Article

Exploring synergistic effect of bacteriophages with probiotics against multidrug resistant Salmonella Typhimurium in a simulated chicken gastrointestinal system using metagenomic- and culturomic approaches

Youbin Choi1, An Kang1, Min-Geun Kang1, Daniel Junpyo Lee1, Dawon Kyoung1, Min-Jin Kwak2, Jung Min Heo3, Minho Song3, Sangnam Oh4, Younghoon Kim1,*
Author Information & Copyright
1Department of Agricultural Biotechnology and Research Institute of Agriculture and Life Science, Seoul National University, Seoul 08826, Korea.
2Emerging Pathogens Institute, Department of Animal Sciences, University of Florida, Gainesville, FL 32611, United States.
3Department of Animal Science and Biotechnology, Chungnam National University, Daejeon 34134, Korea.
4Department of Functional Food and Biotechnology, Jeonju University, Jeonju 55069, Korea.
*Corresponding Author: Younghoon Kim, Department of Agricultural Biotechnology and Research Institute of Agriculture and Life Science, Seoul National University, Seoul 08826, Korea, Republic of. Phone: +8228804808. E-mail: junpyo1357@snu.ac.kr.

© Copyright 2025 Korean Society of Animal Science and Technology. This is an Open-Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

Abstract

The present study explored the synergistic potential of combining bacteriophages and probiotics as a dual approach for <italic>Salmonella</italic> suppression and gut microbiota modulation. Using a multiomics approach integrating culture and metagenomics, we isolated <italic>Lactobacillus</italic> <italic>reuteri</italic> J2M1, a robust probiotic strain with strong acid and bile tolerance, intestinal adhesion, and safety profiles. Concurrently, two bacteriophages, SLAM_phiST45 and SLAM_phiST56, targeting <italic>Salmonella</italic> Typhimurium were selected based on their broad host range, enhanced inhibitory effects as a cocktail, and genomic safety validated through whole-genome sequencing. In a model that simulated the gut environment of poultry, the combined application of bacteriophages and <italic>L. reuteri</italic> J2M1 resulted in significant changes in the microbial community at the genus level. Although the application of bacteriophages alone effectively reduced <italic>Salmonella</italic> populations, it also led to the proliferation of genera containing potential pathogens, such as <italic>Clostridium perfringens</italic>. In contrast, the co-application of <italic>L. reuteri</italic> J2M1 mitigated these negative effects by promoting the growth of beneficial genera, including <italic>Oscillibacter</italic> and <italic>Clostridium butyricum</italic>, which are associated with anti-inflammatory properties and gut health. These findings demonstrate that combining bacteriophages with probiotics suppresses pathogens as well as contributes to the establishment of a balanced gut microbial community. This study highlights the utility of a multiomics approach for probiotic discovery, the efficacy of bacteriophage cocktails in pathogen suppression, and the benefits of their synergistic application with probiotics. Although <italic>in vivo</italic> validation is required, these in vitro results provide a robust foundation for the development of sustainable and effective alternatives to antibiotics for poultry production.

Keywords: Salmonella; bacteriophages; probiotics; multi-omics; simulated chicken gastrointestinal system