Distinct regions of H. pylori’s bactofilin CcmA regulate protein–protein interactions to control helical cell shape
The helical shape of Helicobacter pylori cells promotes robust stomach colonization; however, how the helical shape of H. pylori cells is determined is unresolved. Previous work identified helical-cell-shape-promoting protein complexes containing a peptidoglycan-hydrolase (Csd1), a peptidoglycan pre...
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| Format: | Article |
| Language: | English |
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eLife Sciences Publications Ltd
2022-09-01
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| Series: | eLife |
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| Online Access: | https://elifesciences.org/articles/80111 |
| _version_ | 1798001471150620672 |
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| author | Sophie R Sichel Benjamin P Bratton Nina R Salama |
| author_facet | Sophie R Sichel Benjamin P Bratton Nina R Salama |
| author_sort | Sophie R Sichel |
| collection | DOAJ |
| description | The helical shape of Helicobacter pylori cells promotes robust stomach colonization; however, how the helical shape of H. pylori cells is determined is unresolved. Previous work identified helical-cell-shape-promoting protein complexes containing a peptidoglycan-hydrolase (Csd1), a peptidoglycan precursor synthesis enzyme (MurF), a non-enzymatic homolog of Csd1 (Csd2), non-enzymatic transmembrane proteins (Csd5 and Csd7), and a bactofilin (CcmA). Bactofilins are highly conserved, spontaneously polymerizing cytoskeletal bacterial proteins. We sought to understand CcmA’s function in generating the helical shape of H. pylori cells. Using CcmA deletion analysis, in vitro polymerization, and in vivo co-immunoprecipitation experiments, we identified that the bactofilin domain and N-terminal region of CcmA are required for helical cell shape and the bactofilin domain of CcmA is sufficient for polymerization and interactions with Csd5 and Csd7. We also found that CcmA’s N-terminal region inhibits interaction with Csd7. Deleting the N-terminal region of CcmA increases CcmA-Csd7 interactions and destabilizes the peptidoglycan-hydrolase Csd1. Using super-resolution microscopy, we found that Csd5 recruits CcmA to the cell envelope and promotes CcmA enrichment at the major helical axis. Thus, CcmA helps organize cell-shape-determining proteins and peptidoglycan synthesis machinery to coordinate cell wall modification and synthesis, promoting the curvature required to build a helical cell. |
| first_indexed | 2024-04-11T11:36:46Z |
| format | Article |
| id | doaj.art-675f46ae859541f2a29b45c047249cf4 |
| institution | Directory Open Access Journal |
| issn | 2050-084X |
| language | English |
| last_indexed | 2024-04-11T11:36:46Z |
| publishDate | 2022-09-01 |
| publisher | eLife Sciences Publications Ltd |
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| series | eLife |
| spelling | doaj.art-675f46ae859541f2a29b45c047249cf42022-12-22T04:25:56ZengeLife Sciences Publications LtdeLife2050-084X2022-09-011110.7554/eLife.80111Distinct regions of H. pylori’s bactofilin CcmA regulate protein–protein interactions to control helical cell shapeSophie R Sichel0https://orcid.org/0000-0001-5079-189XBenjamin P Bratton1https://orcid.org/0000-0003-1128-2560Nina R Salama2https://orcid.org/0000-0003-2762-1424Division of Human Biology, Fred Hutchinson Cancer Center, Seattle, United States; Molecular Medicine and Mechanisms of Disease Graduate Program, University of Washington, Seattle, United StatesDepartment of Pathology, Microbiology and Immunology, Vanderbilt University Medical Center, Nashville, United States; Vanderbilt Institute for Infection, Immunology and Inflammation, Nashville, United StatesDivision of Human Biology, Fred Hutchinson Cancer Center, Seattle, United StatesThe helical shape of Helicobacter pylori cells promotes robust stomach colonization; however, how the helical shape of H. pylori cells is determined is unresolved. Previous work identified helical-cell-shape-promoting protein complexes containing a peptidoglycan-hydrolase (Csd1), a peptidoglycan precursor synthesis enzyme (MurF), a non-enzymatic homolog of Csd1 (Csd2), non-enzymatic transmembrane proteins (Csd5 and Csd7), and a bactofilin (CcmA). Bactofilins are highly conserved, spontaneously polymerizing cytoskeletal bacterial proteins. We sought to understand CcmA’s function in generating the helical shape of H. pylori cells. Using CcmA deletion analysis, in vitro polymerization, and in vivo co-immunoprecipitation experiments, we identified that the bactofilin domain and N-terminal region of CcmA are required for helical cell shape and the bactofilin domain of CcmA is sufficient for polymerization and interactions with Csd5 and Csd7. We also found that CcmA’s N-terminal region inhibits interaction with Csd7. Deleting the N-terminal region of CcmA increases CcmA-Csd7 interactions and destabilizes the peptidoglycan-hydrolase Csd1. Using super-resolution microscopy, we found that Csd5 recruits CcmA to the cell envelope and promotes CcmA enrichment at the major helical axis. Thus, CcmA helps organize cell-shape-determining proteins and peptidoglycan synthesis machinery to coordinate cell wall modification and synthesis, promoting the curvature required to build a helical cell.https://elifesciences.org/articles/80111Helicobacter pyloricell shapebactofilincytoskeleton |
| spellingShingle | Sophie R Sichel Benjamin P Bratton Nina R Salama Distinct regions of H. pylori’s bactofilin CcmA regulate protein–protein interactions to control helical cell shape eLife Helicobacter pylori cell shape bactofilin cytoskeleton |
| title | Distinct regions of H. pylori’s bactofilin CcmA regulate protein–protein interactions to control helical cell shape |
| title_full | Distinct regions of H. pylori’s bactofilin CcmA regulate protein–protein interactions to control helical cell shape |
| title_fullStr | Distinct regions of H. pylori’s bactofilin CcmA regulate protein–protein interactions to control helical cell shape |
| title_full_unstemmed | Distinct regions of H. pylori’s bactofilin CcmA regulate protein–protein interactions to control helical cell shape |
| title_short | Distinct regions of H. pylori’s bactofilin CcmA regulate protein–protein interactions to control helical cell shape |
| title_sort | distinct regions of h pylori s bactofilin ccma regulate protein protein interactions to control helical cell shape |
| topic | Helicobacter pylori cell shape bactofilin cytoskeleton |
| url | https://elifesciences.org/articles/80111 |
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