Diabetes mellitus promotes the nasal colonization of high virulent Staphylococcus aureus through the regulation of SaeRS two-component system

ABSTRACTDiabetic foot infections are a common complication of diabetes. Staphylococcus aureus is frequently isolated from diabetic foot infections and commonly colonizes human nares. According to the study, the nasal microbiome analysis revealed that diabetic patients had a significantly altered nas...

Full description

Bibliographic Details
Main Authors: Qichen Wang, Nadira Nurxat, Lei Zhang, Yao Liu, Yanan Wang, Na Zhao, Yingxin Dai, Ying Jian, Lei He, Hua Wang, Taeok Bae, Min Li, Qian Liu
Format: Article
Language:English
Published: Taylor & Francis Group 2023-12-01
Series:Emerging Microbes and Infections
Subjects:
Online Access:https://www.tandfonline.com/doi/10.1080/22221751.2023.2276335
_version_ 1797257041124786176
author Qichen Wang
Nadira Nurxat
Lei Zhang
Yao Liu
Yanan Wang
Lei Zhang
Na Zhao
Yingxin Dai
Ying Jian
Lei He
Hua Wang
Taeok Bae
Min Li
Qian Liu
author_facet Qichen Wang
Nadira Nurxat
Lei Zhang
Yao Liu
Yanan Wang
Lei Zhang
Na Zhao
Yingxin Dai
Ying Jian
Lei He
Hua Wang
Taeok Bae
Min Li
Qian Liu
author_sort Qichen Wang
collection DOAJ
description ABSTRACTDiabetic foot infections are a common complication of diabetes. Staphylococcus aureus is frequently isolated from diabetic foot infections and commonly colonizes human nares. According to the study, the nasal microbiome analysis revealed that diabetic patients had a significantly altered nasal microbial composition and diversity. Typically, the fasting blood glucose (FBG) level had an impact on the abundance and sequence type (ST) of S. aureus in diabetic patients. We observed that highly virulent S. aureus ST7 strains were more frequently colonized in diabetic patients, especially those with poorly controlled FBG, while ST59 was dominant in healthy individuals. S. aureus ST7 strains were more resistant to human antimicrobial peptides and formed stronger biofilms than ST59 strains. Critically, S. aureus ST7 strains displayed higher virulence compared to ST59 strains in vivo. The dominance of S. aureus ST7 strains in hyperglycemic environment is due to the higher activity of the SaeRS two-component system (TCS). S. aureus ST7 strains outcompeted ST59 both in vitro, and in nasal colonization model in diabetic mice, which was abolished by the deletion of the SaeRS TCS. Our data indicated that highly virulent S. aureus strains preferentially colonize diabetic patients with poorly controlled FBG through SaeRS TCS. Detection of S. aureus colonization and elimination of colonizing S. aureus are critical in the care of diabetic patients with high FBG.
first_indexed 2024-03-08T11:52:08Z
format Article
id doaj.art-32b89f34cea84aeaad2573583baabc2a
institution Directory Open Access Journal
issn 2222-1751
language English
last_indexed 2024-04-24T22:31:20Z
publishDate 2023-12-01
publisher Taylor & Francis Group
record_format Article
series Emerging Microbes and Infections
spelling doaj.art-32b89f34cea84aeaad2573583baabc2a2024-03-19T19:34:17ZengTaylor & Francis GroupEmerging Microbes and Infections2222-17512023-12-0112210.1080/22221751.2023.2276335Diabetes mellitus promotes the nasal colonization of high virulent Staphylococcus aureus through the regulation of SaeRS two-component systemQichen Wang0Nadira Nurxat1Lei Zhang2Yao Liu3Yanan Wang4Lei Zhang5Na Zhao6Yingxin Dai7Ying Jian8Lei He9Hua Wang10Taeok Bae11Min Li12Qian Liu13Department of Laboratory Medicine, Ren Ji Hospital, School of Medicine, Shanghai Jiao Tong University, Shanghai, People’s Republic of ChinaDepartment of Laboratory Medicine, Ren Ji Hospital, School of Medicine, Shanghai Jiao Tong University, Shanghai, People’s Republic of ChinaDepartment of Vascular Surgery, Yueyang Hospital of Integrated Traditional Chinese and Western Medicine, Shanghai University of Traditional Chinese Medicine, Shanghai, People’s Republic of ChinaDepartment of Laboratory Medicine, Ren Ji Hospital, School of Medicine, Shanghai Jiao Tong University, Shanghai, People’s Republic of ChinaDepartment of Laboratory Medicine, Ren Ji Hospital, School of Medicine, Shanghai Jiao Tong University, Shanghai, People’s Republic of ChinaDepartment of Otorhinolaryngology, Head and Neck Surgery, The Second Hospital of Anhui Medical University, Hefei, People’s Republic of ChinaDepartment of Laboratory Medicine, Ren Ji Hospital, School of Medicine, Shanghai Jiao Tong University, Shanghai, People’s Republic of ChinaDepartment of Laboratory Medicine, Ren Ji Hospital, School of Medicine, Shanghai Jiao Tong University, Shanghai, People’s Republic of ChinaDepartment of Laboratory Medicine, Ren Ji Hospital, School of Medicine, Shanghai Jiao Tong University, Shanghai, People’s Republic of ChinaDepartment of Laboratory Medicine, Ren Ji Hospital, School of Medicine, Shanghai Jiao Tong University, Shanghai, People’s Republic of ChinaDepartment of Laboratory Medicine, Ren Ji Hospital, School of Medicine, Shanghai Jiao Tong University, Shanghai, People’s Republic of ChinaDepartment of Microbiology and Immunology, Indiana University School of Medicine-Northwest, Gary, IN, USADepartment of Laboratory Medicine, Ren Ji Hospital, School of