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Review
. 2021 May;29(5):428-440.
doi: 10.1016/j.tim.2020.10.001. Epub 2020 Oct 24.

How Microbes Evolved to Tolerate Oxygen

Maryam Khademian  1 , James A Imlay  2
Affiliations
Review

How Microbes Evolved to Tolerate Oxygen

Maryam Khademian et al. Trends Microbiol. 2021 May.

Abstract

Ancient microbes invented biochemical mechanisms and assembled core metabolic pathways on an anoxic Earth. Molecular oxygen appeared far later, forcing microbes to devise layers of defensive tactics that fend off the destructive actions of both reactive oxygen species (ROS) and oxygen itself. Recent work has pinpointed the enzymes that ROS attack, plus an array of clever protective strategies that abet the well known scavenging systems. Oxygen also directly damages the low-potential metal centers and radical-based mechanisms that optimize anaerobic metabolism; therefore, committed anaerobes have evolved customized tactics that defend these various enzymes from occasional oxygen exposure. Thus a more comprehensive, detailed, and surprising view of oxygen toxicity is coming into view.

Keywords: anaerobiosis; evolution; iron; reactive oxygen species.

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Figures

Figure 1.
Figure 1.. The Timetable of Evolution of Major Cellular Features.
The data are inferred from fossils, environmental proxies, and high-resolution geochronology [16,98,99]. Bottom. Life evolved for 1.5 billion years (Gya) prior to the Great Oxygenation Event (GOE). Both reactive oxygen species (ROS) scavenging and aerobic respiration may have pre-dated the GOE, suggesting that significant amounts of oxygen may have accrued locally prior to its general accumulation in the atmosphere. Abbreviation: Rubisco, ribulose-1,5-bisphosphate carboxylase/oxygenase.
Figure 2.
Figure 2.. Changes in Atmospheric Oxygen and Oceanic Elemental Concentrations over Time.
(A) The prevailing view of the concentration of atmospheric oxygen suggests three steady states that roughly correspond to Archaean, Proterozoic, and Phanerozic eras. The gray areas show the range provided by geological proxies [13]. (B) The approximate concentrations of elements in the ocean are inferred from geochemical models and sediments, as summarized by Anbar [2]. A different pattern for changes in Ni and Zn concentrations was recently suggested by Robbins et al. [100]. Note the orders-of-magnitude decline in iron and the rise in copper. Abbreviations: Gya, billion years ago; PAL, present atmospheric level.
Figure 3.
Figure 3.. Few Steps Were Required to Evolve Aerobic Oxidizers.
(A) The green-sulfur photosynthetic bacterium Chlorobium lives in hypoxic, sulfur-rich waters under solar radiation – an environment that may resemble that in which similar bacteria lived on the ancient Earth. Its photocycle generates a protonmotive force that is used to both generate ATP and push electrons uphill through the bc1 and NADH dehydrogenase complexes, ultimately producing NADH as a cellular reductant. Carbon dioxide is assimilated by a reverse tricarboxylic acid (TCA) cycle, and larger biosynthetic precursors are produced by gluconeogenesis. The role of the TCA cycle and gluconeogenesis is to enable biosynthesis. (B) To evolve bacteria that oxidize carbohydrates, mass action need only reverse glycolysis, the TCA cycle, and the respiratory chain, while a single new enzyme – cytochrome oxidase – delivered the electrons to oxygen. Thus, most components of aerobic respiratory chains pre-dated the oxic world. Abbreviations: α-kg, α-ketoglutarate; AAs, amino acids; Ac-CoA, acetyl coenzyme A; AS, ATP synthase; bc1, ubiquinol cytochrome c oxidoreductase; bo oxidase; c, cytochrome c; Cyo, cytochrome F6P, fructose-6-phosphate; NTPs, nucleoside triphosphates; Nuo, NADH dehydrogenase 1; OAA, oxaloacetate; Pnt, transhydrogenase; R5P, ribulose-5-phosphate; RC, reaction center; SO, sulfide oxidase.
Figure 4.
Figure 4.. An Overview of Damage Caused by Molecular Oxygen and Its Reactive Species, Hydrogen Peroxide and Superoxide.
Oxygen freely equilibrates across cell membranes. Exogenous sources (lactic acid bacteria, macrophages, reduced thiols and metals) and endogenous sources (electron leak from redox enzymes and redox-cycling compounds) generate reactive oxygen species (ROS). The Fenton reaction between hydrogen peroxide and loosely bound intracellular iron forms hydroxyl radicals that can damage DNA. Hydrogen peroxide and superoxide disrupt enzymes that employ solvent-exposed Fe(II) or [4Fe-4S] cofactors. Molecular oxygen directly inactivates radical-based and low-potential enzymes.
Figure I.
Figure I.
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