Summary
Bacteria in fluctuating environments must balance the high metabolic costs of motility against risks of bacteriophage predation and immune clearance. While flagellar trade-off mechanisms are well-documented, regulation of type IV pilus (T4P) activity during environmental transitions remains unclear. We show that Pseudomonas aeruginosa uses an energy-dependent idling strategy to synchronize T4P-mediated surface motility with nutrient availability. In nutrient-depleted stationary phase, T4P transcription and protein levels remain constant, pre-assembled machines persist at the cell pole, yet cells produce only sparse, truncated pili that extend and retract slowly. Using a single-cell ATP biosensor, we show that T4P dynamics respond directly to cellular adenylate energy charge. Carbon source addition rapidly elevates intracellular ATP, reactivating pre-assembled T4P within minutes. This bypasses de novo protein synthesis, restoring pilus number, length, and extension/retraction rates. This rapid response drives opportunistic biofilm dispersal but, at the same time, creates an immediate tradeoff: reactivated T4P restore susceptibility to pilus-specific phages upon nutrient upshift. Thus, energetic gating of T4P enables P. aeruginosa to minimize exposure to phages during starvation while remaining poised for rapid reactivation. Importantly, T4P promote resistance to opsonization and phagocytosis by macrophages and neutrophils. Upon nutrient upshift, full T4P activity therefore supports dispersal and host colonization while conferring immune protection, revealing a fundamental dispersal-infection tradeoff at the host- microbe interface in fluctuating environments such as the lung and gut.
Outcomes reported
Bacteria in fluctuating environments must balance the high metabolic costs of motility against risks of bacteriophage predation and immune clearance. While flagellar trade-off mechanisms are well-documented, regulation of type IV pilus (T4P) activity during environmental transitions remains unclear. We show that Pseudomonas aeruginosa uses an energy-dependent idling strategy to synchronize T4P-mediated surface motility with nutrient availability. In nutrient-depleted stationary phase, T4P transcription and protein levels remain constant, pre-assembled machines persist at the cell pole, yet cells produce only sparse, truncated pili that extend and retract slowly. Using a single-cell ATP biosensor, we show that T4P dynamics respond directly to cellular adenylate energy charge. Carbon source addition rapidly elevates intracellular ATP, reactivating pre-assembled T4P within minutes. This bypasses de novo protein synthesis, restoring pilus number, length, and extension/retraction rates. This rapid response drives opportunistic biofilm dispersal but, at the same time, creates an immediate tradeoff: reactivated T4P restore susceptibility to pilus-specific phages upon nutrient upshift. Thus, energetic gating of T4P enables P. aeruginosa to minimize exposure to phages during starvation while remaining poised for rapid reactivation. Importantly, T4P promote resistance to opsonization and phagocytosis by macrophages and neutrophils. Upon nutrient upshift, full T4P activity therefore supports dispersal and host colonization while conferring immune protection, revealing a fundamental dispersal-infection tradeoff at the host- microbe interface in fluctuating environments such as the lung and gut.
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