Efficient screening of adsorbed receptors for Salmonella phage LP31 and identification of receptor-binding protein
ABSTRACT The adsorption process is the first step in the lifecycle of phages and plays a decisive role in the entire infection process. Identifying the adsorption mechanism of phages not only makes phage therapy more precise and efficient but also enables the exploration of other potential applicati...
| Main Authors: | , , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
American Society for Microbiology
2023-10-01
|
| Series: | Microbiology Spectrum |
| Subjects: | |
| Online Access: | https://journals.asm.org/doi/10.1128/spectrum.02604-23 |
| _version_ | 1797658147235561472 |
|---|---|
| author | Haojie Ge Ling Ye Yueyi Cai Huimin Guo Dan Gu Zhengzhong Xu Maozhi Hu Heather E. Allison Xin'an Jiao Xiang Chen |
| author_facet | Haojie Ge Ling Ye Yueyi Cai Huimin Guo Dan Gu Zhengzhong Xu Maozhi Hu Heather E. Allison Xin'an Jiao Xiang Chen |
| author_sort | Haojie Ge |
| collection | DOAJ |
| description | ABSTRACT The adsorption process is the first step in the lifecycle of phages and plays a decisive role in the entire infection process. Identifying the adsorption mechanism of phages not only makes phage therapy more precise and efficient but also enables the exploration of other potential applications and modifications of phages. Phage LP31 can lyse multiple Salmonella serotypes, efficiently clearing biofilms formed by Salmonella enterica serovar Enteritidis (S. Enteritidis) and significantly reducing the concentration of S. Enteritidis in chicken feces. Therefore, LP31 has great potential for many practical applications. In this study, we established an efficient screening method for phage infection-related genes and identified a total of 10 genes related to the adsorption process of phage LP31. After the construction of strain C50041ΔrfaL 58−358, it was found that the knockout strain had a rough phenotype as an O-antigen-deficient strain. Adsorption rate and transmission electron microscopy experiments showed that the receptor for phage LP31 was the O9 antigen of S. Enteritidis. Homology comparison and adsorption experiments confirmed that the tail fiber protein Lp35 of phage LP31 participated in the adsorption process as a receptor-binding protein. IMPORTANCE A full understanding of the interaction between phages and their receptors can help with the development of phage-related products. Phages like LP31 with the tail fiber protein Lp35, or a closely related protein, have been reported to effectively recognize and infect multiple Salmonella serotypes. However, the role of these proteins in phage infection has not been previously described. In this study, we established an efficient screening method to detect phage adsorption to host receptors. We found that phage LP31 can utilize its tail fiber protein Lp35 to adsorb to the O9 antigen of S. Enteritidis, initiating the infection process. This study provides a great model system for further studies of how a phage-encoded receptor-binding protein (RBP) interacts with its host's RBP binding target, and this new model offers opportunities for further theoretical and experimental studies to understand the infection mechanism of phages. |
| first_indexed | 2024-03-11T17:55:58Z |
| format | Article |
| id | doaj.art-477fe862446d46dea3bc5ebe9fb2cc42 |
| institution | Directory Open Access Journal |
| issn | 2165-0497 |
| language | English |
| last_indexed | 2024-03-11T17:55:58Z |
| publishDate | 2023-10-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | Microbiology Spectrum |
| spelling | doaj.art-477fe862446d46dea3bc5ebe9fb2cc422023-10-17T13:04:36ZengAmerican Society for MicrobiologyMicrobiology Spectrum2165-04972023-10-0111510.1128/spectrum.02604-23Efficient screening of adsorbed receptors for Salmonella phage LP31 and identification of receptor-binding proteinHaojie Ge0Ling Ye1Yueyi Cai2Huimin Guo3Dan Gu4Zhengzhong Xu5Maozhi Hu6Heather E. Allison7Xin'an Jiao8Xiang Chen9Jiangsu Key Laboratory of Zoonosis/Jiangsu Co-Innovation Center for Prevention and Control of Important Animal Infectious Diseases and Zoonoses, Yangzhou University , Yangzhou, ChinaJiangsu Key Laboratory of Zoonosis/Jiangsu Co-Innovation Center for Prevention and Control of Important Animal Infectious Diseases and Zoonoses, Yangzhou University , Yangzhou, ChinaDepartment of Clinical Infection, Microbiology and Immunology, Institute of Infection, Veterinary and Ecological Sciences, University of Liverpool , Liverpool, United KingdomJiangsu Key Laboratory of Zoonosis/Jiangsu Co-Innovation Center for Prevention and Control of Important Animal Infectious Diseases and Zoonoses, Yangzhou University , Yangzhou, ChinaJiangsu Key Laboratory of Zoonosis/Jiangsu Co-Innovation Center for Prevention and Control of Important Animal Infectious Diseases and Zoonoses, Yangzhou University , Yangzhou, ChinaJiangsu Key Laboratory of Zoonosis/Jiangsu Co-Innovation Center for Prevention and Control of Important Animal Infectious Diseases and Zoonoses, Yangzhou University , Yangzhou, ChinaJiangsu Key Laboratory of Zoonosis/Jiangsu Co-Innovation Center for Prevention and Control of Important Animal Infectious Diseases and Zoonoses, Yangzhou University , Yangzhou, ChinaDepartment of Clinical