Abstract
Metal ions are necessary for the proper functioning of the immune system, and, therefore, they might have a significant influence on the interaction between bacteria and host. Ionic dyshomeostasis has been recently observed also in cystic fibrosis (CF) patients, whose respiratory tract is frequently colonized by Stenotrophomonas maltophilia. For the first time, here we used an inductively mass spectrometry method to perform a spatial and temporal analysis of the pattern of changes in a broad range of major trace elements in response to pulmonary infection by S. maltophilia. To this, DBA/2 mouse lungs were comparatively infected by a CF strain and by an environmental one. Our results showed that pulmonary ionomic profile was significantly affected during infection. Infected mice showed increased lung levels of Mg, P, S, K, Zn, Se, and Rb. To the contrary, Mn, Fe, Co, and Cu levels resulted significantly decreased. Changes of element concentrations were correlated with pulmonary bacterial load and markers of inflammation, and occurred mostly on day 3 post-exposure, when severity of infection culminated. Interestingly, CF strain – significantly more virulent than the environmental one in our murine model - provoked a more significant impact in perturbing pulmonary metal homeostasis. Particularly, exposure to CF strain exclusively increased P and K levels, while decreased Fe and Mn ones. Overall, our data clearly indicate that S. maltophilia modulates pulmonary metal balance in a concerted and virulence-dependent manner highlighting the potential role of the element dyshomeostasis during the progression of S. maltophilia infection, probably exacerbating the harmful effects of the loss of CF transmembrane conductance regulator function. Further investigations are required to understand the biological significance of these alterations and to confirm they are specifically caused by S. maltophilia.
Highlights
Stenotrophomonas maltophilia is a Gram-negative opportunistic pathogen especially in hospitalized or compromised patients where infection is associated to high mortality and morbidity [1,2]
Changes in lung element concentrations correlate with the severity of infection In order to tentatively investigate the biological significance of lung metal dyshomeostasis caused by S. maltophilia infection, we further evaluated the existence of a correlation between changes in lung element concentrations and markers for the severity of the infection, as assessed by pulmonary bacterial load (CFU/lung) and pro-inflammatory cytokine levels
Our results demonstrated that Inductively Coupled Plasma Mass Spectrometry (ICP-MS) analysis represents an useful technique to evaluate changes in host ionomic profile during pulmonary infection, in order to understand the impact infection might have on the host
Summary
Stenotrophomonas maltophilia is a Gram-negative opportunistic pathogen especially in hospitalized or compromised patients where infection is associated to high mortality and morbidity [1,2]. In a series of studies we found evidences highly suggestive for the pathogenetic role of S. maltophilia in CF patients [7,8,9,10,11,12,13]. This microorganism is able to grow as biofilms – sessile communities inherently resistant to antibiotics - on abiotic surfaces [7,8,9,10], and on CF-derived epithelial monolayer [11], probably as a consequence of a selective adaptation to CF airways [12]. In a model of acute respiratory infection we observed that S. maltophilia significantly contributes to the inflammatory process resulting in compromised respiratory function and death [13]
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