Medicine, Shanghai Jiao Tong University, Shanghai, People’s Republic of ChinaDepartment of Laboratory Medicine, Ren Ji Hospital, School of Medicine, Shanghai Jiao Tong University, Shanghai, People’s Republic of ChinaABSTRACTDiabetic foot infections are a common complication of diabetes. Staphylococcus aureus is frequently isolated from diabetic foot infections and commonly colonizes human nares. According to the study, the nasal microbiome analysis revealed that diabetic patients had a significantly altered nasal microbial composition and diversity. Typically, the fasting blood glucose (FBG) level had an impact on the abundance and sequence type (ST) of S. aureus in diabetic patients. We observed that highly virulent S. aureus ST7 strains were more frequently colonized in diabetic patients, especially those with poorly controlled FBG, while ST59 was dominant in healthy individuals. S. aureus ST7 strains were more resistant to human antimicrobial peptides and formed stronger biofilms than ST59 strains. Critically, S. aureus ST7 strains displayed higher virulence compared to ST59 strains in vivo. The dominance of S. aureus ST7 strains in hyperglycemic environment is due to the higher activity of the SaeRS two-component system (TCS). S. aureus ST7 strains outcompeted ST59 both in vitro, and in nasal colonization model in diabetic mice, which was abolished by the deletion of the SaeRS TCS. Our data indicated that highly virulent S. aureus strains preferentially colonize diabetic patients with poorly controlled FBG through SaeRS TCS. Detection of S. aureus colonization and elimination of colonizing S. aureus are critical in the care of diabetic patients with high FBG.https://www.tandfonline.com/doi/10.1080/22221751.2023.2276335DiabetesStaphylococcus aureuscolonizationSaeRS two-component systemmicrobiome
spellingShingle Qichen Wang
Nadira Nurxat
Lei Zhang
Yao Liu
Yanan Wang
Lei Zhang
Na Zhao
Yingxin Dai
Ying Jian
Lei He
Hua Wang
Taeok Bae
Min Li
Qian Liu
Diabetes mellitus promotes the nasal colonization of high virulent Staphylococcus aureus through the regulation of SaeRS two-component system
Emerging Microbes and Infections
Diabetes
Staphylococcus aureus
colonization
SaeRS two-component system
microbiome
title Diabetes mellitus promotes the nasal colonization of high virulent Staphylococcus aureus through the regulation of SaeRS two-component system
title_full Diabetes mellitus promotes the nasal colonization of high virulent Staphylococcus aureus through the regulation of SaeRS two-component system
title_fullStr Diabetes mellitus promotes the nasal colonization of high virulent Staphylococcus aureus through the regulation of SaeRS two-component system
title_full_unstemmed Diabetes mellitus promotes the nasal colonization of high virulent Staphylococcus aureus through the regulation of SaeRS two-component system
title_short Diabetes mellitus promotes the nasal colonization of high virulent Staphylococcus aureus through the regulation of SaeRS two-component system
title_sort diabetes mellitus promotes the nasal colonization of high virulent staphylococcus aureus through the regulation of saers two component system
topic Diabetes
Staphylococcus aureus
colonization
SaeRS two-component system
microbiome
url https://www.tandfonline.com/doi/10.1080/22221751.2023.2276335
work_keys_str_mv AT qichenwang diabetesmellituspromotesthenasalcolonizationofhighvirulentstaphylococcusaureusthroughtheregulationofsaerstwocomponentsystem
AT nadiranurxat diabetesmellituspromotesthenasalcolonizationofhighvirulentstaphylococcusaureusthroughtheregulationofsaerstwocomponentsystem
AT leizhang diabetesmellituspromotesthenasalcolonizationofhighvirulentstaphylococcusaureusthroughtheregulationofsaerstwocomponentsystem
AT yaoliu diabetesmellituspromotesthenasalcolonizationofhighvirulentstaphylococcusaureusthroughtheregulationofsaerstwocomponentsystem
AT yananwang diabetesmellituspromotesthenasalcolonizationofhighvirulentstaphylococcusaureusthroughtheregulationofsaerstwocomponentsystem
AT leizhang diabetesmellituspromotesthenasalcolonizationofhighvirulentstaphylococcusaureusthroughtheregulationofsaerstwocomponentsystem
AT nazhao diabetesmellituspromotesthenasalcolonizationofhighvirulentstaphylococcusaureusthroughtheregulationofsaerstwocomponentsystem
AT yingxindai diabetesmellituspromotesthenasalcolonizationofhighvirulentstaphylococcusaureusthroughtheregulationofsaerstwocomponentsystem
AT yingjian diabetesmellituspromotesthenasalcolonizationofhighvirulentstaphylococcusaureusthroughtheregulationofsaerstwocomponentsystem
AT leihe diabetesmellituspromotesthenasalcolonizationofhighvirulentstaphylococcusaureusthroughtheregulationofsaerstwocomponentsystem
AT huawang diabetesmellituspromotesthenasalcolonizationofhighvirulentstaphylococcusaureusthroughtheregulationofsaerstwocomponentsystem
AT taeokbae diabetesmellituspromotesthenasalcolonizationofhighvirulentstaphylococcusaureusthroughtheregulationofsaerstwocomponentsystem
AT minli diabetesmellituspromotesthenasalcolonizationofhighvirulentstaphylococcusaureusthroughtheregulationofsaerstwocomponentsystem
AT qianliu diabetesmellituspromotesthenasalcolonizationofhighvirulentstaphylococcusaureusthroughtheregulationofsaerstwocomponentsystem