An in vitro fermentation model to study the impact of bacteriophages targeting shiga toxin-encoding escherichia coli on the colonic microbiota
Autor(a) principal: | |
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Data de Publicação: | 2022 |
Outros Autores: | , , , , , , |
Tipo de documento: | Artigo |
Idioma: | eng |
Título da fonte: | Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos) |
Texto Completo: | https://hdl.handle.net/1822/79875 |
Resumo: | Lytic bacteriophages are considered safe for human consumption as biocontrol agents against foodborne pathogens, in particular in ready-to-eat foodstuffs. Phages could, however, evolve to infect different hosts when passing through the gastrointestinal tract (GIT). This underlines the importance of understanding the impact of phages towards colonic microbiota, particularly towards bacterial families usually found in the colon such as the Enterobacteriaceae. Here we propose in vitro batch fermentation as model for initial safety screening of lytic phages targeting Shiga toxin-producing Escherichia coli (STEC). As inoculum we used faecal material of three healthy donors. To assess phage safety, we monitored fermentation parameters, including short chain fatty acid production and gas production/intake by colonic microbiota. We performed shotgun metagenomic analysis to evaluate the outcome of phage interference with colonic microbiota composition and functional potential. During the 24h incubation, concentrations of phage and its host were also evaluated. We found the phage used in this study, named E. coli phage vB_EcoS_Ace (Ace), to be safe towards human colonic microbiota, independently of the donors faecal content used. This suggests that individuality of donor faecal microbiota did not interfere with phage effect on the fermentations. However, the model revealed that the attenuated STEC strain used as phage host perturbed the faecal microbiota as based on metagenomic analysis, with potential differences in metabolic output. We conclude that the in vitro batch fermentation model used in this study is a reliable safety screening for lytic phages intended to be used as biocontrol agents. |
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An in vitro fermentation model to study the impact of bacteriophages targeting shiga toxin-encoding escherichia coli on the colonic microbiotaAntimicrobialsApplied microbiologyMetagenomicsMicrobiotaNext-generation sequencingScience & TechnologyLytic bacteriophages are considered safe for human consumption as biocontrol agents against foodborne pathogens, in particular in ready-to-eat foodstuffs. Phages could, however, evolve to infect different hosts when passing through the gastrointestinal tract (GIT). This underlines the importance of understanding the impact of phages towards colonic microbiota, particularly towards bacterial families usually found in the colon such as the Enterobacteriaceae. Here we propose in vitro batch fermentation as model for initial safety screening of lytic phages targeting Shiga toxin-producing Escherichia coli (STEC). As inoculum we used faecal material of three healthy donors. To assess phage safety, we monitored fermentation parameters, including short chain fatty acid production and gas production/intake by colonic microbiota. We performed shotgun metagenomic analysis to evaluate the outcome of phage interference with colonic microbiota composition and functional potential. During the 24h incubation, concentrations of phage and its host were also evaluated. We found the phage used in this study, named E. coli phage vB_EcoS_Ace (Ace), to be safe towards human colonic microbiota, independently of the donors faecal content used. This suggests that individuality of donor faecal microbiota did not interfere with phage effect on the fermentations. However, the model revealed that the attenuated STEC strain used as phage host perturbed the faecal microbiota as based on metagenomic analysis, with potential differences in metabolic output. We conclude that the in vitro batch fermentation model used in this study is a reliable safety screening for lytic phages intended to be used as biocontrol agents.The authors thank Dr. Siavash Atashgahi and Prof. Dr. Willem M. de Vos for providing the faecal samples from an independent study. This study was financially supported by (i) by the Portuguese Foundation for Science and Technology (FCT) under the scope of the strategic funding of UIDB/04469/2020 unit; (ii) project PhageSTEC (POCI-01-0145-FEDER-029628) funded by FEDER through COMPETE2020 (Programa Operacional Competitividade e InternacionalizacAo) and by National Funds thought FCT (FundacAo para a Ciencia e a Tecnologia); (iii) Project PTDC/SAU-PUB/29182/2017 [POCI-01-0145-FEDER-029182]. This project received funding from the European Union's Horizon 2020 research and innovation program under grant agreement No. 713640; iv) by the Netherlands Organisation for Scientific Research funded UNLOCK project NRGWI.obrug.2018.005. The author G.P. acknowledges FCT for PhD grant SFRH/BD/117365/2016. The author R.F.S.G. acknowledges FCT for PhD grant SFRH/BD/140182/2018.info:eu-repo/semantics/publishedVersionNature Publishing GroupUniversidade do MinhoPinto, GraçaShetty, Sudarshan A.Zoetendal, Erwin G.Gonçalves, Raquel F. S.Pinheiro, Ana CristinaAlmeida, Carina Manuela FernandesAzeredo, JoanaSmidt, Hauke2022-09-262022-09-26T00:00:00Zinfo:eu-repo/semantics/publishedVersioninfo:eu-repo/semantics/articleapplication/pdfhttps://hdl.handle.net/1822/79875engPinto, Graça; Shetty, Sudarshan; Zoetendal, Erwin G.; Gonçalves, Raquel F. S.; Pinheiro, Ana Cristina; Almeida, Carina; Azeredo, Joana; Smidt, Hauke, An in vitro fermentation model to study the impact of bacteriophages targeting Shiga toxin-encoding Escherichia coli on the colonic microbiota. npj Biofilms and Microbiomes, 8(74), 20222055-500810.1038/s41522-022-00334-836163472http://www.nature.com/npjbiofilms/info: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:RCAAP2023-07-21T12:51:03Zoai:repositorium.sdum.uminho.pt:1822/79875Portal AgregadorONGhttps://www.rcaap.pt/oai/openaireopendoar:71602024-03-19T19:49:49.946190Repositório 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 |
