Functional and Structural Characterization of Pediococcus pentosaceus-Derived Biosurfactant and Its Biomedical Potential against Bacterial Adhesion, Quorum Sensing, and Biofilm Formation.

Mohd Adnan,Mitesh Patel,Md Imtaiyaz Hassan,Manojkumar Sachidanandan,Syed Amir Ashraf,Walid Sabri Hamadou,Arif Jamal Siddiqui,Arshad Jamal,Amir Mahgoub Awadelkareem,Fevzi Bardakci,Riadh Badraoui,Mejdi Snoussi

doi:10.3390/antibiotics10111371

Abstract

Biosurfactants are surface-active molecules of microbial origin and alternatives to synthetic surfactants with various applications. Due to their environmental-friendliness, biocompatibility, biodegradability, effectiveness to work under various environmental conditions, and non-toxic nature, they have been recently recognized as potential agents with therapeutic and commercial importance. The biosurfactant produced by various probiotic lactic acid bacteria (LAB) has enormous applications in different fields. Thus, in vitro assessment of biofilm development prevention or disruption by natural biosurfactants derived from probiotic LAB is a plausible approach that can lead to the discovery of novel antimicrobials. Primarily, this study aims to isolate, screen, and characterize the functional and biomedical potential of biosurfactant synthesized by probiotic LAB Pediococcus pentosaceus (P. pentosaceus). Characterization consists of the assessment of critical micelle concentration (CMC), reduction in surface tension, and emulsification index (% EI24). Evaluation of antibacterial, antibiofilm, anti-QS, and anti-adhesive activities of cell-bound biosurfactants were carried out against different human pathogenic bacteria (B. subtilis, P. aeruginosa, S. aureus, and E. coli). Moreover, bacterial cell damage, viability of cells within the biofilm, and exopolysaccharide (EPS) production were also evaluated. As a result, P. pentosaceus was found to produce 4.75 ± 0.17 g/L biosurfactant, which displayed a CMC of 2.4 ± 0.68 g/L and reduced the surface tension from 71.11 ± 1.12 mN/m to 38.18 ± 0.58 mN/m. P. pentosaceus cells bound to the crude biosurfactant were found to be effective against all tested bacterial pathogens. It exhibited an anti-adhesion ability and impeded the architecture of the biofilm matrix by affecting the viability and integrity of bacterial cells within biofilms and reducing the total EPS content. Furthermore, the crude biosurfactant derived from P. pentosaceus was structurally characterized as a lipoprotein by GC-MS analysis, which confirms the presence of lipids and proteins. Thus, our findings represent the potent anti-adhesion and antibiofilm potential of P. pentosaceus crude biosurfactant for the first time, which may be explored further as an alternative to antibiotics or chemically synthesized toxic antibiofilm agents.

Highlights

Adherence of bacteria on living and non-living surfaces is the first and most important step in the formation of biofilms, a natural phenomenon of most bacteria producing extracellular polymeric matrix in response to various environmental cues
Based on morphological and 16S rRNA sequence analysis, isolated probiotic lactic acid bacteria (LAB) was was identified as P. pentosaceus
In the present study, we focused on production ability, characterizing a LAB-derived biosurfactant

Summary

Introduction

Adherence of bacteria on living and non-living surfaces is the first and most important step in the formation of biofilms, a natural phenomenon of most bacteria producing extracellular polymeric matrix in response to various environmental cues. Various evidence suggests that microbial life in biofilm mode leads to increased resistance toward host defense systems, antibiotics, and other modes of actions [3,4,5,6,7,8,9]. Biofilm removal is a global challenge that necessitates developing novel natural bioactive compounds to control biofilms as an alternative to antibiotics or chemically synthesized antibiofilm agents. Biosurfactants are amphiphilic substances commonly synthesized by different microbes on their surface or as extracellular secretion, which efficiently reduces the surface tension and represent emulsifying activities [10]. Various biosurfactants have displayed antimicrobial and anti-adhesive properties, leading them as suitable candidates to combat a variety of infections and biofilms caused by diverse microorganisms [12]

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