Functional proteomics identify mannitol metabolism in serum resistance and therapeutic implications in Vibrio alginolyticus
Serum resistance is recognized as one of the most important pathogenic traits of bacterial pathogens, and no control measure is available. Based on our previous discovery that pathogenic Escherichia coli represses glycine, serine, and threonine metabolism to confer serum resistance and that the reac...
| Main Authors: | , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Frontiers Media S.A.
2022-10-01
|
| Series: | Frontiers in Immunology |
| Subjects: | |
| Online Access: | https://www.frontiersin.org/articles/10.3389/fimmu.2022.1010526/full |
| _version_ | 1811192257968078848 |
|---|---|
| author | Tian-shun Kou Tian-shun Kou Jia-han Wu Jia-han Wu Xuan-wei Chen Xuan-wei Chen Bo Peng Bo Peng |
| author_facet | Tian-shun Kou Tian-shun Kou Jia-han Wu Jia-han Wu Xuan-wei Chen Xuan-wei Chen Bo Peng Bo Peng |
| author_sort | Tian-shun Kou |
| collection | DOAJ |
| description | Serum resistance is recognized as one of the most important pathogenic traits of bacterial pathogens, and no control measure is available. Based on our previous discovery that pathogenic Escherichia coli represses glycine, serine, and threonine metabolism to confer serum resistance and that the reactivation of this pathway by exogenous glycine could restore serum sensitivity, we further investigate the mechanism underlying the action of glycine in Vibrio alginolyticus. Thus, V. alginolyticus is treated with glycine, and the proteomic change is profiled with tandem mass tag-based quantitative proteomics. Compared to the control group, glycine treatment influences the expression of a total of 291 proteins. Among them, a trap-type mannitol/chloroaromatic compound transport system with periplasmic component, encoded by N646_0992, is the most significantly increased protein. In combination with the pathway enrichment analysis showing the altered fructose and mannitol metabolism, mannitol has emerged as a possible metabolite in enhancing the serum killing activity. To demonstrate this, exogenous mannitol reduces bacterial viability. This synergistic effect is further confirmed in a V. alginolyticus–Danio rerio infection model. Furthermore, the mechanism underlying mannitol-enabled serum killing is dependent on glycolysis and the pyruvate cycle that increases the deposition of complement components C3b and C5b-9 on the bacterial surface, whereas inhibiting glycolysis or the pyruvate cycle significantly weakened the synergistic effects and complement deposition. These data together suggest that mannitol is a potent metabolite in reversing the serum resistance of V. alginolyticus and has promising use in aquaculture. |
| first_indexed | 2024-04-11T23:49:30Z |
| format | Article |
| id | doaj.art-1ed1db2cfc9a4995b0ffcfda65c1471f |
| institution | Directory Open Access Journal |
| issn | 1664-3224 |
| language | English |
| last_indexed | 2024-04-11T23:49:30Z |
| publishDate | 2022-10-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Immunology |
| spelling | doaj.art-1ed1db2cfc9a4995b0ffcfda65c1471f2022-12-22T03:56:31ZengFrontiers Media S.A.Frontiers in Immunology1664-32242022-10-011310.3389/fimmu.2022.10105261010526Functional proteomics identify mannitol metabolism in serum resistance and therapeutic implications in Vibrio alginolyticusTian-shun Kou0Tian-shun Kou1Jia-han Wu2Jia-han Wu3Xuan-wei Chen4Xuan-wei Chen5Bo Peng6Bo Peng7State Key Laboratory of Biocontrol, Guangdong Key Laboratory of Pharmaceutical Functional Genes, School of Life Sciences, Southern Marine Science and Engineering Guangdong Laboratory (Zhuhai), Sun Yat-sen University, Higher Education Mega Center, Guangzhou, ChinaLaboratory for Marine Biology and Biotechnology, Qingdao National Laboratory for Marine Science and Technology, Qingdao, ChinaState Key Laboratory of Biocontrol, Guangdong Key Laboratory of Pharmaceutical Functional Genes, School of Life Sciences, Southern Marine Science and Engineering Guangdong Laboratory (Zhuhai), Sun Yat-sen University, Higher Education Mega Center, Guangzhou, ChinaLaboratory for Marine Biology and Biotechnology, Qingdao National Laboratory for Marine Science and Technology, Qingdao, ChinaState Key Laboratory of Biocontrol, Guangdong Key Laboratory of Pharmaceutical Functional Genes, School of Life Sciences, Southern Marine Science and Engineering Guangdong Laboratory (Zhuhai), Sun Yat-sen University, Higher Education Mega Center, Guangzhou, ChinaLaboratory for Marine Biology and Biotechnology, Qingdao National Laboratory for Marine Science and