Communication across the bacterial cell envelope depends on the size of the periplasm

Citations Over TimeTop 10% of 2017 papers

Abstract

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.

Related Papers

• → Lipopolysaccharides: Regulated Biosynthesis and Structural Diversity(2023)7 cited
• → PapA , a peptidoglycan‐associated protein, interacts with OmpC and maintains cell envelope integrity(2020)5 cited
• → Multilayered Distribution of Peptidoglycan in the Periplasmic Space of Escherichia coli(1989)51 cited
• → The Bacterial Cell Envelope(2010)3,573 cited
• → The Structural and Physiological Roles of the Layers of the Gram-Negative Bacterial Envelope(2001)