How oxygen damages microbes: Oxygen tolerance and obligate anaerobiosis

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The orbital structure of molecular oxygen constrains it to accept electrons one at a time, and its unfavourable univalent reduction potential ensures that it can do so only with low-potential redox partners. In E. coli, this restriction prevents oxygen from oxidizing structural molecules. Instead, it primarily oxidizes reduced flavins, a reaction that is harmful only in that it generates superoxide and hydrogen peroxide as products. These species are stronger oxidants than is oxygen itself. They can oxidize dehydratase iron-sulphur clusters and sulphydryls, respectively, and thereby inactivate enzymes that are dependent upon these functional groups. Hydrogen peroxide also oxidizes free iron, generating hydroxyl radicals. Because hydroxyl radicals react with virtually any biomolecules they encounter, their reactivity is broadly dissipated, and only their reactions with DNA are known to have an important physiological impact. E. coli elaborates scavenging and repair systems to minimize the impact of this adventitious chemistry; mutants that lack these defences grow poorly in aerobic habitats. Some of the growth deficits of these mutants cannot be easily ascribed to sulphydryl, cluster, or DNA damage, indicating that important aspects of oxidative stress still lack a biochemical explanation. Obligate anaerobes cannot tolerate oxygen because they utilize metabolic schemes built around enzymes that react with oxidants. The reliance upon low-potential flavoproteins for anaerobic respiration probably causes substantial superoxide and hydrogen peroxide to be produced when anaerobes are exposed to air. These species then generate damage of the same type that they produce in aerotolerant bacteria. However, obligate anaerobes also utilize several classes of dioxygen-sensitive enzymes that are not needed by aerobes. These enzymes are used for processes that help maintain the redox balance during anaerobic fermentations. They catalyse reactions that are chemically difficult, and the reaction mechanisms require the solvent exposure of radicals or low-potential metal clusters that can react rapidly with oxygen. Recent work has uncovered adaptive strategies by which obligate anaerobes seek to minimize the damage done by superoxide and hydrogen peroxide. Their failure to divest themselves of enzymes that can be directly damaged by molecular oxygen suggests that evolution has not yet provided economical options to them.

Original languageEnglish (US)
Pages (from-to)111-153
Number of pages43
JournalAdvances in Microbial Physiology
StatePublished - 2002

ASJC Scopus subject areas

  • Microbiology
  • Physiology


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