Phage SEP1 hijacks Staphylococcus epidermidis stationary cells metabolism to replicate

Bibliographic Details
Main Author: Silva, Maria Daniela
Publication Date: 2024
Other Authors: Pinto, Graça, França, Ângela Maria Oliveira Sousa, Azeredo, Joana, Melo, Luís Daniel Rodrigues
Format: Article
Language: eng
Source: Repositórios Científicos de Acesso Aberto de Portugal (RCAAP)
Download full: https://hdl.handle.net/1822/93033
Summary: In nature, bacteria often survive in a stationary state with low metabolic activity. Phages use the metabolic machinery of the host cell to replicate, and, therefore, their efficacy against non-dividing cells is usually limited. Nevertheless, it was previously shown that the Staphylococcus epidermidis phage SEP1 has the remarkable capacity to actively replicate in stationary-phase cells, reducing their numbers. Here, we studied for the first time the transcriptomic profiles of both exponential and stationary cells infected with SEP1 phage using RNA-seq to gain a better understanding of this rare phenomenon. We showed that SEP1 successfully takes over the transcriptional apparatus of both exponential and stationary cells. Infection was, however, delayed in stationary cells, with genes within the gp142-gp154 module putatively implicated in host takeover. S. epidermidis responded to SEP1 infection by upregulating three genes involved in a DNA modification system, with this being observed already 5 min after infection in exponential cells and later in stationary cells. In stationary cells, a significant number of genes involved in translation and RNA metabolic and biosynthetic processes were upregulated after 15 and 30 min of SEP1 infection in comparison with the uninfected control, showing that SEP1 activates metabolic and biosynthetic pathways necessary to its successful replication.
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spelling Phage SEP1 hijacks Staphylococcus epidermidis stationary cells metabolism to replicatephagephage-host interactionRNA-seqstationary cellsIn nature, bacteria often survive in a stationary state with low metabolic activity. Phages use the metabolic machinery of the host cell to replicate, and, therefore, their efficacy against non-dividing cells is usually limited. Nevertheless, it was previously shown that the Staphylococcus epidermidis phage SEP1 has the remarkable capacity to actively replicate in stationary-phase cells, reducing their numbers. Here, we studied for the first time the transcriptomic profiles of both exponential and stationary cells infected with SEP1 phage using RNA-seq to gain a better understanding of this rare phenomenon. We showed that SEP1 successfully takes over the transcriptional apparatus of both exponential and stationary cells. Infection was, however, delayed in stationary cells, with genes within the gp142-gp154 module putatively implicated in host takeover. S. epidermidis responded to SEP1 infection by upregulating three genes involved in a DNA modification system, with this being observed already 5 min after infection in exponential cells and later in stationary cells. In stationary cells, a significant number of genes involved in translation and RNA metabolic and biosynthetic processes were upregulated after 15 and 30 min of SEP1 infection in comparison with the uninfected control, showing that SEP1 activates metabolic and biosynthetic pathways necessary to its successful replication.This study was supported by the Portuguese Foundation for Science and Technology (FCT) under the scope of the strategic funding of UIDB/04469/2020 unit and project PTDC/BIA-MIC/2312/2020 and by LABBELS–Associate Laboratory in Biotech nology, Bioengineering and Microelectromechanical Systems, LA/P/0029/2020. A.F. acknowledges funding from the FCT through the DL57/2016 program (DL 57/2016/CP1377/CT0032) and L.D.R.M. through the Scientific Employment Stimulus Program (2021.00221.CEECIND).info:eu-repo/semantics/publishedVersionAmerican Society for MicrobiologyUniversidade do MinhoSilva, Maria DanielaPinto, GraçaFrança, Ângela Maria Oliveira SousaAzeredo, JoanaMelo, Luís Daniel Rodrigues2024-06-212024-06-21T00:00:00Zinfo:eu-repo/semantics/publishedVersioninfo:eu-repo/semantics/articleapplication/pdfhttps://hdl.handle.net/1822/93033engSilva, M. D., Pinto, G., França, A., Azeredo, J., & Melo, L. D. R. (2024, July 23). Phage SEP1 hijacks Staphylococcus epidermidis stationary cells’ metabolism to replicate. (D. W. Cleary, Ed.), mSystems. American Society for Microbiology. http://doi.org/10.1128/msystems.00263-242379-507710.1128/msystems.00263-2438904376https://journals.asm.org/doi/10.1128/msystems.00263-24info:eu-repo/semantics/openAccessreponame:Repositórios Científicos de Acesso Aberto de Portugal (RCAAP)instname:FCCN, serviços digitais da FCT – Fundação para a Ciência e a Tecnologiainstacron:RCAAP2025-03-29T01:45:42Zoai:repositorium.sdum.uminho.pt:1822/93033Portal AgregadorONGhttps://www.rcaap.pt/oai/openaireinfo@rcaap.ptopendoar:https://opendoar.ac.uk/repository/71602025-05-28T18:49:36.719626Repositórios Científicos de Acesso Aberto de Portugal (RCAAP) - FCCN, serviços digitais da FCT – Fundação para a Ciência e a Tecnologiafalse
