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Comparative Phenotypic, Proteomic, and Phosphoproteomic Analysis Reveals Different Roles of Serine/Threonine Phosphatase and Kinase in the Growth, Cell Division, and Pathogenicity of Streptococcus suis

Eukaryote-like serine/threonine kinases (STKs) and cognate phosphatases (STPs) comprise an important regulatory system in many bacterial pathogens. The complexity of this regulatory system has not been fully understood due to the presence of multiple STKs/STPs in many bacteria and their multiple sub...

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Autores principales: Hu, Qiao, Yao, Lun, Liao, Xia, Zhang, Liang-Sheng, Li, Hao-Tian, Li, Ting-Ting, Jiang, Qing-Gen, Tan, Mei-Fang, Li, Lu, Draheim, Roger R., Huang, Qi, Zhou, Rui
Formato: Online Artículo Texto
Lenguaje:English
Publicado: MDPI 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8707513/
https://www.ncbi.nlm.nih.gov/pubmed/34946045
http://dx.doi.org/10.3390/microorganisms9122442
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author Hu, Qiao
Yao, Lun
Liao, Xia
Zhang, Liang-Sheng
Li, Hao-Tian
Li, Ting-Ting
Jiang, Qing-Gen
Tan, Mei-Fang
Li, Lu
Draheim, Roger R.
Huang, Qi
Zhou, Rui
author_facet Hu, Qiao
Yao, Lun
Liao, Xia
Zhang, Liang-Sheng
Li, Hao-Tian
Li, Ting-Ting
Jiang, Qing-Gen
Tan, Mei-Fang
Li, Lu
Draheim, Roger R.
Huang, Qi
Zhou, Rui
author_sort Hu, Qiao
collection PubMed
description Eukaryote-like serine/threonine kinases (STKs) and cognate phosphatases (STPs) comprise an important regulatory system in many bacterial pathogens. The complexity of this regulatory system has not been fully understood due to the presence of multiple STKs/STPs in many bacteria and their multiple substrates involved in many different physiological and pathogenetic processes. Streptococci are the best materials for the study due to a single copy of the gene encoding STK and its cognate STP. Although several studies have been done to investigate the roles of STK and STP in zoonotic Streptococcus suis, respectively, few studies were performed on the coordinated regulatory roles of this system. In this study, we carried out a systemic study on STK/STP in S. suis by using a comparative phenotypic, proteomic, and phosphoproteomic analysis. Mouse infection assays revealed that STK played a much more important role in S. suis pathogenesis than STP. The ∆stk and ∆stp∆stk strains, but not ∆stp, showed severe growth retardation. Moreover, both ∆stp and ∆stk strains displayed defects in cell division, but they were abnormal in different ways. The comparative proteomics and phosphoproteomics revealed that deletion of stk or stp had a significant influence on protein expression. Interestingly, more virulence factors were found to be downregulated in ∆stk than ∆stp. In ∆stk strain, a substantial number of the proteins with a reduced phosphorylation level were involved in cell division, energy metabolism, and protein translation. However, only a few proteins showed increased phosphorylation in ∆stp, which also included some proteins related to cell division. Collectively, our results show that both STP and STK are critical regulatory proteins for S. suis and that STK seems to play more important roles in growth, cell division, and pathogenesis.
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spelling pubmed-87075132021-12-25 Comparative Phenotypic, Proteomic, and Phosphoproteomic Analysis Reveals Different Roles of Serine/Threonine Phosphatase and Kinase in the Growth, Cell Division, and Pathogenicity of Streptococcus suis Hu, Qiao Yao, Lun Liao, Xia Zhang, Liang-Sheng Li, Hao-Tian Li, Ting-Ting Jiang, Qing-Gen Tan, Mei-Fang Li, Lu Draheim, Roger R. Huang, Qi Zhou, Rui Microorganisms Article Eukaryote-like serine/threonine kinases (STKs) and cognate phosphatases (STPs) comprise an important regulatory system in many bacterial pathogens. The complexity of this regulatory system has not been fully understood due to the presence of multiple STKs/STPs in many bacteria and their multiple substrates involved in many different physiological and pathogenetic processes. Streptococci are the best materials for the study due to a single copy of the gene encoding STK and its cognate STP. Although several studies have been done to investigate the roles of STK and STP in zoonotic Streptococcus suis, respectively, few studies were performed on the coordinated regulatory roles of this system. In this study, we carried out a systemic study on STK/STP in S. suis by using a comparative phenotypic, proteomic, and phosphoproteomic analysis. Mouse infection assays revealed that STK played a much more important role in S. suis pathogenesis than STP. The ∆stk and ∆stp∆stk strains, but not ∆stp, showed severe growth retardation. Moreover, both ∆stp and ∆stk strains displayed defects in cell division, but they were abnormal in different ways. The comparative proteomics and phosphoproteomics revealed that deletion of stk or stp had a significant influence on protein expression. Interestingly, more virulence factors were found to be downregulated in ∆stk than ∆stp. In ∆stk strain, a substantial number of the proteins with a reduced phosphorylation level were involved in cell division, energy metabolism, and protein translation. However, only a few proteins showed increased phosphorylation in ∆stp, which also included some proteins related to cell division. Collectively, our results show that both STP and STK are critical regulatory proteins for S. suis and that STK seems to play more important roles in growth, cell division, and pathogenesis. MDPI 2021-11-26 /pmc/articles/PMC8707513/ /pubmed/34946045 http://dx.doi.org/10.3390/microorganisms9122442 Text en © 2021 by the authors. https://creativecommons.org/licenses/by/4.0/Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
spellingShingle Article
Hu, Qiao
Yao, Lun
Liao, Xia
Zhang, Liang-Sheng
Li, Hao-Tian
Li, Ting-Ting
Jiang, Qing-Gen
Tan, Mei-Fang
Li, Lu
Draheim, Roger R.
Huang, Qi
Zhou, Rui
Comparative Phenotypic, Proteomic, and Phosphoproteomic Analysis Reveals Different Roles of Serine/Threonine Phosphatase and Kinase in the Growth, Cell Division, and Pathogenicity of Streptococcus suis
title Comparative Phenotypic, Proteomic, and Phosphoproteomic Analysis Reveals Different Roles of Serine/Threonine Phosphatase and Kinase in the Growth, Cell Division, and Pathogenicity of Streptococcus suis
title_full Comparative Phenotypic, Proteomic, and Phosphoproteomic Analysis Reveals Different Roles of Serine/Threonine Phosphatase and Kinase in the Growth, Cell Division, and Pathogenicity of Streptococcus suis
title_fullStr Comparative Phenotypic, Proteomic, and Phosphoproteomic Analysis Reveals Different Roles of Serine/Threonine Phosphatase and Kinase in the Growth, Cell Division, and Pathogenicity of Streptococcus suis
title_full_unstemmed Comparative Phenotypic, Proteomic, and Phosphoproteomic Analysis Reveals Different Roles of Serine/Threonine Phosphatase and Kinase in the Growth, Cell Division, and Pathogenicity of Streptococcus suis
title_short Comparative Phenotypic, Proteomic, and Phosphoproteomic Analysis Reveals Different Roles of Serine/Threonine Phosphatase and Kinase in the Growth, Cell Division, and Pathogenicity of Streptococcus suis
title_sort comparative phenotypic, proteomic, and phosphoproteomic analysis reveals different roles of serine/threonine phosphatase and kinase in the growth, cell division, and pathogenicity of streptococcus suis
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8707513/
https://www.ncbi.nlm.nih.gov/pubmed/34946045
http://dx.doi.org/10.3390/microorganisms9122442
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