Patatin-like phospholipase CapV in Escherichia coli - morphological and physiological effects of one amino acid substitution
Abstract In rod-shaped bacteria, morphological plasticity occurs in response to stress, which blocks cell division to promote filamentation. We demonstrate here that overexpression of the patatin-like phospholipase variant CapVQ329R, but not CapV, causes pronounced sulA-independent pyridoxine-inhibi...
| Main Authors: | , , , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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Nature Portfolio
2022-05-01
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| Series: | npj Biofilms and Microbiomes |
| Online Access: | https://doi.org/10.1038/s41522-022-00294-z |
| _version_ | 1818203772248129536 |
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| author | Fengyang Li Lianying Cao Heike Bähre Soo-Kyoung Kim Kristen Schroeder Kristina Jonas Kira Koonce Solomon A. Mekonnen Soumitra Mohanty Fengwu Bai Annelie Brauner Vincent T. Lee Manfred Rohde Ute Römling |
| author_facet | Fengyang Li Lianying Cao Heike Bähre Soo-Kyoung Kim Kristen Schroeder Kristina Jonas Kira Koonce Solomon A. Mekonnen Soumitra Mohanty Fengwu Bai Annelie Brauner Vincent T. Lee Manfred Rohde Ute Römling |
| author_sort | Fengyang Li |
| collection | DOAJ |
| description | Abstract In rod-shaped bacteria, morphological plasticity occurs in response to stress, which blocks cell division to promote filamentation. We demonstrate here that overexpression of the patatin-like phospholipase variant CapVQ329R, but not CapV, causes pronounced sulA-independent pyridoxine-inhibited cell filamentation in the Escherichia coli K-12-derivative MG1655 associated with restriction of flagella production and swimming motility. Conserved amino acids in canonical patatin-like phospholipase A motifs, but not the nucleophilic serine, are required to mediate CapVQ329R phenotypes. Furthermore, CapVQ329R production substantially alters the lipidome and colony morphotype including rdar biofilm formation with modulation of the production of the biofilm activator CsgD, and affects additional bacterial traits such as the efficiency of phage infection and antimicrobial susceptibility. Moreover, genetically diverse commensal and pathogenic E. coli strains and Salmonella typhimurium responded with cell filamentation and modulation in colony morphotype formation to CapVQ329R expression. In conclusion, this work identifies the CapV variant CapVQ329R as a pleiotropic regulator, emphasizes a scaffold function for patatin-like phospholipases, and highlights the impact of the substitution of a single conserved amino acid for protein functionality and alteration of host physiology. |
| first_indexed | 2024-12-12T03:30:39Z |
| format | Article |
| id | doaj.art-f72d9cfa90e54928b2698dae554d3e45 |
| institution | Directory Open Access Journal |
| issn | 2055-5008 |
| language | English |
| last_indexed | 2024-12-12T03:30:39Z |
| publishDate | 2022-05-01 |
| publisher | Nature Portfolio |
| record_format | Article |
| series | npj Biofilms and Microbiomes |
| spelling | doaj.art-f72d9cfa90e54928b2698dae554d3e452022-12-22T00:39:56ZengNature Portfolionpj Biofilms and Microbiomes2055-50082022-05-018111810.1038/s41522-022-00294-zPatatin-like phospholipase CapV in Escherichia coli - morphological and physiological effects of one amino acid substitutionFengyang Li0Lianying Cao1Heike Bähre2Soo-Kyoung Kim3Kristen Schroeder4Kristina Jonas5Kira Koonce6Solomon A. Mekonnen7Soumitra Mohanty8Fengwu Bai9Annelie Brauner10Vincent T. Lee11Manfred Rohde12Ute Römling13Department of Microbiology, Tumor and Cell Biology, Karolinska InstitutetDepartment of Microbiology, Tumor and Cell Biology, Karolinska InstitutetResearch Core Unit Metabolomics, Hannover Medical SchoolDepartment of Cell Biology and Molecular Genetics, University of MarylandScience for Life Laboratory, Department of Molecular Biosciences, The Wenner-Gren Institute, Stockholm UniversityScience for Life Laboratory, Department of Molecular Biosciences, The Wenner-Gren Institute, Stockholm UniversityScience for Life Laboratory, Department of Molecular Biosciences, The Wenner-Gren Institute, Stockholm UniversityDepartment of Cell Biology and Molecular Genetics, University of MarylandDepartment of Microbiology, Tumor and Cell Biology, Division of Clinical Microbiology, Karolinska Institutet and Karolinska University HospitalSchool of Life Sciences and Biotechnology, Shanghai Jiao Tong UniversityDepartment of Microbiology, Tumor and Cell Biology, Division of Clinical Microbiology, Karolinska Institutet and Karolinska University HospitalDepartment of Cell Biology and Molecular Genetics, University of MarylandCentral Facility for Microscopy, Helmholtz Center for Infection ResearchDepartment of Microbiology, Tumor and Cell Biology, Karolinska InstitutetAbstract In rod-shaped bacteria, morphological plasticity occurs in response to stress, which blocks cell division to promote filamentation. We demonstrate here that overexpression of the patatin-like phospholipase variant CapVQ329R, but not CapV, causes pronounced sulA-independent pyridoxine-inhibited cell filamentation in the Escherichia coli K-12-derivative MG1655 associated with restriction of flagella production and swimming motility. Conserved amino acids in canonical patatin-like phospholipase A motifs, but not the nucleophilic serine, are required to mediate CapVQ329R phenotypes. Furthermore, CapVQ329R production substantially alters the lipidome and colony morphotype including rdar biofilm formation with modulation of the production of the biofilm activator CsgD, and affects additional bacterial traits such as the efficiency of phage infection and antimicrobial susceptibility. Moreover, genetically diverse commensal and pathogenic E. coli strains and Salmonella typhimurium responded with cell filamentation and modulation in colony morphotype formation to CapVQ329R expression. In conclusion, this work identifies the CapV variant CapVQ329R as a pleiotropic regulator, emphasizes a scaffold function for patatin-like phospholipases, and highlights the impact of the substitution of a single conserved amino acid for protein functionality and alteration of host physiology.https://doi.org/10.1038/s41522-022-00294-z |
| spellingShingle | Fengyang Li Lianying Cao Heike Bähre Soo-Kyoung Kim Kristen Schroeder Kristina Jonas Kira Koonce Solomon A. Mekonnen Soumitra Mohanty Fengwu Bai Annelie Brauner Vincent T. Lee Manfred Rohde Ute Römling Patatin-like phospholipase CapV in Escherichia coli - morphological and physiological effects of one amino acid substitution npj Biofilms and Microbiomes |
| title | Patatin-like phospholipase CapV in Escherichia coli - morphological and physiological effects of one amino acid substitution |
| title_full | Patatin-like phospholipase CapV in Escherichia coli - morphological and physiological effects of one amino acid substitution |
| title_fullStr | Patatin-like phospholipase CapV in Escherichia coli - morphological and physiological effects of one amino acid substitution |
| title_full_unstemmed | Patatin-like phospholipase CapV in Escherichia coli - morphological and physiological effects of one amino acid substitution |
| title_short | Patatin-like phospholipase CapV in Escherichia coli - morphological and physiological effects of one amino acid substitution |
| title_sort | patatin like phospholipase capv in escherichia coli morphological and physiological effects of one amino acid substitution |
| url | https://doi.org/10.1038/s41522-022-00294-z |
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