Incorporation of collagen into Pseudomonas aeruginosa, Staphylococcus aureus, and Burkholderia pseudomallei biofilms enhances their elasticity and resistance against phagocytic clearance

Abstract

Biofilms are communities of microbes embedded in a matrix of extracellular polymeric substances (EPS) and other components such as proteins. Matrix components can be produced by the microorganisms themselves but can also originate from the environment and then be incorporated into the biofilm. For example, we and our collaborators have recently shown that collagen, a host-produced protein that is abundant in many different infection sites, can be taken up into the matrices of Pseudomonas aeruginosa biofilms, altering biofilm mechanics. In an infection, the biofilm matrix protects bacteria from clearance by the immune system, and some of that protection likely arises from the mechanical properties of the biofilm. P. aeruginosa, Staphylococcus aureus, and Burkholderia pseudomallei are human pathogens notable for forming biofilms in vitro and in vivo in tissues rich in collagen such as lung and skin. Here, we show that the incorporation of Type I collagen into P. aeruginosa, S. aureus, and B. pseudomallei biofilms significantly enhances biofilm elasticity and hinders phagocytosis of biofilm bacteria by human neutrophils. Additionally, enzymatic degradation of collagen using collagenase reverses these effects, increasing biofilm susceptibility to neutrophils. Our findings suggest that host materials play significant roles in stabilizing biofilms and may present promising targets for therapeutic interventions.