Spontaneously induced prophages are abundant in a naturally evolved bacterial starter culture and deliver competitive advantage to the host
Abstract 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 identifie...
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| Format: | Article |
| Language: | English |
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BMC
2018-09-01
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| Series: | BMC Microbiology |
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| Online Access: | http://link.springer.com/article/10.1186/s12866-018-1229-1 |
| _version_ | 1818264640353730560 |
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| author | Svetlana Alexeeva Jesús Adrián Guerra Martínez Maciej Spus Eddy J. Smid |
| author_facet | Svetlana Alexeeva Jesús Adrián Guerra Martínez Maciej Spus Eddy J. Smid |
| author_sort | Svetlana Alexeeva |
| collection | DOAJ |
| description | Abstract 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 ~ 1010·ml− 1 phage particles from all tested strains. Furthermore, phages were also released in substantial amounts due to spontaneous induction: more than 108·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. |
| first_indexed | 2024-12-12T19:38:07Z |
| format | Article |
| id | doaj.art-e6a16b34eb19498fb8c339f4c9b5bbf2 |
| institution | Directory Open Access Journal |
| issn | 1471-2180 |
| language | English |
| last_indexed | 2024-12-12T19:38:07Z |
| publishDate | 2018-09-01 |
| publisher | BMC |
| record_format | Article |
| series | BMC Microbiology |
| spelling | doaj.art-e6a16b34eb19498fb8c339f4c9b5bbf22022-12-22T00:14:15ZengBMCBMC Microbiology1471-21802018-09-0118111610.1186/s12866-018-1229-1Spontaneously induced prophages are abundant in a naturally evolved bacterial starter culture and deliver competitive advantage to the hostSvetlana Alexeeva0Jesús Adrián Guerra Martínez1Maciej Spus2Eddy J. Smid3Laboratory of Food Microbiology, Wageningen UniversityLaboratory of Food Microbiology, Wageningen UniversityLaboratory of Food Microbiology, Wageningen UniversityLaboratory of Food Microbiology, Wageningen UniversityAbstract 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 ~ 1010·ml− 1 phage particles from all tested strains. Furthermore, phages were also released in substantial amounts due to spontaneous induction: more than 108·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.http://link.springer.com/article/10.1186/s12866-018-1229-1Lactococcus lactisProphageBacteriophageLysogenyMixed cultureEvolution |
| spellingShingle | Svetlana Alexeeva Jesús Adrián Guerra Martínez Maciej Spus Eddy J. Smid Spontaneously induced prophages are abundant in a naturally evolved bacterial starter culture and deliver competitive advantage to the host BMC Microbiology Lactococcus lactis Prophage Bacteriophage Lysogeny Mixed culture Evolution |
| 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 | Lactococcus lactis Prophage Bacteriophage Lysogeny Mixed culture Evolution |
| url | http://link.springer.com/article/10.1186/s12866-018-1229-1 |
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