Development of the Pseudomonas aeruginosa mushroom morphology and cavity formation by iron-starvation: A mathematical modeling study

• Published in: Journal of theoretical biology 2012-09, Vol.308, p.68-78
• Main Authors: Miller, James K., Badawy, Hope T., Clemons, Curtis, Kreider, K.L., Wilber, Pat, Milsted, Amy, Young, Gerald
• Format: Article
• Language: English
• Subjects: bacteria; Biofilm; Biofilms - drug effects; Biofilms - growth & development; Computer Simulation; Continuum modeling; friction; Iron Deficiencies; Iron signaling; mathematical models; Models, Biological; mushrooms; Oligopeptides - pharmacology; Pseudomonas aeruginosa; Pseudomonas aeruginosa - drug effects; Pseudomonas aeruginosa - growth & development; Pseudomonas aeruginosa - physiology; Signal Transduction - drug effects; starvation
• ISSN: 0022-5193; 1095-8541
• DOI: 10.1016/j.jtbi.2012.05.029

We present a mathematical model of mushroom-like architecture and cavity formation in Pseudomonas aeruginosa biofilms. We demonstrate that a proposed disparity in internal friction between the stalk and cap extracellular polymeric substances (EPS) leads to spatial variation in volumetric expansion sufficient to produce the mushroom morphology. The capability of diffusible signals to induce the formation of a fluid-filled cavity within the cap is then investigated. We assume that conversion of bacteria to the planktonic state within the cap occurs in response to the accumulation or depletion of some signal molecule. We (a) show that neither simple nutrient starvation nor signal production by one or more subpopulations of bacteria is sufficient to trigger localized cavity formation. We then (b) demonstrate various hypothetical scenarios that could result in localized cavity formation. Finally, we (c) model iron availability as a detachment signal and show simulation results demonstrating cavity formation by iron starvation. We conclude that iron availability is a plausible mechanism by which fluid-filled cavities form in the cap region of mushroom-like structures. ► We model mushroom morphology and cavity formation in Pseudomonas aeruginosa biofilms. ► Disparity in stiffness between cap and stalk may be responsible for mushroom morphology. ► Simple nutrient starvation or signal accumulation is unlikely causes of cavities. ► Iron starvation is a plausible cause for cavity formation.