An extended catalog of integrated prophages in the infant and adult fecal microbiome shows high prevalence of lysogeny
Background and aimsThe acquisition and gradual maturation of gut microbial communities during early childhood is central to an individual’s healthy development. Bacteriophages have the potential to shape the gut bacterial communities. However, the complex ecological interactions between phages and t...
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2023-09-01
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| Series: | Frontiers in Microbiology |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fmicb.2023.1254535/full |
| _version_ | 1797692471322345472 |
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| author | Evgenia Dikareva Dollwin Matharu Emilia Lahtinen Kaija-Leena Kolho Kaija-Leena Kolho Willem M. De Vos Willem M. De Vos Anne Salonen Alise J. Ponsero |
| author_facet | Evgenia Dikareva Dollwin Matharu Emilia Lahtinen Kaija-Leena Kolho Kaija-Leena Kolho Willem M. De Vos Willem M. De Vos Anne Salonen Alise J. Ponsero |
| author_sort | Evgenia Dikareva |
| collection | DOAJ |
| description | Background and aimsThe acquisition and gradual maturation of gut microbial communities during early childhood is central to an individual’s healthy development. Bacteriophages have the potential to shape the gut bacterial communities. However, the complex ecological interactions between phages and their bacterial host are still poorly characterized. In this study, we investigated the abundance and diversity of integrated prophages in infant and adult gut bacteria by detecting integrated prophages in metagenome assembled genomes (MAGs) of commensal bacteria.MethodsOur study included 88 infants sampled at 3 weeks, 3 months, 6 months, and 12 months (n = 323 total samples), and their parents around delivery time (n = 138 total samples). Fecal DNA was extracted and characterized by using shotgun metagenomic sequencing, and a collection of prokaryotic MAGs was generated. The MAG collection was screened for the presence of integrated bacteriophage sequences, allowing their taxonomic and functional characterization.ResultsA large collection of 6,186 MAGs from infant and adult gut microbiota was obtained and screened for integrated prophages, allowing the identification of 7,165 prophage sequences longer than 10 kb. Strikingly, more than 70% of the near-complete MAGs were identified as lysogens. The prevalence of prophages in MAGs varied across bacterial families, with a lower prevalence observed among Coriobacteriaceae, Eggerthellaceae, Veillonellaceae and Burkholderiaceae, while a very high prevalence of lysogen MAGs were observed in Oscillospiraceae, Enterococcaceae, and Enterobacteriaceae. Interestingly for several bacterial families such as Bifidobacteriaceae and Bacteroidaceae, the prevalence of prophages in MAGs was higher in early infant time point (3 weeks and 3 months) than in later sampling points (6 and 12 months) and in adults. The prophage sequences were clustered into 5,616 species-like vOTUs, 77% of which were novel. Finally, we explored the functional repertoire of the potential auxiliary metabolic genes carried by these prophages, encoding functions involved in carbohydrate metabolism and degradation, amino acid metabolism and carbon metabolism.ConclusionOur study provides an enhanced understanding of the diversity and prevalence of lysogens in infant and adult gut microbiota and suggests a complex interplay between prophages and their bacterial hosts. |
| first_indexed | 2024-03-12T02:28:00Z |
| format | Article |
| id | doaj.art-7e1418f59e8a4b78aef57fa6be74f866 |
| institution | Directory Open Access Journal |
| issn | 1664-302X |
| language | English |
| last_indexed | 2024-03-12T02:28:00Z |
| publishDate | 2023-09-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Microbiology |
| spelling | doaj.art-7e1418f59e8a4b78aef57fa6be74f8662023-09-05T11:11:27ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2023-09-011410.3389/fmicb.2023.12545351254535An extended catalog of integrated prophages in the infant and adult fecal microbiome shows high prevalence of lysogenyEvgenia Dikareva0Dollwin Matharu1Emilia Lahtinen2Kaija-Leena Kolho3Kaija-Leena Kolho4Willem M. De Vos5Willem M. De Vos6Anne Salonen7Alise J. Ponsero8Human Microbiome Research Program, Faculty of Medicine, University of Helsinki, Helsinki, FinlandHuman Microbiome Research Program, Faculty of Medicine, University of Helsinki, Helsinki, FinlandHuman Microbiome Research Program, Faculty of Medicine, University of Helsinki, Helsinki, FinlandChildren's