Isolation and Characterization of a Novel Temperate Escherichia coli Bacteriophage, Kapi1, Which Modifies the O-Antigen and Contributes to the Competitiveness of Its Host during Colonization of the Murine Gastrointestinal Tract
ABSTRACT In this study, we describe the isolation and characterization of novel bacteriophage vB_EcoP_Kapi1 (Kapi1) isolated from a strain of commensal Escherichia coli inhabiting the gastrointestinal tract of healthy mice. We show that Kapi1 is a temperate phage integrated into tRNA argW of strain...
| Main Authors: | , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
American Society for Microbiology
2022-02-01
|
| Series: | mBio |
| Subjects: | |
| Online Access: | https://journals.asm.org/doi/10.1128/mbio.02085-21 |
| _version_ | 1819280562564628480 |
|---|---|
| author | Kat Pick Tingting Ju Benjamin P. Willing Tracy L. Raivio |
| author_facet | Kat Pick Tingting Ju Benjamin P. Willing Tracy L. Raivio |
| author_sort | Kat Pick |
| collection | DOAJ |
| description | ABSTRACT In this study, we describe the isolation and characterization of novel bacteriophage vB_EcoP_Kapi1 (Kapi1) isolated from a strain of commensal Escherichia coli inhabiting the gastrointestinal tract of healthy mice. We show that Kapi1 is a temperate phage integrated into tRNA argW of strain MP1 and describe its genome annotation and structure. Kapi1 shows limited homology to other characterized prophages but is most similar to the seroconverting phages of Shigella flexneri and clusters taxonomically with P22-like phages. The receptor for Kapi1 is the lipopolysaccharide O-antigen, and we further show that Kapi1 alters the structure of its host’s O-antigen in multiple ways. Kapi1 displays unstable lysogeny, and we find that the lysogenic state is more stable during growth in simulated intestinal fluid. Furthermore, Kapi1 lysogens have a competitive advantage over their nonlysogenic counterparts both in vitro and in vivo, suggesting a role for Kapi1 during colonization. We thus report the use of MP1 and Kapi1 as a model system to explore the molecular mechanisms of mammalian colonization by E. coli to ask what the role(s) of prophages in this context might be. IMPORTANCE Although research exploring the microbiome has exploded in recent years, our understanding of the viral component of the microbiome is lagging far behind our understanding of the bacterial component. The vast majority of intestinal bacteria carry prophages integrated into their chromosomes, but most of these bacteriophages remain uncharacterized and unexplored. Here, we isolate and characterize a novel temperate bacteriophage infecting a commensal strain of Escherichia coli. We aim to explore the interactions between bacteriophages and their hosts in the context of the gastrointestinal tract, asking what role(s) temperate bacteriophages may play in growth and survival of bacteria in the gut. Understanding the fundamental biology of gut commensal bacteria can inform the development of novel antimicrobial or probiotic strategies for intestinal infections. |
| first_indexed | 2024-12-24T00:45:46Z |
| format | Article |
| id | doaj.art-ab415b0388474a7db333625b524a00fa |
| institution | Directory Open Access Journal |
| issn | 2150-7511 |
| language | English |
| last_indexed | 2024-12-24T00:45:46Z |
| publishDate | 2022-02-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | mBio |
| spelling | doaj.art-ab415b0388474a7db333625b524a00fa2022-12-21T17:23:49ZengAmerican Society for MicrobiologymBio2150-75112022-02-0113110.1128/mbio.02085-21Isolation and Characterization of a Novel Temperate Escherichia coli Bacteriophage, Kapi1, Which Modifies the O-Antigen and Contributes to the Competitiveness of Its Host during Colonization of the Murine Gastrointestinal TractKat Pick0Tingting Ju1Benjamin P. Willing2Tracy L. Raivio3Department of Biological Sciences, University of Alberta, Edmonton, Alberta, CanadaDepartment of Agricultural, Food and Nutritional Science, University of Alberta, Edmonton, Alberta, CanadaDepartment of Agricultural, Food and Nutritional Science, University of Alberta, Edmonton, Alberta, CanadaDepartment of Biological Sciences, University of Alberta, Edmonton, Alberta, CanadaABSTRACT In this study, we describe the isolation and characterization of novel bacteriophage vB_EcoP_Kapi1 (Kapi1) isolated from a strain of commensal Escherichia coli inhabiting the gastrointestinal tract of healthy mice. We show that Kapi1 is a temperate phage integrated into tRNA argW of strain MP1 and describe its genome annotation and structure. Kapi1 shows limited