The ribonuclease PNPase is a key regulator of biofilm formation in Listeria monocytogenes and affects invasion of host cells
| Autor(a) principal: | |
|---|---|
| Data de Publicação: | 2023 |
| Outros Autores: | , , , , , |
| Tipo de documento: | Artigo |
| Idioma: | eng |
| Título da fonte: | Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos) |
| Texto Completo: | http://hdl.handle.net/10362/165713 |
| Resumo: | Funding Information: This work was supported by FCT-Fundação para a Ciência e a Tecnologia, I.P., through: MOSTMICRO-ITQB R&D Unit (UIDB/04612/2020, UIDP/04612/2020); LS4FUTURE Associated Laboratory (LA/P/0087/2020); Grant PTDC/BIA-MIC/32525/2017 to J.M.A.; Doctoral Fellowship to A.P.Q. (PD/BD/135487/2018); FCT contracts according to DL57/2016 to S.N.P. (SFRH/BPD/92409/2013) and to V.P. (SFRH/BPD/87188/2012). Publisher Copyright: © 2023, The Author(s). |
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The ribonuclease PNPase is a key regulator of biofilm formation in Listeria monocytogenes and affects invasion of host cellsBiotechnologyMicrobiologyApplied Microbiology and BiotechnologyFunding Information: This work was supported by FCT-Fundação para a Ciência e a Tecnologia, I.P., through: MOSTMICRO-ITQB R&D Unit (UIDB/04612/2020, UIDP/04612/2020); LS4FUTURE Associated Laboratory (LA/P/0087/2020); Grant PTDC/BIA-MIC/32525/2017 to J.M.A.; Doctoral Fellowship to A.P.Q. (PD/BD/135487/2018); FCT contracts according to DL57/2016 to S.N.P. (SFRH/BPD/92409/2013) and to V.P. (SFRH/BPD/87188/2012). Publisher Copyright: © 2023, The Author(s).Biofilms provide an environment that protects microorganisms from external stresses such as nutrient deprivation, antibiotic treatments, and immune defences, thereby creating favorable conditions for bacterial survival and pathogenesis. Here we show that the RNA-binding protein and ribonuclease polynucleotide phosphorylase (PNPase) is a positive regulator of biofilm formation in the human pathogen Listeria monocytogenes, a major responsible for food contamination in food-processing environments. The PNPase mutant strain produces less biofilm biomass and exhibits an altered biofilm morphology that is more susceptible to antibiotic treatment. Through biochemical assays and microscopical analysis, we demonstrate that PNPase is a previously unrecognized regulator of the composition of the biofilm extracellular matrix, greatly affecting the levels of proteins, extracellular DNA, and sugars. Noteworthy, we have adapted the use of the fluorescent complex ruthenium red-phenanthroline for the detection of polysaccharides in Listeria biofilms. Transcriptomic analysis of wild-type and PNPase mutant biofilms reveals that PNPase impacts many regulatory pathways associated with biofilm formation, particularly by affecting the expression of genes involved in the metabolism of carbohydrates (e.g., lmo0096 and lmo0783, encoding PTS components), of amino acids (e.g., lmo1984 and lmo2006, encoding biosynthetic enzymes) and in the Agr quorum sensing-like system (lmo0048-49). Moreover, we show that PNPase affects mRNA levels of the master regulator of virulence PrfA and PrfA-regulated genes, and these results could help to explain the reduced bacterial internalization in human cells of the ΔpnpA mutant. Overall, this work demonstrates that PNPase is an important post-transcriptional regulator for virulence and adaptation to the biofilm lifestyle of Gram-positive bacteria and highlights the expanding role of ribonucleases as critical players in pathogenicity.Instituto de Tecnologia Química e Biológica António Xavier (ITQB)RUNQuendera, Ana PatríciaPinto, Sandra NunesPobre, VâniaAntunes, WilsonBonifácio, Vasco D.B.Arraiano, Cecília MariaAndrade, José Marques2024-04-02T23:18:18Z2023-122023-12-01T00:00:00Zinfo:eu-repo/semantics/publishedVersioninfo:eu-repo/semantics/articleapplication/pdfhttp://hdl.handle.net/10362/165713eng2055-5008PURE: 72012455https://doi.org/10.1038/s41522-023-00397-1info:eu-repo/semantics/openAccessreponame:Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos)instname:Agência para a Sociedade do Conhecimento (UMIC) - FCT - Sociedade da Informaçãoinstacron:RCAAP2024-05-22T18:20:06Zoai:run.unl.pt:10362/165713Portal AgregadorONGhttps://www.rcaap.pt/oai/openairemluisa.alvim@gmail.comopendoar:71602024-05-22T18:20:06Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos) - Agência para a Sociedade do Conhecimento (UMIC) - FCT - Sociedade da Informaçãofalse |
