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

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 i...

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Main Authors: Saki Onishi-Sakamoto, Tadashi Fujii, Keito Watanabe, Reina Makida, Keita Iyori, Yoichi Toyoda, Takumi Tochio, Koji Nishifuji
Format: Article
Language:English
Published: Frontiers Media S.A. 2024-01-01
Series:Frontiers in Veterinary Science
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fvets.2023.1272595/full
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author Saki Onishi-Sakamoto
Tadashi Fujii
Tadashi Fujii
Keito Watanabe
Reina Makida
Keita Iyori
Yoichi Toyoda
Takumi Tochio
Takumi Tochio
Koji Nishifuji
author_facet Saki Onishi-Sakamoto
Tadashi Fujii
Tadashi Fujii
Keito Watanabe
Reina Makida
Keita Iyori
Yoichi Toyoda
Takumi Tochio
Takumi Tochio
Koji Nishifuji
author_sort Saki Onishi-Sakamoto
collection DOAJ
description 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.
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spelling doaj.art-9dab64860e6f4b68981275752a52b5872024-01-04T05:02:41ZengFrontiers Media S.A.Frontiers in Veterinary Science2297-17692024-01-011010.3389/fvets.2023.12725951272595Erythritol alters phosphotransferase gene expression and inhibits the in vitro growth of Staphylococcus coagulans isolated from canines with pyodermaSaki Onishi-Sakamoto0Tadashi Fujii1Tadashi Fujii2Keito Watanabe3Reina Makida4Keita Iyori5Yoichi Toyoda6Takumi Tochio7Takumi Tochio8Koji Nishifuji9Cooperative Division of Veterinary Sciences, Graduate School of Agriculture, Tokyo University of Agriculture and Technology, Fuchu, Tokyo, JapanDepartment of Gastroenterology and Hepatology, Fujita Health University, Toyoake, JapanDepartment of Medical Research on Prebiotics and Probiotics, Fujita Health University, Toyoake, JapanCooperative Department of Veterinary Medicine, Faculty of Agriculture, Tokyo University of Agriculture and Technology, Fuchu, Tokyo, JapanResearch and Development Center, B Food Science Co., Ltd., Chita, JapanDermatological and Laboratory Service for Animals, Vet Derm Tokyo, Fujisawa, JapanDermatological and Laboratory Service for Animals, Vet Derm Tokyo, Fujisawa, JapanDepartment of Gastroenterology and Hepatology, Fujita Health University, Toyoake, JapanDepartment of Medical Research on Prebiotics and Probiotics, Fujita Health University, Toyoake, JapanDivision of Animal Life Science, Institute of Agriculture, Tokyo University of Agriculture and Technology, Fuchu, Tokyo, JapanStaphylococcus 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.https://www.frontiersin.org/articles/10.3389/fvets.2023.1272595/fullerythritolStaphylococcus coagulansdogpyodermaglucosephosphotransferase system
spellingShingle Saki Onishi-Sakamoto
Tadashi Fujii
Tadashi Fujii
Keito Watanabe
Reina Makida
Keita Iyori
Yoichi Toyoda
Takumi Tochio
Takumi Tochio
Koji Nishifuji
Erythritol alters phosphotransferase gene expression and inhibits the in vitro growth of Staphylococcus coagulans isolated from canines with pyoderma
Frontiers in Veterinary Science
erythritol
Staphylococcus coagulans
dog
pyoderma
glucose
phosphotransferase system
title Erythritol alters phosphotransferase gene expression and inhibits the in vitro growth of Staphylococcus coagulans isolated from canines with pyoderma
title_full Erythritol alters phosphotransferase gene expression and inhibits the in vitro growth of Staphylococcus coagulans isolated from canines with pyoderma
title_fullStr Erythritol alters phosphotransferase gene expression and inhibits the in vitro growth of Staphylococcus coagulans isolated from canines with pyoderma
title_full_unstemmed Erythritol alters phosphotransferase gene expression and inhibits the in vitro growth of Staphylococcus coagulans isolated from canines with pyoderma
title_short Erythritol alters phosphotransferase gene expression and inhibits the in vitro growth of Staphylococcus coagulans isolated from canines with pyoderma
title_sort erythritol alters phosphotransferase gene expression and inhibits the in vitro growth of staphylococcus coagulans isolated from canines with pyoderma
topic erythritol
Staphylococcus coagulans
dog
pyoderma
glucose
phosphotransferase system
url https://www.frontiersin.org/articles/10.3389/fvets.2023.1272595/full
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