Modulation of virulence and metabolic profiles in Klebsiella pneumoniae under indole-mediated stress response
Indole, a crucial bacterial signaling molecule, plays a fundamental role in regulating various physiological processes within bacteria, including growth, acid tolerance, biofilm development, motility, and other cellular functions. Its regulatory influence extends beyond indole-producing bacteria, si...
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2025-02-01
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| Series: | Frontiers in Cellular and Infection Microbiology |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fcimb.2025.1546991/full |
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| author | Xueyao Fang Yanhui Chen Longhua Hu Shumin Gu Junqi Zhu Yaping Hang Xingwei Cao Yanping Xiao Hong Luo Chuwen Zhao Lianhua Xiao Qiaoshi Zhong |
| author_facet | Xueyao Fang Yanhui Chen Longhua Hu Shumin Gu Junqi Zhu Yaping Hang Xingwei Cao Yanping Xiao Hong Luo Chuwen Zhao Lianhua Xiao Qiaoshi Zhong |
| author_sort | Xueyao Fang |
| collection | DOAJ |
| description | Indole, a crucial bacterial signaling molecule, plays a fundamental role in regulating various physiological processes within bacteria, including growth, acid tolerance, biofilm development, motility, and other cellular functions. Its regulatory influence extends beyond indole-producing bacteria, significantly impacting the physiological activities in non-indole-producing species. In this study, we demonstrate that indole enhances the pathogenicity and viability of Klebsiella pneumoniae using the Galleria mellonella infection model and serum killing assay. Concurrently, indole has varying effects on biofilm formation in K. pneumoniae, with some strains showing enhanced biofilm formation ability. To elucidate the underlying molecular mechanisms, transcriptome analysis revealed that indole exposure in K. pneumoniae led to the upregulation of genes associated with pili formation and iron acquisition systems, while simultaneously inducing oxidative stress responses. Additionally, our analysis uncovered extensive metabolic remodeling. Specifically, we observed significant upregulation of genes involved in simple carbohydrate utilization pathways, including those responsible for galactose, mannose, and maltose metabolism, as well as enhanced expression of genes associated with pyrimidine biosynthesis. These findings collectively indicate that indole enhances the intestinal colonization and pathogenicity of K. pneumoniae primarily by modulation of fimbriae expression and metabolic pathway regulation. |
| format | Article |
| id | doaj-art-35c8cd360dd245928fc1e19b04244995 |
| institution | Kabale University |
| issn | 2235-2988 |
| language | English |
| publishDate | 2025-02-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Cellular and Infection Microbiology |
| spelling | doaj-art-35c8cd360dd245928fc1e19b042449952025-02-03T06:33:33ZengFrontiers Media S.A.Frontiers in Cellular and Infection Microbiology2235-29882025-02-011510.3389/fcimb.2025.15469911546991Modulation of virulence and metabolic profiles in Klebsiella pneumoniae under indole-mediated stress responseXueyao Fang0Yanhui Chen1Longhua Hu2Shumin Gu3Junqi Zhu4Yaping Hang5Xingwei Cao6Yanping Xiao7Hong Luo8Chuwen Zhao9Lianhua Xiao10Qiaoshi Zhong11Jiangxi Province Key Laboratory of Immunology and Inflammation, Jiangxi Provincial Clinical Research Center for Laboratory Medicine, Department of Clinical Laboratory, The Second Affiliated Hospital, Jiangxi Medical College, Nanchang University, Nanchang, Jiangxi, ChinaJiangxi Province Key Laboratory of Immunology and Inflammation, Jiangxi Provincial Clinical Research Center for Laboratory Medicine, Department of Clinical Laboratory, The Second Affiliated Hospital, Jiangxi Medical College, Nanchang University, Nanchang, Jiangxi, ChinaJiangxi Province Key Laboratory of Immunology and Inflammation, Jiangxi Provincial Clinical Research Center for Laboratory Medicine, Department of Clinical Laboratory, The Second Affiliated Hospital, Jiangxi Medical College, Nanchang University, Nanchang, Jiangxi, ChinaJiangxi Province Key Laboratory of Immunology and Inflammation, Jiangxi Provincial Clinical Research Center for Laboratory Medicine, Department of Clinical Laboratory, The Second Affiliated Hospital, Jiangxi Medical College, Nanchang University, Nanchang, Jiangxi, ChinaJiangxi Province Key Laboratory of Immunology and Inflammation, Jiangxi Provincial Clinical Research Center for Laboratory Medicine, Department of Clinical Laboratory, The Second Affiliated Hospital, Jiangxi Medical College, Nanchang University, Nanchang, Jiangxi, ChinaJiangxi