Abstract
Staphylococcus aureus is a human pathogen known for its capacity to shift between the planktonic and biofilm lifestyles. In vivo, the antimicrobial immune response is characterized by the recruitment of inflammatory phagocytes, namely polymorphonuclear neutrophils (PMNs) and monocytes/macrophages. Immune responses to planktonic bacteria have been extensively studied, but many questions remain about how biofilms can modulate inflammatory responses and cause recurrent infections in live vertebrates. Thus, the use of biologically sound experimental models is essential to study the specific immune signatures elicited by biofilms. Here, a mouse ear pinna model of infection was used to compare early innate immune responses toward S. aureus planktonic or biofilm bacteria. Flow cytometry and cytokine assays were carried out to study the inflammatory responses in infected tissues. These data were complemented with intravital confocal imaging analyses, allowing the real-time observation of the dynamic interactions between EGFP + phagocytes and bacteria in the ear pinna tissue of LysM-EGFP transgenic mice. Both bacterial forms induced an early and considerable recruitment of phagocytes in the ear tissue, associated with a predominantly pro-inflammatory cytokine profile. The inflammatory response was mostly composed of PMNs in the skin and the auricular lymph node. However, the kinetics of PMN recruitment were different between the 2 forms in the first 2 days post-infection (pi). Two hours pi, biofilm inocula recruited more PMNs than planktonic bacteria, but with decreased motility parameters and capacity to emit pseudopods. Inversely, biofilm inocula recruited less PMNs 2 days pi, but with an “over-activated” status, illustrated by an increased phagocytic activity, CD11b level of expression and ROS production. Thus, the mouse ear pinna model allowed us to reveal specific differences in the dynamics of recruitment and functional properties of phagocytes against biofilms. These differences would influence the specific adaptive immune responses to biofilms elicited in the lymphoid tissues.
Highlights
Staphylococcus aureus (S. aureus) is a Gram-positive commensal bacterium that is a leading cause of various invasive infections from soft skin tissue colonization to infections on implanted medical devices such as prosthetic joints
This sharp decrease seemed more pronounced in mice inoculated with planktonic bacteria, no significant difference was observed between the two forms
As the infection outcome is conditioned in the first few days following host-bacteria contact, we sought out to highlight the very early impacts of S. aureus biofilms on the main cellular components of innate immune responses, meaning phagocytes
Summary
Staphylococcus aureus (S. aureus) is a Gram-positive commensal bacterium that is a leading cause of various invasive infections from soft skin tissue colonization to infections on implanted medical devices such as prosthetic joints. The intrinsic capacity of S. aureus to adapt to its environment contributes toward its survival inside host tissues. An example of this type of adaptation is the capacity to form biofilms which are, contrary to the free-floating planktonic form of growth, microbial communities encased in a self-produced matrix composed of extracellular DNA (eDNA), proteins and polysaccharides (Moormeier and Bayles, 2017). According to the US Center for Disease Control, approximately 65% of human infections involve biofilms, with S. aureus accounting for up to 50% of pathogens isolated from prosthetic joint infections (Costerton, 2001; Ricciardi et al, 2018). Biofilms are often implicated in recurrent infections due to their increased tolerance toward antimicrobial treatments and even host immune attacks (Bjarnsholt, 2013)
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