An in vitro fermentation model to study the impact of bacteriophages targeting shiga toxin-encoding escherichia coli on the colonic microbiota |
title |
An in vitro fermentation model to study the impact of bacteriophages targeting shiga toxin-encoding escherichia coli on the colonic microbiota |
spellingShingle |
An in vitro fermentation model to study the impact of bacteriophages targeting shiga toxin-encoding escherichia coli on the colonic microbiota Pinto, Graça Antimicrobials Applied microbiology Metagenomics Microbiota Next-generation sequencing Science & Technology |
title_short |
An in vitro fermentation model to study the impact of bacteriophages targeting shiga toxin-encoding escherichia coli on the colonic microbiota |
title_full |
An in vitro fermentation model to study the impact of bacteriophages targeting shiga toxin-encoding escherichia coli on the colonic microbiota |
title_fullStr |
An in vitro fermentation model to study the impact of bacteriophages targeting shiga toxin-encoding escherichia coli on the colonic microbiota |
title_full_unstemmed |
An in vitro fermentation model to study the impact of bacteriophages targeting shiga toxin-encoding escherichia coli on the colonic microbiota |
title_sort |
An in vitro fermentation model to study the impact of bacteriophages targeting shiga toxin-encoding escherichia coli on the colonic microbiota |
author |
Pinto, Graça |
author_facet |
Pinto, Graça Shetty, Sudarshan A. Zoetendal, Erwin G. Gonçalves, Raquel F. S. Pinheiro, Ana Cristina Almeida, Carina Manuela Fernandes Azeredo, Joana Smidt, Hauke |
author_role |
author |
author2 |
Shetty, Sudarshan A. Zoetendal, Erwin G. Gonçalves, Raquel F. S. Pinheiro, Ana Cristina Almeida, Carina Manuela Fernandes Azeredo, Joana Smidt, Hauke |
author2_role |
author author author author author author author |
dc.contributor.none.fl_str_mv |
Universidade do Minho |
dc.contributor.author.fl_str_mv |
Pinto, Graça Shetty, Sudarshan A. Zoetendal, Erwin G. Gonçalves, Raquel F. S. Pinheiro, Ana Cristina Almeida, Carina Manuela Fernandes Azeredo, Joana Smidt, Hauke |
dc.subject.por.fl_str_mv |
Antimicrobials Applied microbiology Metagenomics Microbiota Next-generation sequencing Science & Technology |
topic |
Antimicrobials Applied microbiology Metagenomics Microbiota Next-generation sequencing Science & Technology |
description |
Lytic bacteriophages are considered safe for human consumption as biocontrol agents against foodborne pathogens, in particular in ready-to-eat foodstuffs. Phages could, however, evolve to infect different hosts when passing through the gastrointestinal tract (GIT). This underlines the importance of understanding the impact of phages towards colonic microbiota, particularly towards bacterial families usually found in the colon such as the Enterobacteriaceae. Here we propose in vitro batch fermentation as model for initial safety screening of lytic phages targeting Shiga toxin-producing Escherichia coli (STEC). As inoculum we used faecal material of three healthy donors. To assess phage safety, we monitored fermentation parameters, including short chain fatty acid production and gas production/intake by colonic microbiota. We performed shotgun metagenomic analysis to evaluate the outcome of phage interference with colonic microbiota composition and functional potential. During the 24h incubation, concentrations of phage and its host were also evaluated. We found the phage used in this study, named E. coli phage vB_EcoS_Ace (Ace), to be safe towards human colonic microbiota, independently of the donors faecal content used. This suggests that individuality of donor faecal microbiota did not interfere with phage effect on the fermentations. However, the model revealed that the attenuated STEC strain used as phage host perturbed the faecal microbiota as based on metagenomic analysis, with potential differences in metabolic output. We conclude that the in vitro batch fermentation model used in this study is a reliable safety screening for lytic phages intended to be used as biocontrol agents. |
publishDate |
2022 |
dc.date.none.fl_str_mv |
2022-09-26 2022-09-26T00:00:00Z |
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/1822/79875 |
url |
https://hdl.handle.net/1822/79875 |
dc.language.iso.fl_str_mv |
eng |
language |
eng |
dc.relation.none.fl_str_mv |
Pinto, Graça; Shetty, Sudarshan; Zoetendal, Erwin G.; Gonçalves, Raquel F. S.; Pinheiro, Ana Cristina; Almeida, Carina; Azeredo, Joana; Smidt, Hauke, An in vitro fermentation model to study the impact of bacteriophages targeting Shiga toxin-encoding Escherichia coli on the colonic microbiota. npj Biofilms and Microbiomes, 8(74), 2022 2055-5008 10.1038/s41522-022-00334-8 36163472 http://www.nature.com/npjbiofilms/ |
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 |
Nature Publishing Group |
publisher.none.fl_str_mv |
Nature Publishing Group |
dc.source.none.fl_str_mv |
reponame:Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos) instname:Agência para a Sociedade do Conhecimento (UMIC) - FCT - Sociedade da Informação instacron:RCAAP |
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Agência para a Sociedade do Conhecimento (UMIC) - FCT - Sociedade da Informação |
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RCAAP |
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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) |
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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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