Abstract
Prodigiosin is a heterocyclic bacterial secondary metabolite belonging to the class of tripyrrole compounds, synthesized by various types of bacteria including Serratia species. Prodigiosin has been the subject of intense research over the last decade for its ability to induce apoptosis in several cancer cell lines. Reports suggest that prodigiosin promotes oxidative damage to double-stranded DNA (dsDNA) in the presence of copper ions and consequently leads to inhibition of cell-cycle progression and cell death. However, prodigiosin has not been previously implicated in biofilm inhibition. In this study, the link between prodigiosin and biofilm inhibition through the production of redox active metabolites is presented. Our study showed that prodigiosin (500 μM) (extracted from Serratia marcescens culture) and a prodigiosin/copper(II) (100 μM each) complex have strong RNA and dsDNA cleaving properties while they have no pronounced effect on protein. Results support a role for oxidative damage to biomolecules by H2O2 and hydroxyl radical generation. Further, it was demonstrated that reactive oxygen species scavengers significantly reduced the DNA and RNA cleaving property of prodigiosin. P. aeruginosa cell surface hydrophobicity and biofilm integrity were significantly altered due to the cleavage of nucleic acids by prodigiosin or the prodigiosin/copper(II) complex. In addition, prodigiosin also facilitated the bactericidal activity. The ability of prodigiosinto cause nucleic acid degradation offers novel opportunities to interfere with extracellular DNA dependent bacterial biofilms.
Highlights
Biofilm formation and persistence is controlled by the biofilm matrix or extracellular polymeric substances (EPS) which represent about 90% of the total dry mass of the biofilm (Flemming and Wingender, 2010)
This study revealed that prodigiosinalone and in combination with copper [Prd/Cu(II)] significantly disrupts both biofilm establishment and pre-established biofilms of P. aeruginosa PA14 wild-type through an impact on nucleic acids
Evidence is presented supporting a role for production of reactive oxygen species that induce oxidative damage to DNA and RNA. These findings provide novel insights into the relationship between prodigiosin and biofilm formation that offer opportunities to interfere with bacterial biofilms
Summary
Biofilm formation and persistence is controlled by the biofilm matrix or extracellular polymeric substances (EPS) which represent about 90% of the total dry mass of the biofilm (Flemming and Wingender, 2010). The biofilm matrix primarily consists of polysaccharides, proteins, lipids, nucleic acids (DNA and RNA), and metabolites. Polysaccharides and proteins constitute the majority (∼75–90%) of EPS whereas lipids and nucleic acids constitute a minority (∼1–10%; More et al, 2014). Removal of extracellular DNA (eDNA) from EPS disrupts biofilms formed by bacterial species including Staphylococcus epidermidis, Bacillus cereus, Neisseria meningiditis, and Pseudomonas aeruginosa (Whitchurch et al, 2002; Liu et al, 2008; Vilain et al, 2009; Das et al, 2010; Lappann et al, 2010)
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