How to define obligatory anaerobiosis? An evolutionary view on the antioxidant response system and the early stages of the evolution of life on Earth

Abstract

One of the former definitions of “obligate anaerobiosis” was based on three main criteria: 1) it occurs in organisms, so-called obligate anaerobes, which live in environments without oxygen (O2), 2) O2-dependent (aerobic) respiration, and 3) antioxidant enzymes are absent in obligate anaerobes. In contrast, aerobes need O2 in order to grow and develop properly. Obligate (or strict) anaerobes belong to prokaryotic microorganisms from two domains, Bacteria and Archaea. A closer look at anaerobiosis covers a wide range of microorganisms that permanently or in a time-dependent manner tolerate different concentrations of O2 in their habitats. On this basis they can be classified as obligate/facultative anaerobes, microaerophiles and nanaerobes. Paradoxically, O2 tolerance in strict anaerobes is usually, as in aerobes, associated with the activity of the antioxidant response system, which involves different antioxidant enzymes responsible for removing excess reactive oxygen species (ROS). In our opinion, the traditional definition of “obligate anaerobiosis” loses its original sense. Strict anaerobiosis should only be restricted to the occurrence of O2-independent pathways involved in energy generation. For that reason, a term better than “obligate anaerobes” would be O2/ROS tolerant anaerobes, where the role of the O2/ROS detoxification system is separated from O2-independent metabolic pathways that supply energy. Ubiquitous key antioxidant enzymes like superoxide dismutase (SOD) and superoxide reductase (SOR) in contemporary obligate anaerobes might suggest that their origin is ancient, maybe even the beginning of the evolution of life on Earth. It cannot be ruled out that c. 3.5 Gyr ago, local microquantities of O2/ROS played a role in the evolution of the last universal common ancestor (LUCA) of all modern organisms. On the basis of data in the literature, the hypothesis that LUCA could be an O2/ROS tolerant anaerobe is discussed together with the question of the abiotic sources of O2/ROS and/or the early evolution of cyanobacteria that perform oxygenic photosynthesis.