A tyrosine phosphoregulatory system controls exopolysaccharide biosynthesis and biofilm formation in Vibrio cholerae
Production of an extracellular matrix is essential for biofilm formation, as this matrix both secures and protects the cells it encases. Mechanisms underlying production and assembly of matrices are poorly understood. Vibrio cholerae, relies heavily on biofilm formation for survival, infectivity, an...
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creator | Schwechheimer, Carmen Hebert, Kassidy Tripathi, Sarvind Singh, Praveen K Floyd, Kyle A Brown, Elise R Porcella, Monique E Osorio, Jacqueline Kiblen, Joseph T. M Pagliai, Fernando A Drescher, Knut Rubin, Seth M Yildiz, Fitnat H Salama, Nina R Parsek, Matthew |
description | Production of an extracellular matrix is essential for biofilm formation, as this matrix both secures and protects the cells it encases. Mechanisms underlying production and assembly of matrices are poorly understood. Vibrio cholerae, relies heavily on biofilm formation for survival, infectivity, and transmission. Biofilm formation requires Vibrio polysaccharide (VPS), which is produced by vps gene-products, yet the function of these products remains unknown. Here, we demonstrate that the vps gene-products vpsO and vpsU encode respectively for a tyrosine kinase and a cognate tyrosine phosphatase. Collectively, VpsO and VpsU act as a tyrosine phosphoregulatory system to modulate VPS production. We present structures of VpsU and the kinase domain of VpsO, and we report observed autocatalytic tyrosine phosphorylation of the VpsO C-terminal tail. The position and amount of tyrosine phosphorylation in the VpsO C-terminal tail represses VPS production and biofilm formation through a mechanism involving the modulation of VpsO oligomerization. We found that tyrosine phosphorylation enhances stability of VpsO. Regulation of VpsO phosphorylation by the phosphatase VpsU is vital for maintaining native VPS levels. This study provides new insights into the mechanism and regulation of VPS production and establishes general principles of biofilm matrix production and its inhibition. |
doi_str_mv | 10.1371/journal.ppat.1008745 |
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M ; Pagliai, Fernando A ; Drescher, Knut ; Rubin, Seth M ; Yildiz, Fitnat H ; Salama, Nina R ; Parsek, Matthew</creator><contributor>Parsek, Matthew</contributor><creatorcontrib>Schwechheimer, Carmen ; Hebert, Kassidy ; Tripathi, Sarvind ; Singh, Praveen K ; Floyd, Kyle A ; Brown, Elise R ; Porcella, Monique E ; Osorio, Jacqueline ; Kiblen, Joseph T. M ; Pagliai, Fernando A ; Drescher, Knut ; Rubin, Seth M ; Yildiz, Fitnat H ; Salama, Nina R ; Parsek, Matthew ; Argonne National Lab. (ANL), Argonne, IL (United States). Advanced Photon Source (APS) ; Parsek, Matthew</creatorcontrib><description>Production of an extracellular matrix is essential for biofilm formation, as this matrix both secures and protects the cells it encases. Mechanisms underlying production and assembly of matrices are poorly understood. Vibrio cholerae, relies heavily on biofilm formation for survival, infectivity, and transmission. Biofilm formation requires Vibrio polysaccharide (VPS), which is produced by vps gene-products, yet the function of these products remains unknown. Here, we demonstrate that the vps gene-products vpsO and vpsU encode respectively for a tyrosine kinase and a cognate tyrosine phosphatase. Collectively, VpsO and VpsU act as a tyrosine phosphoregulatory system to modulate VPS production. We present structures of VpsU and the kinase domain of VpsO, and we report observed autocatalytic tyrosine phosphorylation of the VpsO C-terminal tail. The position and amount of tyrosine phosphorylation in the VpsO C-terminal tail represses VPS production and biofilm formation through a mechanism involving the modulation of VpsO oligomerization. We found that tyrosine phosphorylation enhances stability of VpsO. Regulation of VpsO phosphorylation by the phosphatase VpsU is vital for maintaining native VPS levels. This study provides new insights into the mechanism and regulation of VPS production and establishes general principles of biofilm matrix production and its inhibition.