| dc.title.none.fl_str_mv |
The ribonuclease PNPase is a key regulator of biofilm formation in Listeria monocytogenes and affects invasion of host cells |
| title |
The ribonuclease PNPase is a key regulator of biofilm formation in Listeria monocytogenes and affects invasion of host cells |
| spellingShingle |
The ribonuclease PNPase is a key regulator of biofilm formation in Listeria monocytogenes and affects invasion of host cells Quendera, Ana Patrícia Biotechnology Microbiology Applied Microbiology and Biotechnology |
| title_short |
The ribonuclease PNPase is a key regulator of biofilm formation in Listeria monocytogenes and affects invasion of host cells |
| title_full |
The ribonuclease PNPase is a key regulator of biofilm formation in Listeria monocytogenes and affects invasion of host cells |
| title_fullStr |
The ribonuclease PNPase is a key regulator of biofilm formation in Listeria monocytogenes and affects invasion of host cells |
| title_full_unstemmed |
The ribonuclease PNPase is a key regulator of biofilm formation in Listeria monocytogenes and affects invasion of host cells |
| title_sort |
The ribonuclease PNPase is a key regulator of biofilm formation in Listeria monocytogenes and affects invasion of host cells |
| author |
Quendera, Ana Patrícia |
| author_facet |
Quendera, Ana Patrícia Pinto, Sandra Nunes Pobre, Vânia Antunes, Wilson Bonifácio, Vasco D.B. Arraiano, Cecília Maria Andrade, José Marques |
| author_role |
author |
| author2 |
Pinto, Sandra Nunes Pobre, Vânia Antunes, Wilson Bonifácio, Vasco D.B. Arraiano, Cecília Maria Andrade, José Marques |
| author2_role |
author author author author author author |
| dc.contributor.none.fl_str_mv |
Instituto de Tecnologia Química e Biológica António Xavier (ITQB) RUN |
| dc.contributor.author.fl_str_mv |
Quendera, Ana Patrícia Pinto, Sandra Nunes Pobre, Vânia Antunes, Wilson Bonifácio, Vasco D.B. Arraiano, Cecília Maria Andrade, José Marques |
| dc.subject.por.fl_str_mv |
Biotechnology Microbiology Applied Microbiology and Biotechnology |
| topic |
Biotechnology Microbiology Applied Microbiology and Biotechnology |
| description |
Funding Information: This work was supported by FCT-Fundação para a Ciência e a Tecnologia, I.P., through: MOSTMICRO-ITQB R&D Unit (UIDB/04612/2020, UIDP/04612/2020); LS4FUTURE Associated Laboratory (LA/P/0087/2020); Grant PTDC/BIA-MIC/32525/2017 to J.M.A.; Doctoral Fellowship to A.P.Q. (PD/BD/135487/2018); FCT contracts according to DL57/2016 to S.N.P. (SFRH/BPD/92409/2013) and to V.P. (SFRH/BPD/87188/2012). Publisher Copyright: © 2023, The Author(s). |
| publishDate |
2023 |
| dc.date.none.fl_str_mv |
2023-12 2023-12-01T00:00:00Z 2024-04-02T23:18:18Z |
| dc.type.status.fl_str_mv |
info:eu-repo/semantics/publishedVersion |
| dc.type.driver.fl_str_mv |
info:eu-repo/semantics/article |
| format |
article |
| status_str |
publishedVersion |
| dc.identifier.uri.fl_str_mv |
http://hdl.handle.net/10362/165713 |
| url |
http://hdl.handle.net/10362/165713 |
| dc.language.iso.fl_str_mv |
eng |
| language |
eng |
| dc.relation.none.fl_str_mv |
2055-5008 PURE: 72012455 https://doi.org/10.1038/s41522-023-00397-1 |
| dc.rights.driver.fl_str_mv |
info:eu-repo/semantics/openAccess |
| eu_rights_str_mv |
openAccess |
| dc.format.none.fl_str_mv |
application/pdf |
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reponame:Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos) instname:Agência para a Sociedade do Conhecimento (UMIC) - FCT - Sociedade da Informação instacron:RCAAP |
| instname_str |
Agência para a Sociedade do Conhecimento (UMIC) - FCT - Sociedade da Informação |
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RCAAP |
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RCAAP |
| reponame_str |
Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos) |
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Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos) |
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Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos) - Agência para a Sociedade do Conhecimento (UMIC) - FCT - Sociedade da Informação |
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mluisa.alvim@gmail.com |
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1817545999807152128 |