Infection, Microbiology and Immunology, Institute of Infection, Veterinary and Ecological Sciences, University of Liverpool , Liverpool, United KingdomJiangsu Key Laboratory of Zoonosis/Jiangsu Co-Innovation Center for Prevention and Control of Important Animal Infectious Diseases and Zoonoses, Yangzhou University , Yangzhou, ChinaJiangsu Key Laboratory of Zoonosis/Jiangsu Co-Innovation Center for Prevention and Control of Important Animal Infectious Diseases and Zoonoses, Yangzhou University , Yangzhou, ChinaABSTRACT The adsorption process is the first step in the lifecycle of phages and plays a decisive role in the entire infection process. Identifying the adsorption mechanism of phages not only makes phage therapy more precise and efficient but also enables the exploration of other potential applications and modifications of phages. Phage LP31 can lyse multiple Salmonella serotypes, efficiently clearing biofilms formed by Salmonella enterica serovar Enteritidis (S. Enteritidis) and significantly reducing the concentration of S. Enteritidis in chicken feces. Therefore, LP31 has great potential for many practical applications. In this study, we established an efficient screening method for phage infection-related genes and identified a total of 10 genes related to the adsorption process of phage LP31. After the construction of strain C50041ΔrfaL 58−358, it was found that the knockout strain had a rough phenotype as an O-antigen-deficient strain. Adsorption rate and transmission electron microscopy experiments showed that the receptor for phage LP31 was the O9 antigen of S. Enteritidis. Homology comparison and adsorption experiments confirmed that the tail fiber protein Lp35 of phage LP31 participated in the adsorption process as a receptor-binding protein. IMPORTANCE A full understanding of the interaction between phages and their receptors can help with the development of phage-related products. Phages like LP31 with the tail fiber protein Lp35, or a closely related protein, have been reported to effectively recognize and infect multiple Salmonella serotypes. However, the role of these proteins in phage infection has not been previously described. In this study, we established an efficient screening method to detect phage adsorption to host receptors. We found that phage LP31 can utilize its tail fiber protein Lp35 to adsorb to the O9 antigen of S. Enteritidis, initiating the infection process. This study provides a great model system for further studies of how a phage-encoded receptor-binding protein (RBP) interacts with its host's RBP binding target, and this new model offers opportunities for further theoretical and experimental studies to understand the infection mechanism of phages.https://journals.asm.org/doi/10.1128/spectrum.02604-23phageadsorption receptorreceptor-binding proteinSalmonellaO9 antigen |
| spellingShingle | Haojie Ge Ling Ye Yueyi Cai Huimin Guo Dan Gu Zhengzhong Xu Maozhi Hu Heather E. Allison Xin'an Jiao Xiang Chen Efficient screening of adsorbed receptors for Salmonella phage LP31 and identification of receptor-binding protein Microbiology Spectrum phage adsorption receptor receptor-binding protein Salmonella O9 antigen |
| title | Efficient screening of adsorbed receptors for Salmonella phage LP31 and identification of receptor-binding protein |
| title_full | Efficient screening of adsorbed receptors for Salmonella phage LP31 and identification of receptor-binding protein |
| title_fullStr | Efficient screening of adsorbed receptors for Salmonella phage LP31 and identification of receptor-binding protein |
| title_full_unstemmed | Efficient screening of adsorbed receptors for Salmonella phage LP31 and identification of receptor-binding protein |
| title_short | Efficient screening of adsorbed receptors for Salmonella phage LP31 and identification of receptor-binding protein |
| title_sort | efficient screening of adsorbed receptors for salmonella phage lp31 and identification of receptor binding protein |
| topic | phage adsorption receptor receptor-binding protein Salmonella O9 antigen |
| url | https://journals.asm.org/doi/10.1128/spectrum.02604-23 |
| work_keys_str_mv | AT haojiege efficientscreeningofadsorbedreceptorsforsalmonellaphagelp31andidentificationofreceptorbindingprotein AT lingye efficientscreeningofadsorbedreceptorsforsalmonellaphagelp31andidentificationofreceptorbindingprotein AT yueyicai efficientscreeningofadsorbedreceptorsforsalmonellaphagelp31andidentificationofreceptorbindingprotein AT huiminguo efficientscreeningofadsorbedreceptorsforsalmonellaphagelp31andidentificationofreceptorbindingprotein AT dangu efficientscreeningofadsorbedreceptorsforsalmonellaphagelp31andidentificationofreceptorbindingprotein AT zhengzhongxu efficientscreeningofadsorbedreceptorsforsalmonellaphagelp31andidentificationofreceptorbindingprotein AT maozhihu efficientscreeningofadsorbedreceptorsforsalmonellaphagelp31andidentificationofreceptorbindingprotein AT heathereallison efficientscreeningofadsorbedreceptorsforsalmonellaphagelp31andidentificationofreceptorbindingprotein AT xinanjiao efficientscreeningofadsorbedreceptorsforsalmonellaphagelp31andidentificationofreceptorbindingprotein AT xiangchen efficientscreeningofadsorbedreceptorsforsalmonellaphagelp31andidentificationofreceptorbindingprotein |