</description><identifier>ISSN: 1553-7374</identifier><identifier>ISSN: 1553-7366</identifier><identifier>EISSN: 1553-7374</identifier><identifier>DOI: 10.1371/journal.ppat.1008745</identifier><identifier>PMID: 32841296</identifier><language>eng</language><publisher>San Francisco: Public Library of Science</publisher><subject>Amino acids ; Antibiotics ; Bacteria ; BASIC BIOLOGICAL SCIENCES ; Biochemistry ; Biofilms ; Biology and Life Sciences ; Biosynthesis ; Exopolysaccharides ; Extracellular matrix ; Funding ; Genes ; Genetic aspects ; Genetic regulation ; Genotypes ; Growth ; Infectivity ; Kinases ; Medicine and Health Sciences ; Microbial mats ; Mutation ; Observations ; Oligomerization ; Phosphatase ; Phosphorylation ; Physical Sciences ; Polysaccharides ; Properties ; Protein-tyrosine kinase ; Protein-tyrosine-phosphatase ; Proteins ; Supervision ; Toxicology ; Tyrosine ; Vibrio cholerae ; Waterborne diseases</subject><ispartof>PLoS pathogens, 2020-08, Vol.16 (8), p.e1008745</ispartof><rights>COPYRIGHT 2020 Public Library of Science</rights><rights>2020 Schwechheimer et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. 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Vibrio cholerae, relies heavily on biofilm formation for survival, infectivity, and transmission. Biofilm formation requires Vibrio polysaccharide (VPS), which is produced by vps gene-products, yet the function of these products remains unknown. Here, we demonstrate that the vps gene-products vpsO and vpsU encode respectively for a tyrosine kinase and a cognate tyrosine phosphatase. Collectively, VpsO and VpsU act as a tyrosine phosphoregulatory system to modulate VPS production. We present structures of VpsU and the kinase domain of VpsO, and we report observed autocatalytic tyrosine phosphorylation of the VpsO C-terminal tail. The position and amount of tyrosine phosphorylation in the VpsO C-terminal tail represses VPS production and biofilm formation through a mechanism involving the modulation of VpsO oligomerization. We found that tyrosine phosphorylation enhances stability of VpsO. Regulation of VpsO phosphorylation by the phosphatase VpsU is vital for maintaining native VPS levels. This study provides new insights into the mechanism and regulation of VPS production and establishes general principles of biofilm matrix production and its inhibition.</abstract><cop>San Francisco</cop><pub>Public Library of Science</pub><pmid>32841296</pmid><doi>10.1371/journal.ppat.1008745</doi><orcidid>https://orcid.org/0000-0001-7674-1997</orcidid><orcidid>https://orcid.org/0000-0002-0254-7400</orcidid><orcidid>https://orcid.org/0000-0003-3261-7999</orcidid><orcidid>https://orcid.org/0000-0002-6959-0577</orcidid><orcidid>https://orcid.org/0000-0002-6943-1760</orcidid><orcidid>https://orcid.org/0000-0002-7340-2444</orcidid><orcidid>https://orcid.org/0000-0002-6384-7167</orcidid><orcidid>https://orcid.org/0000-0002-0434-4594</orcidid><orcidid>https://orcid.org/0000000263847167</orcidid><orcidid>https://orcid.org/0000000204344594</orcidid><orcidid>https://orcid.org/0000000176741997</orcidid><orcidid>https://orcid.org/0000000273402444</orcidid><orcidid>https://orcid.org/0000000269431760</orcidid><orcidid>https://orcid.org/0000000332617999</orcidid><orcidid>https://orcid.org/0000000269590577</orcidid><orcidid>https://orcid.org/0000000202547400</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Amino acids Antibiotics Bacteria BASIC BIOLOGICAL SCIENCES Biochemistry Biofilms Biology and Life Sciences Biosynthesis Exopolysaccharides Extracellular matrix Funding Genes Genetic aspects Genetic regulation Genotypes Growth Infectivity Kinases Medicine and Health Sciences Microbial mats Mutation Observations Oligomerization Phosphatase Phosphorylation Physical Sciences Polysaccharides Properties Protein-tyrosine kinase Protein-tyrosine-phosphatase Proteins Supervision Toxicology Tyrosine Vibrio cholerae Waterborne diseases |
title | A tyrosine phosphoregulatory system controls exopolysaccharide biosynthesis and biofilm formation in Vibrio cholerae |
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