Technology, Qingdao, ChinaState Key Laboratory of Biocontrol, Guangdong Key Laboratory of Pharmaceutical Functional Genes, School of Life Sciences, Southern Marine Science and Engineering Guangdong Laboratory (Zhuhai), Sun Yat-sen University, Higher Education Mega Center, Guangzhou, ChinaLaboratory for Marine Biology and Biotechnology, Qingdao National Laboratory for Marine Science and Technology, Qingdao, ChinaSerum resistance is recognized as one of the most important pathogenic traits of bacterial pathogens, and no control measure is available. Based on our previous discovery that pathogenic Escherichia coli represses glycine, serine, and threonine metabolism to confer serum resistance and that the reactivation of this pathway by exogenous glycine could restore serum sensitivity, we further investigate the mechanism underlying the action of glycine in Vibrio alginolyticus. Thus, V. alginolyticus is treated with glycine, and the proteomic change is profiled with tandem mass tag-based quantitative proteomics. Compared to the control group, glycine treatment influences the expression of a total of 291 proteins. Among them, a trap-type mannitol/chloroaromatic compound transport system with periplasmic component, encoded by N646_0992, is the most significantly increased protein. In combination with the pathway enrichment analysis showing the altered fructose and mannitol metabolism, mannitol has emerged as a possible metabolite in enhancing the serum killing activity. To demonstrate this, exogenous mannitol reduces bacterial viability. This synergistic effect is further confirmed in a V. alginolyticus–Danio rerio infection model. Furthermore, the mechanism underlying mannitol-enabled serum killing is dependent on glycolysis and the pyruvate cycle that increases the deposition of complement components C3b and C5b-9 on the bacterial surface, whereas inhibiting glycolysis or the pyruvate cycle significantly weakened the synergistic effects and complement deposition. These data together suggest that mannitol is a potent metabolite in reversing the serum resistance of V. alginolyticus and has promising use in aquaculture.https://www.frontiersin.org/articles/10.3389/fimmu.2022.1010526/fullmannitolVibriosserumproteomicsglycolysispyruvate cycle |
| spellingShingle | Tian-shun Kou Tian-shun Kou Jia-han Wu Jia-han Wu Xuan-wei Chen Xuan-wei Chen Bo Peng Bo Peng Functional proteomics identify mannitol metabolism in serum resistance and therapeutic implications in Vibrio alginolyticus Frontiers in Immunology mannitol Vibrios serum proteomics glycolysis pyruvate cycle |
| title | Functional proteomics identify mannitol metabolism in serum resistance and therapeutic implications in Vibrio alginolyticus |
| title_full | Functional proteomics identify mannitol metabolism in serum resistance and therapeutic implications in Vibrio alginolyticus |
| title_fullStr | Functional proteomics identify mannitol metabolism in serum resistance and therapeutic implications in Vibrio alginolyticus |
| title_full_unstemmed | Functional proteomics identify mannitol metabolism in serum resistance and therapeutic implications in Vibrio alginolyticus |
| title_short | Functional proteomics identify mannitol metabolism in serum resistance and therapeutic implications in Vibrio alginolyticus |
| title_sort | functional proteomics identify mannitol metabolism in serum resistance and therapeutic implications in vibrio alginolyticus |
| topic | mannitol Vibrios serum proteomics glycolysis pyruvate cycle |
| url | https://www.frontiersin.org/articles/10.3389/fimmu.2022.1010526/full |
| work_keys_str_mv | AT tianshunkou functionalproteomicsidentifymannitolmetabolisminserumresistanceandtherapeuticimplicationsinvibrioalginolyticus AT tianshunkou functionalproteomicsidentifymannitolmetabolisminserumresistanceandtherapeuticimplicationsinvibrioalginolyticus AT jiahanwu functionalproteomicsidentifymannitolmetabolisminserumresistanceandtherapeuticimplicationsinvibrioalginolyticus AT jiahanwu functionalproteomicsidentifymannitolmetabolisminserumresistanceandtherapeuticimplicationsinvibrioalginolyticus AT xuanweichen functionalproteomicsidentifymannitolmetabolisminserumresistanceandtherapeuticimplicationsinvibrioalginolyticus AT xuanweichen functionalproteomicsidentifymannitolmetabolisminserumresistanceandtherapeuticimplicationsinvibrioalginolyticus AT bopeng functionalproteomicsidentifymannitolmetabolisminserumresistanceandtherapeuticimplicationsinvibrioalginolyticus AT bopeng functionalproteomicsidentifymannitolmetabolisminserumresistanceandtherapeuticimplicationsinvibrioalginolyticus |