homology to other characterized prophages but is most similar to the seroconverting phages of Shigella flexneri and clusters taxonomically with P22-like phages. The receptor for Kapi1 is the lipopolysaccharide O-antigen, and we further show that Kapi1 alters the structure of its host’s O-antigen in multiple ways. Kapi1 displays unstable lysogeny, and we find that the lysogenic state is more stable during growth in simulated intestinal fluid. Furthermore, Kapi1 lysogens have a competitive advantage over their nonlysogenic counterparts both in vitro and in vivo, suggesting a role for Kapi1 during colonization. We thus report the use of MP1 and Kapi1 as a model system to explore the molecular mechanisms of mammalian colonization by E. coli to ask what the role(s) of prophages in this context might be. IMPORTANCE Although research exploring the microbiome has exploded in recent years, our understanding of the viral component of the microbiome is lagging far behind our understanding of the bacterial component. The vast majority of intestinal bacteria carry prophages integrated into their chromosomes, but most of these bacteriophages remain uncharacterized and unexplored. Here, we isolate and characterize a novel temperate bacteriophage infecting a commensal strain of Escherichia coli. We aim to explore the interactions between bacteriophages and their hosts in the context of the gastrointestinal tract, asking what role(s) temperate bacteriophages may play in growth and survival of bacteria in the gut. Understanding the fundamental biology of gut commensal bacteria can inform the development of novel antimicrobial or probiotic strategies for intestinal infections.https://journals.asm.org/doi/10.1128/mbio.02085-21gastrointestinal colonizationlysogentemperate |
| spellingShingle | Kat Pick Tingting Ju Benjamin P. Willing Tracy L. Raivio Isolation and Characterization of a Novel Temperate Escherichia coli Bacteriophage, Kapi1, Which Modifies the O-Antigen and Contributes to the Competitiveness of Its Host during Colonization of the Murine Gastrointestinal Tract mBio gastrointestinal colonization lysogen temperate |
| title | Isolation and Characterization of a Novel Temperate Escherichia coli Bacteriophage, Kapi1, Which Modifies the O-Antigen and Contributes to the Competitiveness of Its Host during Colonization of the Murine Gastrointestinal Tract |
| title_full | Isolation and Characterization of a Novel Temperate Escherichia coli Bacteriophage, Kapi1, Which Modifies the O-Antigen and Contributes to the Competitiveness of Its Host during Colonization of the Murine Gastrointestinal Tract |
| title_fullStr | Isolation and Characterization of a Novel Temperate Escherichia coli Bacteriophage, Kapi1, Which Modifies the O-Antigen and Contributes to the Competitiveness of Its Host during Colonization of the Murine Gastrointestinal Tract |
| title_full_unstemmed | Isolation and Characterization of a Novel Temperate Escherichia coli Bacteriophage, Kapi1, Which Modifies the O-Antigen and Contributes to the Competitiveness of Its Host during Colonization of the Murine Gastrointestinal Tract |
| title_short | Isolation and Characterization of a Novel Temperate Escherichia coli Bacteriophage, Kapi1, Which Modifies the O-Antigen and Contributes to the Competitiveness of Its Host during Colonization of the Murine Gastrointestinal Tract |
| title_sort | isolation and characterization of a novel temperate escherichia coli bacteriophage kapi1 which modifies the o antigen and contributes to the competitiveness of its host during colonization of the murine gastrointestinal tract |
| topic | gastrointestinal colonization lysogen temperate |
| url | https://journals.asm.org/doi/10.1128/mbio.02085-21 |
| work_keys_str_mv | AT katpick isolationandcharacterizationofanoveltemperateescherichiacolibacteriophagekapi1whichmodifiestheoantigenandcontributestothecompetitivenessofitshostduringcolonizationofthemurinegastrointestinaltract AT tingtingju isolationandcharacterizationofanoveltemperateescherichiacolibacteriophagekapi1whichmodifiestheoantigenandcontributestothecompetitivenessofitshostduringcolonizationofthemurinegastrointestinaltract AT benjaminpwilling isolationandcharacterizationofanoveltemperateescherichiacolibacteriophagekapi1whichmodifiestheoantigenandcontributestothecompetitivenessofitshostduringcolonizationofthemurinegastrointestinaltract AT tracylraivio isolationandcharacterizationofanoveltemperateescherichiacolibacteriophagekapi1whichmodifiestheoantigenandcontributestothecompetitivenessofitshostduringcolonizationofthemurinegastrointestinaltract |