotechnology Bioengineering Biochemistry Applied Microbiology and Biotechnology |
| topic_facet | Biotechnology Bioengineering Biochemistry Applied Microbiology and Biotechnology |
| url | http://hdl.handle.net/10362/172691 |
| visible | 1 |
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