dc.title.none.fl_str_mv Phage SEP1 hijacks Staphylococcus epidermidis stationary cells metabolism to replicate
title Phage SEP1 hijacks Staphylococcus epidermidis stationary cells metabolism to replicate
spellingShingle Phage SEP1 hijacks Staphylococcus epidermidis stationary cells metabolism to replicate
Silva, Maria Daniela
phage
phage-host interaction
RNA-seq
stationary cells
title_short Phage SEP1 hijacks Staphylococcus epidermidis stationary cells metabolism to replicate
title_full Phage SEP1 hijacks Staphylococcus epidermidis stationary cells metabolism to replicate
title_fullStr Phage SEP1 hijacks Staphylococcus epidermidis stationary cells metabolism to replicate
title_full_unstemmed Phage SEP1 hijacks Staphylococcus epidermidis stationary cells metabolism to replicate
title_sort Phage SEP1 hijacks Staphylococcus epidermidis stationary cells metabolism to replicate
author Silva, Maria Daniela
author_facet Silva, Maria Daniela
Pinto, Graça
França, Ângela Maria Oliveira Sousa
Azeredo, Joana
Melo, Luís Daniel Rodrigues
author_role author
author2 Pinto, Graça
França, Ângela Maria Oliveira Sousa
Azeredo, Joana
Melo, Luís Daniel Rodrigues
author2_role author
author
author
author
dc.contributor.none.fl_str_mv Universidade do Minho
dc.contributor.author.fl_str_mv Silva, Maria Daniela
Pinto, Graça
França, Ângela Maria Oliveira Sousa
Azeredo, Joana
Melo, Luís Daniel Rodrigues
dc.subject.por.fl_str_mv phage
phage-host interaction
RNA-seq
stationary cells
topic phage
phage-host interaction
RNA-seq
stationary cells
description In nature, bacteria often survive in a stationary state with low metabolic activity. Phages use the metabolic machinery of the host cell to replicate, and, therefore, their efficacy against non-dividing cells is usually limited. Nevertheless, it was previously shown that the Staphylococcus epidermidis phage SEP1 has the remarkable capacity to actively replicate in stationary-phase cells, reducing their numbers. Here, we studied for the first time the transcriptomic profiles of both exponential and stationary cells infected with SEP1 phage using RNA-seq to gain a better understanding of this rare phenomenon. We showed that SEP1 successfully takes over the transcriptional apparatus of both exponential and stationary cells. Infection was, however, delayed in stationary cells, with genes within the gp142-gp154 module putatively implicated in host takeover. S. epidermidis responded to SEP1 infection by upregulating three genes involved in a DNA modification system, with this being observed already 5 min after infection in exponential cells and later in stationary cells. In stationary cells, a significant number of genes involved in translation and RNA metabolic and biosynthetic processes were upregulated after 15 and 30 min of SEP1 infection in comparison with the uninfected control, showing that SEP1 activates metabolic and biosynthetic pathways necessary to its successful replication.
publishDate 2024
dc.date.none.fl_str_mv 2024-06-21
2024-06-21T00:00:00Z
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 https://hdl.handle.net/1822/93033
url https://hdl.handle.net/1822/93033
dc.language.iso.fl_str_mv eng
language eng
dc.relation.none.fl_str_mv Silva, M. D., Pinto, G., França, A., Azeredo, J., & Melo, L. D. R. (2024, July 23). Phage SEP1 hijacks Staphylococcus epidermidis stationary cells’ metabolism to replicate. (D. W. Cleary, Ed.), mSystems. American Society for Microbiology. http://doi.org/10.1128/msystems.00263-24
2379-5077
10.1128/msystems.00263-24
38904376
https://journals.asm.org/doi/10.1128/msystems.00263-24
dc.rights.driver.fl_str_mv info:eu-repo/semantics/openAccess
eu_rights_str_mv openAccess
dc.format.none.fl_str_mv application/pdf
dc.publisher.none.fl_str_mv American Society for Microbiology
publisher.none.fl_str_mv American Society for Microbiology
dc.source.none.fl_str_mv reponame:Repositórios Científicos de Acesso Aberto de Portugal (RCAAP)
instname:FCCN, serviços digitais da FCT – Fundação para a Ciência e a Tecnologia
instacron:RCAAP
instname_str FCCN, serviços digitais da FCT – Fundação para a Ciência e a Tecnologia
instacron_str RCAAP
institution RCAAP
reponame_str Repositórios Científicos de Acesso Aberto de Portugal (RCAAP)
collection Repositórios Científicos de Acesso Aberto de Portugal (RCAAP)
repository.name.fl_str_mv Repositórios Científicos de Acesso Aberto de Portugal (RCAAP) - FCCN, serviços digitais da FCT – Fundação para a Ciência e a Tecnologia
repository.mail.fl_str_mv info@rcaap.pt
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