Communication across the bacterial cell envelope depends on the size of the periplasm.
The cell envelope of gram-negative bacteria, a structure comprising an outer (OM) and an inner (IM) membrane, is essential for life. The OM and the IM are separated by the periplasm, a compartment that contains the peptidoglycan. The OM is tethered to the peptidoglycan via the lipoprotein, Lpp. Howe...
| Main Authors: | , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Public Library of Science (PLoS)
2017-12-01
|
| Series: | PLoS Biology |
| Online Access: | http://europepmc.org/articles/PMC5736177?pdf=render |
| _version_ | 1818883928367300608 |
|---|---|
| author | Abir T Asmar Josie L Ferreira Eli J Cohen Seung-Hyun Cho Morgan Beeby Kelly T Hughes Jean-François Collet |
| author_facet | Abir T Asmar Josie L Ferreira Eli J Cohen Seung-Hyun Cho Morgan Beeby Kelly T Hughes Jean-François Collet |
| author_sort | Abir T Asmar |
| collection | DOAJ |
| description | The cell envelope of gram-negative bacteria, a structure comprising an outer (OM) and an inner (IM) membrane, is essential for life. The OM and the IM are separated by the periplasm, a compartment that contains the peptidoglycan. The OM is tethered to the peptidoglycan via the lipoprotein, Lpp. However, the importance of the envelope's multilayered architecture remains unknown. Here, when we removed physical coupling between the OM and the peptidoglycan, cells lost the ability to sense defects in envelope integrity. Further experiments revealed that the critical parameter for the transmission of stress signals from the envelope to the cytoplasm, where cellular behaviour is controlled, is the IM-to-OM distance. Augmenting this distance by increasing the length of the lipoprotein Lpp destroyed signalling, whereas simultaneously increasing the length of the stress-sensing lipoprotein RcsF restored signalling. Our results demonstrate the physiological importance of the size of the periplasm. They also reveal that strict control over the IM-to-OM distance is required for effective envelope surveillance and protection, suggesting that cellular architecture and the structure of transenvelope protein complexes have been evolutionarily co-optimised for correct function. Similar strategies are likely at play in cellular compartments surrounded by 2 concentric membranes, such as chloroplasts and mitochondria. |
| first_indexed | 2024-12-19T15:41:26Z |
| format | Article |
| id | doaj.art-763a322153d944db878381a4397822de |
| institution | Directory Open Access Journal |
| issn | 1544-9173 1545-7885 |
| language | English |
| last_indexed | 2024-12-19T15:41:26Z |
| publishDate | 2017-12-01 |
| publisher | Public Library of Science (PLoS) |
| record_format | Article |
| series | PLoS Biology |
| spelling | doaj.art-763a322153d944db878381a4397822de2022-12-21T20:15:27ZengPublic Library of Science (PLoS)PLoS Biology1544-91731545-78852017-12-011512e200430310.1371/journal.pbio.2004303Communication across the bacterial cell envelope depends on the size of the periplasm.Abir T AsmarJosie L FerreiraEli J CohenSeung-Hyun ChoMorgan BeebyKelly T HughesJean-François ColletThe cell envelope of gram-negative bacteria, a structure comprising an outer (OM) and an inner (IM) membrane, is essential for life. The OM and the IM are separated by the periplasm, a compartment that contains the peptidoglycan. The OM is tethered to the peptidoglycan via the lipoprotein, Lpp. However, the importance of the envelope's multilayered architecture remains unknown. Here, when we removed physical coupling between the OM and the peptidoglycan, cells lost the ability to sense defects in envelope integrity. Further experiments revealed that the critical parameter for the transmission of stress signals from the envelope to the cytoplasm, where cellular behaviour is controlled, is the IM-to-OM distance. Augmenting this distance by increasing the length of the lipoprotein Lpp destroyed signalling, whereas simultaneously increasing the length of the stress-sensing lipoprotein RcsF restored signalling. Our results demonstrate the physiological importance of the size of the periplasm. They also reveal that strict control over the IM-to-OM distance is required for effective envelope surveillance and protection, suggesting that cellular architecture and the structure of transenvelope protein complexes have been evolutionarily co-optimised for correct function. Similar strategies are likely at play in cellular compartments surrounded by 2 concentric membranes, such as chloroplasts and mitochondria.http://europepmc.org/articles/PMC5736177?pdf=render |
| spellingShingle | Abir T Asmar Josie L Ferreira Eli J Cohen Seung-Hyun Cho Morgan Beeby Kelly T Hughes Jean-François Collet Communication across the bacterial cell envelope depends on the size of the periplasm. PLoS Biology |
| title | Communication across the bacterial cell envelope depends on the size of the periplasm. |
| title_full | Communication across the bacterial cell envelope depends on the size of the periplasm. |
| title_fullStr | Communication across the bacterial cell envelope depends on the size of the periplasm. |
| title_full_unstemmed | Communication across the bacterial cell envelope depends on the size of the periplasm. |
| title_short | Communication across the bacterial cell envelope depends on the size of the periplasm. |
| title_sort | communication across the bacterial cell envelope depends on the size of the periplasm |
| url | http://europepmc.org/articles/PMC5736177?pdf=render |
| work_keys_str_mv | AT abirtasmar communicationacrossthebacterialcellenvelopedependsonthesizeoftheperiplasm AT josielferreira communicationacrossthebacterialcellenvelopedependsonthesizeoftheperiplasm AT elijcohen communicationacrossthebacterialcellenvelopedependsonthesizeoftheperiplasm AT seunghyuncho communicationacrossthebacterialcellenvelopedependsonthesizeoftheperiplasm AT morganbeeby communicationacrossthebacterialcellenvelopedependsonthesizeoftheperiplasm AT kellythughes communicationacrossthebacterialcellenvelopedependsonthesizeoftheperiplasm AT jeanfrancoiscollet communicationacrossthebacterialcellenvelopedependsonthesizeoftheperiplasm |