Province Key Laboratory of Immunology and Inflammation, Jiangxi Provincial Clinical Research Center for Laboratory Medicine, Department of Clinical Laboratory, The Second Affiliated Hospital, Jiangxi Medical College, Nanchang University, Nanchang, Jiangxi, ChinaJiangxi Province Key Laboratory of Immunology and Inflammation, Jiangxi Provincial Clinical Research Center for Laboratory Medicine, Department of Clinical Laboratory, The Second Affiliated Hospital, Jiangxi Medical College, Nanchang University, Nanchang, Jiangxi, ChinaJiangxi Province Key Laboratory of Immunology and Inflammation, Jiangxi Provincial Clinical Research Center for Laboratory Medicine, Department of Clinical Laboratory, The Second Affiliated Hospital, Jiangxi Medical College, Nanchang University, Nanchang, Jiangxi, ChinaJiangxi Province Key Laboratory of Immunology and Inflammation, Jiangxi Provincial Clinical Research Center for Laboratory Medicine, Department of Clinical Laboratory, The Second Affiliated Hospital, Jiangxi Medical College, Nanchang University, Nanchang, Jiangxi, ChinaJiangxi Province Key Laboratory of Immunology and Inflammation, Jiangxi Provincial Clinical Research Center for Laboratory Medicine, Department of Clinical Laboratory, The Second Affiliated Hospital, Jiangxi Medical College, Nanchang University, Nanchang, Jiangxi, ChinaDepartment of Marriage and Pregnancy, Ganzhou Zhanggong District Maternal and Child Health Hospital, Ganzhou, Jiangxi, ChinaJiangxi Province Key Laboratory of Immunology and Inflammation, Jiangxi Provincial Clinical Research Center for Laboratory Medicine, Department of Clinical Laboratory, The Second Affiliated Hospital, Jiangxi Medical College, Nanchang University, Nanchang, Jiangxi, ChinaIndole, a crucial bacterial signaling molecule, plays a fundamental role in regulating various physiological processes within bacteria, including growth, acid tolerance, biofilm development, motility, and other cellular functions. Its regulatory influence extends beyond indole-producing bacteria, significantly impacting the physiological activities in non-indole-producing species. In this study, we demonstrate that indole enhances the pathogenicity and viability of Klebsiella pneumoniae using the Galleria mellonella infection model and serum killing assay. Concurrently, indole has varying effects on biofilm formation in K. pneumoniae, with some strains showing enhanced biofilm formation ability. To elucidate the underlying molecular mechanisms, transcriptome analysis revealed that indole exposure in K. pneumoniae led to the upregulation of genes associated with pili formation and iron acquisition systems, while simultaneously inducing oxidative stress responses. Additionally, our analysis uncovered extensive metabolic remodeling. Specifically, we observed significant upregulation of genes involved in simple carbohydrate utilization pathways, including those responsible for galactose, mannose, and maltose metabolism, as well as enhanced expression of genes associated with pyrimidine biosynthesis. These findings collectively indicate that indole enhances the intestinal colonization and pathogenicity of K. pneumoniae primarily by modulation of fimbriae expression and metabolic pathway regulation.https://www.frontiersin.org/articles/10.3389/fcimb.2025.1546991/fullK. pneumoniaeindolefimbriaemetabolismvirulence |
| spellingShingle | Xueyao Fang Yanhui Chen Longhua Hu Shumin Gu Junqi Zhu Yaping Hang Xingwei Cao Yanping Xiao Hong Luo Chuwen Zhao Lianhua Xiao Qiaoshi Zhong Modulation of virulence and metabolic profiles in Klebsiella pneumoniae under indole-mediated stress response Frontiers in Cellular and Infection Microbiology K. pneumoniae indole fimbriae metabolism virulence |
| title | Modulation of virulence and metabolic profiles in Klebsiella pneumoniae under indole-mediated stress response |
| title_full | Modulation of virulence and metabolic profiles in Klebsiella pneumoniae under indole-mediated stress response |
| title_fullStr | Modulation of virulence and metabolic profiles in Klebsiella pneumoniae under indole-mediated stress response |
| title_full_unstemmed | Modulation of virulence and metabolic profiles in Klebsiella pneumoniae under indole-mediated stress response |
| title_short | Modulation of virulence and metabolic profiles in Klebsiella pneumoniae under indole-mediated stress response |
| title_sort | modulation of virulence and metabolic profiles in klebsiella pneumoniae under indole mediated stress response |
| topic | K. pneumoniae indole fimbriae metabolism virulence |
| url | https://www.frontiersin.org/articles/10.3389/fcimb.2025.1546991/full |
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