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Heat-shock proteases promote survival of Pseudomonas aeruginosa during growth arrest
Wednesday, 2020/02/26 | 07:23:04

David W. Basta, David Angeles-Albores, Melanie A. Spero, John A. Ciemniecki, and Dianne K. Newman

PNAS February 25, 2020 117 (8) 4358-4367

Significance

This study reveals that protein degradation plays a major role in the survival of the opportunistic bacterial pathogen Pseudomonas aeruginosa. Loss of multiple proteases, better known for their roles in proteostasis in response to stresses such as heat shock, accelerates cell death during growth arrest. This finding, coupled to the fact that the accumulation of misfolded and aggregated proteins in aging in eukaryotic cells is well appreciated to contribute to cellular damage and senescence, suggests that a general role for proteases in preserving bacterial proteostasis during aging has been overlooked. Our findings have implications for the study and treatment of infectious disease and highlight potentially conserved functions for proteases in combatting aging from bacteria to humans.

Abstract

When nutrients in their environment are exhausted, bacterial cells become arrested for growth. During these periods, a primary challenge is maintaining cellular integrity with a reduced capacity for renewal or repair. Here, we show that the heat-shock protease FtsH is generally required for growth arrest survival of Pseudomonas aeruginosa, and that this requirement is independent of a role in regulating lipopolysaccharide synthesis, as has been suggested for Escherichia coli. We find that ftsH interacts with diverse genes during growth and overlaps functionally with the other heat-shock protease-encoding genes hslVUlon, and clpXP to promote survival during growth arrest. Systematic deletion of the heat-shock protease-encoding genes reveals that the proteases function hierarchically during growth arrest, with FtsH and ClpXP having primary, nonredundant roles, and HslVU and Lon deploying a secondary response to aging stress. This hierarchy is partially conserved during growth at high temperature and alkaline pH, suggesting that heat, pH, and growth arrest effectively impose a similar type of proteostatic stress at the cellular level. In support of this inference, heat and growth arrest act synergistically to kill cells, and protein aggregation appears to occur more rapidly in protease mutants during growth arrest and correlates with the onset of cell death. Our findings suggest that protein aggregation is a major driver of aging and cell death during growth arrest, and that coordinated activity of the heat-shock response is required to ensure ongoing protein quality control in the absence of growth.

 

See https://www.pnas.org/content/117/8/4358

Figure 1: FtsH maintains cell integrity during growth arrest. Loss of ftsH exacerbates cell death during stationary phase (A) and carbon starvation (B). Viability was below the limit of detection (∼3 × 102 CFU mL−1) for ΔftsH at 60 h in A. Representative data from at least three independent experiments are shown in A and the averages and SD of biological replicates are shown in B (n = 3). (C) Characteristic morphology of ΔftsH cells after 24 h of carbon starvation. The white arrow indicates a “detached” inner membrane and the black arrow indicates a “ghost cell.” (D) Quantification of the cellular morphologies described in C. A minimum of 300 cells were counted for each strain. (E) OM staining with FM 4-64 and cytoplasmic expression of GFP confirms that detachment occurs between the IM and OM.

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