Hospital, Paediatric Research Centre, University of Helsinki and HUS, Helsinki, FinlandFaculty of Medicine and Health Technology, Tampere University, Tampere, FinlandHuman Microbiome Research Program, Faculty of Medicine, University of Helsinki, Helsinki, FinlandLaboratory of Microbiology, Wageningen University and Research, Wageningen, NetherlandsHuman Microbiome Research Program, Faculty of Medicine, University of Helsinki, Helsinki, FinlandHuman Microbiome Research Program, Faculty of Medicine, University of Helsinki, Helsinki, FinlandBackground and aimsThe acquisition and gradual maturation of gut microbial communities during early childhood is central to an individual’s healthy development. Bacteriophages have the potential to shape the gut bacterial communities. However, the complex ecological interactions between phages and their bacterial host are still poorly characterized. In this study, we investigated the abundance and diversity of integrated prophages in infant and adult gut bacteria by detecting integrated prophages in metagenome assembled genomes (MAGs) of commensal bacteria.MethodsOur study included 88 infants sampled at 3 weeks, 3 months, 6 months, and 12 months (n = 323 total samples), and their parents around delivery time (n = 138 total samples). Fecal DNA was extracted and characterized by using shotgun metagenomic sequencing, and a collection of prokaryotic MAGs was generated. The MAG collection was screened for the presence of integrated bacteriophage sequences, allowing their taxonomic and functional characterization.ResultsA large collection of 6,186 MAGs from infant and adult gut microbiota was obtained and screened for integrated prophages, allowing the identification of 7,165 prophage sequences longer than 10 kb. Strikingly, more than 70% of the near-complete MAGs were identified as lysogens. The prevalence of prophages in MAGs varied across bacterial families, with a lower prevalence observed among Coriobacteriaceae, Eggerthellaceae, Veillonellaceae and Burkholderiaceae, while a very high prevalence of lysogen MAGs were observed in Oscillospiraceae, Enterococcaceae, and Enterobacteriaceae. Interestingly for several bacterial families such as Bifidobacteriaceae and Bacteroidaceae, the prevalence of prophages in MAGs was higher in early infant time point (3 weeks and 3 months) than in later sampling points (6 and 12 months) and in adults. The prophage sequences were clustered into 5,616 species-like vOTUs, 77% of which were novel. Finally, we explored the functional repertoire of the potential auxiliary metabolic genes carried by these prophages, encoding functions involved in carbohydrate metabolism and degradation, amino acid metabolism and carbon metabolism.ConclusionOur study provides an enhanced understanding of the diversity and prevalence of lysogens in infant and adult gut microbiota and suggests a complex interplay between prophages and their bacterial hosts.https://www.frontiersin.org/articles/10.3389/fmicb.2023.1254535/fullinfant gut microbiotabacteriophagesprophagelysogenymetagenome assembled genomes (MAGs)auxilliary metabolic genes |
| spellingShingle | Evgenia Dikareva Dollwin Matharu Emilia Lahtinen Kaija-Leena Kolho Kaija-Leena Kolho Willem M. De Vos Willem M. De Vos Anne Salonen Alise J. Ponsero An extended catalog of integrated prophages in the infant and adult fecal microbiome shows high prevalence of lysogeny Frontiers in Microbiology infant gut microbiota bacteriophages prophage lysogeny metagenome assembled genomes (MAGs) auxilliary metabolic genes |
| title | An extended catalog of integrated prophages in the infant and adult fecal microbiome shows high prevalence of lysogeny |
| title_full | An extended catalog of integrated prophages in the infant and adult fecal microbiome shows high prevalence of lysogeny |
| title_fullStr | An extended catalog of integrated prophages in the infant and adult fecal microbiome shows high prevalence of lysogeny |
| title_full_unstemmed | An extended catalog of integrated prophages in the infant and adult fecal microbiome shows high prevalence of lysogeny |
| title_short | An extended catalog of integrated prophages in the infant and adult fecal microbiome shows high prevalence of lysogeny |
| title_sort | extended catalog of integrated prophages in the infant and adult fecal microbiome shows high prevalence of lysogeny |
| topic | infant gut microbiota bacteriophages prophage lysogeny metagenome assembled genomes (MAGs) auxilliary metabolic genes |
| url | https://www.frontiersin.org/articles/10.3389/fmicb.2023.1254535/full |
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