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. 2024 Nov 22;12(12):2400.
doi: 10.3390/microorganisms12122400.

Salmonella Phage vB_SpuM_X5: A Novel Approach to Reducing Salmonella Biofilms with Implications for Food Safety

Xinxin Jin  1   2 , Xiuxiu Sun  1 , Qin Lu  2 , Zui Wang  1   2 , Zhenggang Zhang  2   3 , Xiaochun Ling  2 , Yunpeng Xu  2   3 , Ruiqin Liang  2   3 , Junjie Yang  1   2 , Li Li  1   2 , Tengfei Zhang  2   3 , Qingping Luo  2   3   4 , Guofu Cheng  1
Affiliations

Salmonella Phage vB_SpuM_X5: A Novel Approach to Reducing Salmonella Biofilms with Implications for Food Safety

Xinxin Jin et al. Microorganisms. .

Abstract

Salmonella, a prevalent foodborne pathogen, poses a significant social and economic strain on both food safety and public health. The application of phages in the control of foodborne pathogens represents an emerging research area. In this study, Salmonella pullorum phage vB_SpuM_X5 (phage X5) was isolated from chicken farm sewage samples. The results revealed that phage X5 is a novel Myoviridae phage. Phage X5 has adequate temperature tolerance (28 °C-60 °C), pH stability (4-12), and a broad host range of Salmonella bacteria (87.50% of tested strains). The addition of phage X5 (MOI of 100 and 1000) to milk inoculated with Salmonella reduced the number of Salmonella by 0.72 to 0.93 log10 CFU/mL and 0.66 to 1.06 log10 CFU/mL at 4 °C and 25 °C, respectively. The addition of phage X5 (MOI of 100 and 1000) to chicken breast inoculated with Salmonella reduced bacterial numbers by 1.13 to 2.42 log10 CFU/mL and 0.81 to 1.25 log10 CFU/mL at 4 °C and 25 °C, respectively. Phage X5 has bactericidal activity against Salmonella and can be used as a potential biological bacteriostatic agent to remove mature biofilms of Salmonella or for the prevention and control of Salmonella.

Keywords: Salmonella; bacteriostatic agent; biofilm; phage.

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Conflict of interest statement

The authors declare no conflict of interest.

Figures

Figure 1
Figure 1
Morphology and microscopic morphology of phage X5 plaque. (A) Phage X5 plaque morphology. (B) Microscopic morphology of phage X5 under transmission electron microscopy. The scale is 100 nm.
Figure 2
Figure 2
Biological characteristics of phage X5. Stability of phage X5 at different temperatures (A) and pH values (B). (C) Optimal MOI of phage X5. (D) Determination of chloroform sensitivity of phage X5. (E) Adsorption rate of phage X5. (F) One–step growth curve.
Figure 3
Figure 3
Genome map of phage X5 generated by CGView. Green areas indicate the distribution of the coding sequence (CDS) regions; arrows indicate the direction of transcription. The total GC.
Figure 4
Figure 4
Phylogenetic evolutionary tree of phage X5. The phylogenetic tree was constructed based on the neighbor–joining method of the terminase large subunit.
Figure 5
Figure 5
Collinearity analysis of phage X5 and GSP044 genomes.
Figure 6
Figure 6
Effect of phage X5 on bacterial biofilm. The initial titers of phage X5 were 105 and 107 PFU/well. The biofilm biomass was obtained after incubation for 24 h. (A) Crystal violet staining analysis. (B) Optical density values measured at 600 nm. (C) Plate count results. The results are expressed as the mean ± SD (standard deviation) of three independent experiments. The one–way ANOVA method was used to assess significant differences between control and test samples. *** p < 0.001, **** p < 0.0001. (D) Pattern diagram of phage entry into bacteria.
Figure 7
Figure 7
Application of phage X5 in the biological control of S. pullorum 519 in milk. (A) Effects of phage X5 on the growth of S. pullorum 519 in milk at 4 °C. (B) Effects of phage X5 on the growth of S. pullorum 519 in milk at 25 °C. * p < 0.05; ** p < 0.01; *** p < 0.001.
Figure 8
Figure 8
Application of phage X5 in biological control of S. pullorum 519 in chicken breast. (A) Effects of phage X5 on the growth of S. pullorum 519 in chicken breast at 4 °C. (B) Effects of phage X5 on the growth of S. pullorum 519 in chicken breast at 25 °C. * p < 0.05; ** p < 0.01; *** p < 0.001.
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