Where in the world do bacteria experience oxidative stress?

Abstract

Reactive oxygen species - superoxide, hydrogen peroxide and hydroxyl radicals - have long been suspected of constraining bacterial growth in important microbial habitats and indeed of shaping microbial communities. Over recent decades, studies of paradigmatic organisms such as Escherichia coli, Salmonella typhimurium, Bacillus subtilis and Saccharomyces cerevisiae have pinpointed the biomolecules that oxidants can damage and the strategies by which microbes minimize their injuries. What is lacking is a good sense of the circumstances under which oxidative stress actually occurs. In this MiniReview several potential natural sources of oxidative stress are considered: endogenous ROS formation, chemical oxidation of reduced species at oxic-anoxic interfaces, H₂ O₂ production by lactic acid bacteria, the oxidative burst of phagocytes and the redox-cycling of secreted small molecules. While all of these phenomena can be reproduced and verified in the lab, the actual quantification of stress in natural habitats remains lacking - and, therefore, we have a fundamental hole in our understanding of the role that oxidative stress actually plays in the biosphere.

Figure 1.. Endogenous oxidative stress.

The adventitious transfer of electrons from redox enzymes to oxygen generates a mixture of O₂⁻ and H₂O₂. These species oxidize the solvent-exposed iron centers of mononuclear Fe²⁺ enzymes and [4Fe-4S] dehydratases, provoking iron dissociation and activity loss. The H₂O₂ also reacts with the pool of loose iron, most notably leading to DNA damage from hydroxyl-radical production.

Figure 2.. Plausible sources of oxidative stress at the oxic-anoxic interface near the intestinal epithelium.

Oxygen influx from the epithelium collides with sulfide generated by luminal bacteria, potentially generating H₂O₂ through direct reaction. Lactic acid bacteria near the epithelium are also likely to excrete H₂O₂ as a direct metabolic product, threatening by-stander bacteria.

Figure 3.. Oxidant formation in phagosomes.

The O₂⁻ produced by the host NADPH oxidase cannot penetrate the cytoplasmic membranes of captive bacteria; either it, or its more-reactive protonated form HO₂^., are believed to injure the extracytoplasmic surface of bacteria. Dismutation produces H₂O₂ that can penetrate membranes. Tentative calculations suggest that O₂⁻, HO₂^., and H₂O₂ levels may be in the ranges of 10–50 μM, 0.1–4 μM, and 1–4 μM, respectively, depending upon phagosomal pH (Imlay, 2009). Modeling of fluxes in neutrophils predicts similar levels (Winterbourn et al., 2006).