Diversity of Human-Associated Bifidobacterial Prophage Sequences

Members of <i>Bifidobacterium</i> play an important role in the development of the immature gut and are associated with positive long-term health outcomes for their human host. It has previously been shown that intestinal bacteriophages are detected within hours of birth, and that induce...

Full description

Bibliographic Details
Main Authors: Darren Buckley, Toshitaka Odamaki, Jinzhong Xiao, Jennifer Mahony, Douwe van Sinderen, Francesca Bottacini
Format: Article
Language:English
Published: MDPI AG 2021-12-01
Series:Microorganisms
Subjects:
Online Access:https://www.mdpi.com/2076-2607/9/12/2559
_version_ 1797502322899681280
author Darren Buckley
Toshitaka Odamaki
Jinzhong Xiao
Jennifer Mahony
Douwe van Sinderen
Francesca Bottacini
author_facet Darren Buckley
Toshitaka Odamaki
Jinzhong Xiao
Jennifer Mahony
Douwe van Sinderen
Francesca Bottacini
author_sort Darren Buckley
collection DOAJ
description Members of <i>Bifidobacterium</i> play an important role in the development of the immature gut and are associated with positive long-term health outcomes for their human host. It has previously been shown that intestinal bacteriophages are detected within hours of birth, and that induced prophages constitute a significant source of such gut phages. The gut phageome can be vertically transmitted from mother to newborn and is believed to exert considerable selective pressure on target prokaryotic hosts affecting abundance levels, microbiota composition, and host characteristics. The objective of the current study was to investigate prophage-like elements and predicted CRISPR-Cas viral immune systems present in publicly available, human-associated <i>Bifidobacterium</i> genomes. Analysis of 585 fully sequenced bifidobacterial genomes identified 480 prophage-like elements with an occurrence of 0.82 prophages per genome. Interestingly, we also detected the presence of very similar bifidobacterial prophages and corresponding CRISPR spacers across different strains and species, thus providing an initial exploration of the human-associated bifidobacterial phageome. Our analyses show that closely related and likely functional prophages are commonly present across four different species of human-associated <i>Bifidobacterium</i>. Further comparative analysis of the CRISPR-Cas spacer arrays against the predicted prophages provided evidence of historical interactions between prophages and different strains at an intra- and inter-species level. Clear evidence of CRISPR-Cas acquired immunity against infection by bifidobacterial prophages across several bifidobacterial strains and species was obtained. Notably, a spacer representing a putative major capsid head protein was found on different genomes representing multiple strains across <i>B. adolescentis</i>, <i>B. breve</i>, and <i>B. bifidum</i>, suggesting that this gene is a preferred target to provide bifidobacterial phage immunity.
first_indexed 2024-03-10T03:31:27Z
format Article
id doaj.art-95d64ec33b77427b8b1b77c2fc7b3a97
institution Directory Open Access Journal
issn 2076-2607
language English
last_indexed 2024-03-10T03:31:27Z
publishDate 2021-12-01
publisher MDPI AG
record_format Article
series Microorganisms
spelling doaj.art-95d64ec33b77427b8b1b77c2fc7b3a972023-11-23T09:39:49ZengMDPI AGMicroorganisms2076-26072021-12-01912255910.3390/microorganisms9122559Diversity of Human-Associated Bifidobacterial Prophage SequencesDarren Buckley0Toshitaka Odamaki1Jinzhong Xiao2Jennifer Mahony3Douwe van Sinderen4Francesca Bottacini5INFANT Research Centre, University College Cork, Cork, IrelandNext Generation Science Institute, Morinaga Milk Industry Co., Ltd., Zama 252-8583, JapanNext Generation Science Institute, Morinaga Milk Industry Co., Ltd., Zama 252-8583, JapanAPC Microbiome Ireland, School of Microbiology, University College Cork, Cork, IrelandAPC Microbiome Ireland, School of Microbiology, University College Cork, Cork, IrelandAPC Microbiome Ireland, School of Microbiology, University College Cork, Cork, IrelandMembers of <i>Bifidobacterium</i> play an important role in the development of the immature gut and are associated with positive long-term health outcomes for their human host. It has previously been shown that intestinal bacteriophages are detected within hours of birth, and that induced prophages constitute a significant source of such gut phages. The gut phageome can be vertically transmitted from mother to newborn and is believed to exert considerable selective pressure on target prokaryotic hosts affecting abundance levels, microbiota composition, and host characteristics. The objective of the current study was to investigate prophage-like elements and predicted CRISPR-Cas viral immune systems present in publicly available, human-associated <i>Bifidobacterium</i> genomes. Analysis of 585 fully sequenced bifidobacterial genomes identified 480 prophage-like elements with an occurrence of 0.82 prophages per genome. Interestingly, we also detected the presence of very similar bifidobacterial prophages and corresponding CRISPR spacers across different strains and species, thus providing an initial exploration of the human-associated bifidobacterial phageome. Our analyses show that closely related and likely functional prophages are commonly present across four different species of human-associated <i>Bifidobacterium</i>. Further comparative analysis of the CRISPR-Cas spacer arrays against the predicted prophages provided evidence of historical interactions between prophages and different strains at an intra- and inter-species level. Clear evidence of CRISPR-Cas acquired immunity against infection by bifidobacterial prophages across several bifidobacterial strains and species was obtained. Notably, a spacer representing a putative major capsid head protein was found on different genomes representing multiple strains across <i>B. adolescentis</i>, <i>B. breve</i>, and <i>B. bifidum</i>, suggesting that this gene is a preferred target to provide bifidobacterial phage immunity.https://www.mdpi.com/2076-2607/9/12/2559gut microbiota<i>Bifidobacterium</i>bifidobacteriaphageomeprophageCRISPR-Cas
spellingShingle Darren Buckley
Toshitaka Odamaki
Jinzhong Xiao
Jennifer Mahony
Douwe van Sinderen
Francesca Bottacini
Diversity of Human-Associated Bifidobacterial Prophage Sequences
Microorganisms
gut microbiota
<i>Bifidobacterium</i>
bifidobacteria
phageome
prophage
CRISPR-Cas
title Diversity of Human-Associated Bifidobacterial Prophage Sequences
title_full Diversity of Human-Associated Bifidobacterial Prophage Sequences
title_fullStr Diversity of Human-Associated Bifidobacterial Prophage Sequences
title_full_unstemmed Diversity of Human-Associated Bifidobacterial Prophage Sequences
title_short Diversity of Human-Associated Bifidobacterial Prophage Sequences
title_sort diversity of human associated bifidobacterial prophage sequences
topic gut microbiota
<i>Bifidobacterium</i>
bifidobacteria
phageome
prophage
CRISPR-Cas
url https://www.mdpi.com/2076-2607/9/12/2559
work_keys_str_mv AT darrenbuckley diversityofhumanassociatedbifidobacterialprophagesequences
AT toshitakaodamaki diversityofhumanassociatedbifidobacterialprophagesequences
AT jinzhongxiao diversityofhumanassociatedbifidobacterialprophagesequences
AT jennifermahony diversityofhumanassociatedbifidobacterialprophagesequences
AT douwevansinderen diversityofhumanassociatedbifidobacterialprophagesequences
AT francescabottacini diversityofhumanassociatedbifidobacterialprophagesequences