Biofilms as protective cocoons against biocides: from bacterial adaptation to One Health issues

Abstract

Bacteria in the food chain mostly live in communities associated with surfaces known as biofilms, which confer specific survival and adaptive abilities. In such communities, the bacteria mostly exhibit higher tolerance to external stress, and their recurrent exposure along the food chain to biocides used during cleaning and disinfection procedures raises concern about the adaptation routes they develop, both at single-cell and communal levels. In recent years, an increasing number of research subjects have focused on understanding the specific features of biofilms that enable bacterial populations to adapt to biocide exposure within a ‘protective cocoon’. The first part of this review concentrates on the diversity of adaptive strategies, including structural modulation of these biofilms, physiological response or the acquisition of genetic resistance. The second part discusses the possible side effects of biofilm adaptation to biocides on antimicrobial cross-resistance, virulence and colonization features from a One Health perspective.

SOS-Inducing Drugs Trigger Nucleic Acid Release and Biofilm Formation in Gram-Negative Bacteria

“…SOS-induced nucleic acid release and protein release were inhibited by zinc salts, the NO donor SNAP, and dequalinium. In addition to triggering emergence of new antibiotic resistance via hypermutation, the SOS-induced biofilm formation may also affect resistance by reducing penetration of drugs into the biofilm [ 6 ], by decreased metabolic activity of bacteria due to limited oxygen or nutrients, and by many other factors.…”

“…The SOS response had previously been implicated as a trigger of biofilm formation, but the role of DNA in the biofilms was not appreciated [ 5 ]. Bacterial biofilms have been recognized as sanctuary sites in which emergence of antimicrobial resistance occurs [ 6 ].…”

Polyhexamethylene biguanide promotes adaptive cross-resistance to gentamicin in Escherichia coli biofilms

“…Resistant variants appear naturally in bacterial populations and could be preferentially selected in Ec709 by the biofilm lifestyle itself rather than biocidal exposure. This can be related to particular chemical microenvironments in the three-dimensional structure of Ec709 biofilm that could participate in the induction of specific phenotypes and/or selection of genetic variants ( Uruén et al., 2020 ; Charron et al., 2023 ). In addition, recent findings showed that hypermutator emergence rates are dependent of stress type in E. coli populations ( Callens et al., 2023 ).…”

“…Unlike antibiotics, which often have specific targets in the bacterial cell, biocides typically employ a multi-targeted mode of action. However, mechanisms developed by bacteria to resist biocides can be close or imply common cellular components to those involved in antibiotic resistance and multiple possible cross-resistances have already been identified in different bacterial species ( Maillard, 2018 ; Charron et al., 2023 ). Schematically, when exposing bacteria to a biocide, cross-adaptations could result from two major types of mechanisms.…”

“…The dense tridimensional structure creates chemical gradients, resulting in distinct microenvironments for bacteria residing in the periphery, exposed to the external medium, as opposed to those in the inner layers, typically with low access to nutrients and oxygen ( Jo et al., 2022 ). This chemical heterogeneity favors varied physiological responses, giving rise to different populations, including persister cells or viable but non-culturable phenotypes, often characterized by a substantial growth slowdown ( Charron et al., 2023 ). These metabolic states can confer a heightened tolerance to antimicrobials, thus enhancing bacterial survival and potential acquisition of genetic resistance ( Levin-Reisman et al., 2017 ; Nordholt et al., 2021 ).…”