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. 2024 Jan 4:10:1272595.
doi: 10.3389/fvets.2023.1272595. eCollection 2023.

Erythritol alters phosphotransferase gene expression and inhibits the in vitro growth of Staphylococcus coagulans isolated from canines with pyoderma

Saki Onishi-Sakamoto  1 , Tadashi Fujii  2   3 , Keito Watanabe  4 , Reina Makida  5 , Keita Iyori  6 , Yoichi Toyoda  6 , Takumi Tochio  2   3 , Koji Nishifuji  7
Affiliations

Erythritol alters phosphotransferase gene expression and inhibits the in vitro growth of Staphylococcus coagulans isolated from canines with pyoderma

Saki Onishi-Sakamoto et al. Front Vet Sci. .

Abstract

Staphylococcus coagulans (SC) belongs to a group of coagulase-positive staphylococci occasionally isolated from the skin lesions of dogs with pyoderma. We recently revealed that erythritol, a sugar alcohol, inhibited the growth of SC strain JCM7470. This study investigated the molecular mechanisms involved in this growth inhibition of JCM7470 by erythritol, and determine whether erythritol inhibits the growth of SC isolated from the skin of dogs with pyoderma. Comprehensive analysis of the gene expression of JCM7470 in the presence of erythritol revealed that erythritol upregulated the expression of glcB and ptsG genes, both of which encode phosphotransferase system (PTS) glucoside- and glucose-specific permease C, B, and A domains (EIICBA), respectively, associated with sugar uptake. Moreover, erythritol suppressed in vitro growth of all 27 SC strains isolated from the skin lesions of canine pyoderma, including 13 mecA gene-positive and 14 mecA gene-negative strains. Finally, the growth inhibition of the SC clinical isolates by erythritol was restored by the addition of glucose. In summary, we revealed that erythritol promotes PTS gene expression and suppresses the in vitro growth of SC clinical isolates from dogs with pyoderma. Restoration of the erythritol-induced growth inhibition by glucose suggested that glucose starvation may contribute to the growth inhibition of SC.

Keywords: Staphylococcus coagulans; dog; erythritol; glucose; phosphotransferase system; pyoderma.

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Conflict of interest statement

RM is an employee of B Food Science Co., Ltd. TF and TT were employees of the same company at the time when this study was started. KI was employed by Vet Derm Tokyo Ltd. where YT the representative director. The remaining authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Figures

Figure 1
Figure 1
Gene expression analysis. (A) PCA plot shows a clear split between the control and erythritol-treated Staphylococcus coagulans JCM7470, with 80% of the variance explained by PC1. (B) The volcano plot shows differences in expression levels of up- and downregulated genes in JCM7470 treated with erythritol. The genes upregulated >10-fold (log2FC > 3.322, p < 0.05) in response to erythritol are highlighted in red. (C) Comparison of the expression levels of glcB and ptsG genes in JCM7470 treated with erythritol or control medium, as determined by RT-qPCR. **p < 0.01.
Figure 2
Figure 2
Restoration of erythritol-induced growth inhibition of SC clinical isolates by glucose supplementation. (A) Bacterial turbidity of the SC clinical isolates (n = 27) immediately or 6 h after incubation with different doses of erythritol. (B) Comparison of bacterial turbidity between mecA gene-positive and -negative SC strains 6 h after incubation with different doses of erythritol. (C) Fluctuation of the bacterial turbidity of the SC strains incubated with different doses of erythritol and glucose. ns, not significant; ****p < 0.0001.
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