Abstract
In food chain, Pseudomonas spp. cause spoilage by reducing shelf life of fresh products, especially during cold storage, with a high economic burden for industries. However, recent studies have shed new light on health risks occurring when they colonize immunocompromised patient tissues. Likewise to P. aeruginosa, they exhibit antibiotic resistance and biofilm formation, responsible for their spread and persistence in the environment. Biofilm formation might be induced by environmental stresses, such as temperature fluctuations causing physiological and metabolic changes exacerbating food spoilage (by protease and pigment synthesis), and the production of adhesion molecules, chemotactic or underestimated virulence factors. In order to provide a new insight into phenotypic biodiversity of Pseudomonas spoilers isolated from cold stored cheese, in this work 19 Pseudomonas spp. were investigated for biofilm, pigments, exopolysaccharide production and motility at low temperature. Only nine strains showed these phenotypic traits and the blue pigmenting cheese strain P. fluorescens ITEM 17298 was the most distinctive. In addition, this strain decreased the survival probability of infected Galleria mellonella larvae, showing, for the first time, a pathogenic potential. Genomic and proteomic analyses performed on the ITEM 17298 planktonic cells treated or not with lactoferrin derived antibiofilm peptides allowed to reveal specific biofilm related-pathways as well as proteins involved in pathogenesis. Indeed, several genes were found related to signaling system by cGMP-dependent protein kinases, cellulose, rhamnolipid and alginate synthesis, antibiotic resistance, adhesion and virulence factors. The proteome of the untreated ITEM 17298, growing at low temperature, showed that most of the proteins associated with biofilm regulation, pigmentation motility, antibiotic resistance and pathogenecity were repressed, or decreased their levels in comparison to that of the untreated cultures. Thus, the results of this work shed light on the complex pathways network allowing psychrotrophic pseudomonads to adapt themselves to food-refrigerated conditions and enhance their spoilage. In addition, the discovery of virulence factors and antibiotic resistance determinants raises some questions about the need to deeper investigate these underestimated bacteria in order to increase awareness and provide input to update legislation on their detection limits in foods.
Highlights
The Pseudomonas genus shows a wide species diversity and encompasses species isolated in a number types of ecological niches and environments
Nine out of 19 strains, belonging to P. fluorescens and P. gessardii species, produced pigmented or fluorescent colonies on King B at 15◦C (Supplementary Table S1); 2 out of 10 P. fluorescens strains grew as brown colonies on King A and King B and only ITEM 17298 and ITEM 17299 produced dark pigment on M63 medium at the fourth day of incubation at 15◦C
In this work for the first time we showed that distinctive traits of psychrotrophic Pseudomonas spp. food spoilers could be involved in adaptive responses to cold stresses and in microbial competition
Summary
The Pseudomonas genus shows a wide species diversity and encompasses species isolated in a number types of ecological niches and environments They occur in soil, water, and marine environments as well as in foods, clinical instruments and medical products (Palleroni, 2010; Raposo et al, 2017). Phenotypic variants of psychrotrophic P. fluorescens strains grew at high temperature, caused hemolysis by means of phospholipase C and surfactant secretion (Sperandio et al, 2010), modulated the permeability of a Caco-2/TC7 intestinal epithelial model (Madi et al, 2010b), and induced macrophage necrosis in a eukaryotic cell model (Sperandio et al, 2012) These findings indicate the emergence of different novel strains, originating from the environment reservoir and spreading in clinical settings, to elicit a neutrophilic response resulting in significant damage to host tissues, often worsen by resistance to clinical treatments (Madi et al, 2010a; Scales et al, 2014; Mazurier et al, 2015). Adaptive behavior of Pseudomonas spp. is mainly correlated
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