The “Jack-of-all-Trades” Flagellum From Salmonella and E. coli Was Horizontally Acquired From an Ancestral β-Proteobacterium
The γ-proteobacteria are a group of diverse bacteria including pathogenic Escherichia, Salmonella, Vibrio, and Pseudomonas species. The majority swim in liquids with polar, sodium-driven flagella and swarm on surfaces with lateral, non-chemotactic flagella. Notable exceptions are the enteric Enterob...
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2021-03-01
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| Series: | Frontiers in Microbiology |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fmicb.2021.643180/full |
| _version_ | 1818738925698547712 |
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| author | Josie L. Ferreira Izaak Coleman Max L. Addison Tobias Zachs Bonnie L. Quigley Kristin Wuichet Morgan Beeby |
| author_facet | Josie L. Ferreira Izaak Coleman Max L. Addison Tobias Zachs Bonnie L. Quigley Kristin Wuichet Morgan Beeby |
| author_sort | Josie L. Ferreira |
| collection | DOAJ |
| description | The γ-proteobacteria are a group of diverse bacteria including pathogenic Escherichia, Salmonella, Vibrio, and Pseudomonas species. The majority swim in liquids with polar, sodium-driven flagella and swarm on surfaces with lateral, non-chemotactic flagella. Notable exceptions are the enteric Enterobacteriaceae such as Salmonella and E. coli. Many of the well-studied Enterobacteriaceae are gut bacteria that both swim and swarm with the same proton-driven peritrichous flagella. How different flagella evolved in closely related lineages, however, has remained unclear. Here, we describe our phylogenetic finding that Enterobacteriaceae flagella are not native polar or lateral γ-proteobacterial flagella but were horizontally acquired from an ancestral β-proteobacterium. Using electron cryo-tomography and subtomogram averaging, we confirmed that Enterobacteriaceae flagellar motors resemble contemporary β-proteobacterial motors and are distinct to the polar and lateral motors of other γ-proteobacteria. Structural comparisons support a model in which γ-proteobacterial motors have specialized, suggesting that acquisition of a β-proteobacterial flagellum may have been beneficial as a general-purpose motor suitable for adjusting to diverse conditions. This acquisition may have played a role in the development of the enteric lifestyle. |
| first_indexed | 2024-12-18T01:16:41Z |
| format | Article |
| id | doaj.art-ceb3de021d844b77ad250fc2235d1cc8 |
| institution | Directory Open Access Journal |
| issn | 1664-302X |
| language | English |
| last_indexed | 2024-12-18T01:16:41Z |
| publishDate | 2021-03-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Microbiology |
| spelling | doaj.art-ceb3de021d844b77ad250fc2235d1cc82022-12-21T21:25:57ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2021-03-011210.3389/fmicb.2021.643180643180The “Jack-of-all-Trades” Flagellum From Salmonella and E. coli Was Horizontally Acquired From an Ancestral β-ProteobacteriumJosie L. Ferreira0Izaak Coleman1Max L. Addison2Tobias Zachs3Bonnie L. Quigley4Kristin Wuichet5Morgan Beeby6Department of Life Sciences, Imperial College London, London, United KingdomDepartment of Life Sciences, Imperial College London, London, United KingdomDepartment of Life Sciences, Imperial College London, London, United KingdomDepartment of Life Sciences, Imperial College London, London, United KingdomDepartment of Life Sciences, Imperial College London, London, United KingdomDepartment of Biomedical Informatics, Vanderbilt University Medical Center, Nashville, TN, United StatesDepartment of Life Sciences, Imperial College London, London, United KingdomThe γ-proteobacteria are a group of diverse bacteria including pathogenic Escherichia, Salmonella, Vibrio, and Pseudomonas species. The majority swim in liquids with polar, sodium-driven flagella and swarm on surfaces with lateral, non-chemotactic flagella. Notable exceptions are the enteric Enterobacteriaceae such as Salmonella and E. coli. Many of the well-studied Enterobacteriaceae are gut bacteria that both swim and swarm with the same proton-driven peritrichous flagella. How different flagella evolved in closely related lineages, however, has remained unclear. Here, we describe our phylogenetic finding that Enterobacteriaceae flagella are not native polar or lateral γ-proteobacterial flagella but were horizontally acquired from an ancestral β-proteobacterium. Using electron cryo-tomography and subtomogram averaging, we confirmed that Enterobacteriaceae flagellar motors resemble contemporary β-proteobacterial motors and are distinct to the polar and lateral motors of other γ-proteobacteria. Structural comparisons support a model in which γ-proteobacterial motors have specialized, suggesting that acquisition of a β-proteobacterial flagellum may have been beneficial as a general-purpose motor suitable for adjusting to diverse conditions. This acquisition may have played a role in the development of the enteric lifestyle.https://www.frontiersin.org/articles/10.3389/fmicb.2021.643180/fullbacterial flagellaelectron cryotomographymolecular evolutionsubtomogram averaginghorizontal gene transfer |
| spellingShingle | Josie L. Ferreira Izaak Coleman Max L. Addison Tobias Zachs Bonnie L. Quigley Kristin Wuichet Morgan Beeby The “Jack-of-all-Trades” Flagellum From Salmonella and E. coli Was Horizontally Acquired From an Ancestral β-Proteobacterium Frontiers in Microbiology bacterial flagella electron cryotomography molecular evolution subtomogram averaging horizontal gene transfer |
| title | The “Jack-of-all-Trades” Flagellum From Salmonella and E. coli Was Horizontally Acquired From an Ancestral β-Proteobacterium |
| title_full | The “Jack-of-all-Trades” Flagellum From Salmonella and E. coli Was Horizontally Acquired From an Ancestral β-Proteobacterium |
| title_fullStr | The “Jack-of-all-Trades” Flagellum From Salmonella and E. coli Was Horizontally Acquired From an Ancestral β-Proteobacterium |
| title_full_unstemmed | The “Jack-of-all-Trades” Flagellum From Salmonella and E. coli Was Horizontally Acquired From an Ancestral β-Proteobacterium |
| title_short | The “Jack-of-all-Trades” Flagellum From Salmonella and E. coli Was Horizontally Acquired From an Ancestral β-Proteobacterium |
| title_sort | jack of all trades flagellum from salmonella and e coli was horizontally acquired from an ancestral β proteobacterium |
| topic | bacterial flagella electron cryotomography molecular evolution subtomogram averaging horizontal gene transfer |
| url | https://www.frontiersin.org/articles/10.3389/fmicb.2021.643180/full |
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