The phage shock protein (PSP) envelope stress response: discovery of novel partners and evolutionary history

• DOI: 10.1128/msystems.00847-23
• Publication Date: 2024-05-29T13:01:46Z
• Authors: Janani Ravi; Vivek Anantharaman; Samuel Zorn Chen; Evan Pierce Brenner; Pratik Datta; L. Aravind; Maria Laura Gennaro
• Keywords: Cell envelope; Comparative Genomics; ESCRT; Three-domain system; Chaperone (clinical)

Bacterial phage shock protein (PSP) systems stabilize the bacterial cell membrane and protect against envelope stress. These have been associated with virulence, but despite their critical roles, PSP components are not well characterized outside proteobacteria. Using comparative genomics sequence-structure-function analyses, we systematically identified analyzed homologs, phyletic patterns, domain architectures, gene neighborhoods. This approach underscored evolutionary significance of system, revealing that its core PspA (Snf7 in ESCRT bacteria) was present last universal common ancestor this ancestral functionality has since diversified into multiple novel, distinct across life. Several novel partners system were identified: (i) Toastrack domain, likely facilitating assembly sub-membrane stress-sensing signaling complexes, (ii) newly defined HTH-associated α-helical domain-PadR-like transcriptional regulator pair (iii) independent associations ATPase, CesT/Tir-like chaperone, Band-7 domains proteins thought to mediate dynamics. Our work also uncovered links between other domains, such as variants SHOCT-like suggesting roles assembling membrane-associated complexes disparate biochemical functions. Results available at our interactive web app, https://jravilab.org/psp.IMPORTANCEPhage virulence-associated, stress-protective systems. They mostly Proteobacteria Firmicutes. We now show a minimal evolved functional contexts. Recognizing conservation evolution phyla contributes understanding stress response mechanisms prokaryotes. Moreover, discovered modularity will prompt new studies lineage-specific structures, lifestyles, adaptation mechanisms. Finally, results validate use architecture genetic context for discovery genomics.