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      Oxidative stress responses in biofilms

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          Abstract

          Oxidizing agents are low-molecular-weight molecules that oxidize other substances by accepting electrons from them. They include reactive oxygen species (ROS), such as superoxide anions (O 2 ), hydrogen peroxide (H 2O 2), and hydroxyl radicals (HO ), and reactive chlorine species (RCS) including sodium hypochlorite (NaOCl) and its active ingredient hypochlorous acid (HOCl), and chloramines. Bacteria encounter oxidizing agents in many different environments and from diverse sources. Among them, they can be produced endogenously by aerobic respiration or exogenously by the use of disinfectants and cleaning agents, as well as by the mammalian immune system. Furthermore, human activities like industrial effluent pollution, agricultural runoff, and environmental activities like volcanic eruptions and photosynthesis are also sources of oxidants. Despite their antimicrobial effects, bacteria have developed many mechanisms to resist the damage caused by these toxic molecules. Previous research has demonstrated that growing as a biofilm particularly enhances bacterial survival against oxidizing agents. This review aims to summarize the current knowledge on the resistance mechanisms employed by bacterial biofilms against ROS and RCS, focussing on the most important mechanisms, including the formation of biofilms in response to oxidative stressors, the biofilm matrix as a protective barrier, the importance of detoxifying enzymes, and increased protection within multi-species biofilm communities. Understanding the complexity of bacterial responses against oxidative stress will provide valuable insights for potential therapeutic interventions and biofilm control strategies in diverse bacterial species.

          Highlights

          • Oxidizing agents induce biofilm formation.

          • Biofilm matrix as a protective barrier against ROS and RCS.

          • Antioxidant enzymes increase survival of biofilms against oxidants.

          • Multi-species biofilms promote oxidative stress resistance.

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          Most cited references175

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          The biofilm matrix.

          The microorganisms in biofilms live in a self-produced matrix of hydrated extracellular polymeric substances (EPS) that form their immediate environment. EPS are mainly polysaccharides, proteins, nucleic acids and lipids; they provide the mechanical stability of biofilms, mediate their adhesion to surfaces and form a cohesive, three-dimensional polymer network that interconnects and transiently immobilizes biofilm cells. In addition, the biofilm matrix acts as an external digestive system by keeping extracellular enzymes close to the cells, enabling them to metabolize dissolved, colloidal and solid biopolymers. Here we describe the functions, properties and constituents of the EPS matrix that make biofilms the most successful forms of life on earth.
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            A common mechanism of cellular death induced by bactericidal antibiotics.

            Antibiotic mode-of-action classification is based upon drug-target interaction and whether the resultant inhibition of cellular function is lethal to bacteria. Here we show that the three major classes of bactericidal antibiotics, regardless of drug-target interaction, stimulate the production of highly deleterious hydroxyl radicals in Gram-negative and Gram-positive bacteria, which ultimately contribute to cell death. We also show, in contrast, that bacteriostatic drugs do not produce hydroxyl radicals. We demonstrate that the mechanism of hydroxyl radical formation induced by bactericidal antibiotics is the end product of an oxidative damage cellular death pathway involving the tricarboxylic acid cycle, a transient depletion of NADH, destabilization of iron-sulfur clusters, and stimulation of the Fenton reaction. Our results suggest that all three major classes of bactericidal drugs can be potentiated by targeting bacterial systems that remediate hydroxyl radical damage, including proteins involved in triggering the DNA damage response, e.g., RecA.
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              Bacterial biofilms: from the natural environment to infectious diseases.

              Biofilms--matrix-enclosed microbial accretions that adhere to biological or non-biological surfaces--represent a significant and incompletely understood mode of growth for bacteria. Biofilm formation appears early in the fossil record (approximately 3.25 billion years ago) and is common throughout a diverse range of organisms in both the Archaea and Bacteria lineages, including the 'living fossils' in the most deeply dividing branches of the phylogenetic tree. It is evident that biofilm formation is an ancient and integral component of the prokaryotic life cycle, and is a key factor for survival in diverse environments. Recent advances show that biofilms are structurally complex, dynamic systems with attributes of both primordial multicellular organisms and multifaceted ecosystems. Biofilm formation represents a protected mode of growth that allows cells to survive in hostile environments and also disperse to colonize new niches. The implications of these survival and propagative mechanisms in the context of both the natural environment and infectious diseases are discussed in this review.
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                Author and article information

                Contributors
                Journal
                Biofilm
                Biofilm
                Biofilm
                Elsevier
                2590-2075
                23 May 2024
                June 2024
                23 May 2024
                : 7
                : 100203
                Affiliations
                [1]Department of Health Sciences, Carleton University, 1125 Colonel By Drive, Ottawa, K1S 5B6, ON, Canada
                Author notes
                [* ]Corresponding author. joerg.overhage@ 123456carleton.ca
                Article
                S2590-2075(24)00028-5 100203
                10.1016/j.bioflm.2024.100203
                11139773
                38827632
                f966b3f6-db66-4965-981a-2f11385fec19
                © 2024 The Authors

                This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/).

                History
                : 28 February 2024
                : 22 May 2024
                : 22 May 2024
                Categories
                Article

                biofilms,oxidative stress,antimicrobial resistance,reactive oxygen species,reactive chlorine species,hydrogen peroxide,hypochlorous acid

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