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Spontaneously induced prophages are abundant in a naturally evolved bacterial starter culture and deliver competitive advantage to the host
BACKGROUND: In complex microbial ecosystems such as the marine environment, the gastrointestinal tract, but also in mixed culture fermentations, bacteriophages are frequently found to be a part of the microbial community. Moreover, prophages or prophage-like elements are frequently identified in seq...
Autores principales: | , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
BioMed Central
2018
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6154921/ https://www.ncbi.nlm.nih.gov/pubmed/30249194 http://dx.doi.org/10.1186/s12866-018-1229-1 |
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author | Alexeeva, Svetlana Guerra Martínez, Jesús Adrián Spus, Maciej Smid, Eddy J. |
author_facet | Alexeeva, Svetlana Guerra Martínez, Jesús Adrián Spus, Maciej Smid, Eddy J. |
author_sort | Alexeeva, Svetlana |
collection | PubMed |
description | BACKGROUND: In complex microbial ecosystems such as the marine environment, the gastrointestinal tract, but also in mixed culture fermentations, bacteriophages are frequently found to be a part of the microbial community. Moreover, prophages or prophage-like elements are frequently identified in sequenced bacterial genomes. The mixed undefined starter cultures represent an ecosystem which is shaped by long term evolution under relatively defined environmental conditions and provides an interesting model to study co-evolution of phages and their hosts as well as the impact of diversity on microbial community stability. RESULTS: In the present study we investigated the presence, identity and behaviour of prophages in lactococci being part of a complex cheese starter culture. Genome analysis of representative strains of the 7 genetic lineages of Lactococcus lactis constituting the culture indicated the presence of prophages in all strains. Exposure of potential lysogens to mitomycin C confirmed the release of ~ 10(10)·ml(− 1) phage particles from all tested strains. Furthermore, phages were also released in substantial amounts due to spontaneous induction: more than 10(8)·ml(− 1) phage particles were present in cultures under non-inducing conditions. This observation suggests continuous release of phage particles by the lactococci. The released bacteriophages exhibited an unusual morphology. For most strains tested, tailless icosahedral phage heads were found. The competitive advantage of lysogens compared to their cured derivatives and their high abundance in the culture suggests that the released tailless bacteriophages play an important role in the ecosystem. CONCLUSIONS: The results of this study indicate that chromosomal genetic elements are active participants in the stable complex microbial community of the starter culture. We show that prophages are abundant in such a community, are produced continuously in large amounts and, despite the huge metabolic burden imposed on the cells by phage particle production, provide a selective advantage to the host. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12866-018-1229-1) contains supplementary material, which is available to authorized users. |
format | Online Article Text |
id | pubmed-6154921 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2018 |
publisher | BioMed Central |
record_format | MEDLINE/PubMed |
spelling | pubmed-61549212018-09-26 Spontaneously induced prophages are abundant in a naturally evolved bacterial starter culture and deliver competitive advantage to the host Alexeeva, Svetlana Guerra Martínez, Jesús Adrián Spus, Maciej Smid, Eddy J. BMC Microbiol Research Article BACKGROUND: In complex microbial ecosystems such as the marine environment, the gastrointestinal tract, but also in mixed culture fermentations, bacteriophages are frequently found to be a part of the microbial community. Moreover, prophages or prophage-like elements are frequently identified in sequenced bacterial genomes. The mixed undefined starter cultures represent an ecosystem which is shaped by long term evolution under relatively defined environmental conditions and provides an interesting model to study co-evolution of phages and their hosts as well as the impact of diversity on microbial community stability. RESULTS: In the present study we investigated the presence, identity and behaviour of prophages in lactococci being part of a complex cheese starter culture. Genome analysis of representative strains of the 7 genetic lineages of Lactococcus lactis constituting the culture indicated the presence of prophages in all strains. Exposure of potential lysogens to mitomycin C confirmed the release of ~ 10(10)·ml(− 1) phage particles from all tested strains. Furthermore, phages were also released in substantial amounts due to spontaneous induction: more than 10(8)·ml(− 1) phage particles were present in cultures under non-inducing conditions. This observation suggests continuous release of phage particles by the lactococci. The released bacteriophages exhibited an unusual morphology. For most strains tested, tailless icosahedral phage heads were found. The competitive advantage of lysogens compared to their cured derivatives and their high abundance in the culture suggests that the released tailless bacteriophages play an important role in the ecosystem. CONCLUSIONS: The results of this study indicate that chromosomal genetic elements are active participants in the stable complex microbial community of the starter culture. We show that prophages are abundant in such a community, are produced continuously in large amounts and, despite the huge metabolic burden imposed on the cells by phage particle production, provide a selective advantage to the host. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12866-018-1229-1) contains supplementary material, which is available to authorized users. BioMed Central 2018-09-24 /pmc/articles/PMC6154921/ /pubmed/30249194 http://dx.doi.org/10.1186/s12866-018-1229-1 Text en © The Author(s). 2018 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. |
spellingShingle | Research Article Alexeeva, Svetlana Guerra Martínez, Jesús Adrián Spus, Maciej Smid, Eddy J. Spontaneously induced prophages are abundant in a naturally evolved bacterial starter culture and deliver competitive advantage to the host |
title | Spontaneously induced prophages are abundant in a naturally evolved bacterial starter culture and deliver competitive advantage to the host |
title_full | Spontaneously induced prophages are abundant in a naturally evolved bacterial starter culture and deliver competitive advantage to the host |
title_fullStr | Spontaneously induced prophages are abundant in a naturally evolved bacterial starter culture and deliver competitive advantage to the host |
title_full_unstemmed | Spontaneously induced prophages are abundant in a naturally evolved bacterial starter culture and deliver competitive advantage to the host |
title_short | Spontaneously induced prophages are abundant in a naturally evolved bacterial starter culture and deliver competitive advantage to the host |
title_sort | spontaneously induced prophages are abundant in a naturally evolved bacterial starter culture and deliver competitive advantage to the host |
topic | Research Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6154921/ https://www.ncbi.nlm.nih.gov/pubmed/30249194 http://dx.doi.org/10.1186/s12866-018-1229-1 |
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