The trouble with oxygen: The ecophysiology of extant phototrophs and implications for the evolution of oxygenic photosynthesis

Abstract

The ability to harvest light to drive chemical reactions and gain energy provided microbes access to high energy electron donors which fueled primary productivity, biogeochemical cycles, and microbial evolution. Oxygenic photosynthesis is often cited as the most important microbial innovation-the emergence of oxygen-evolving photosynthesis, aided by geologic events, is credited with tipping the scale from a reducing early Earth to an oxygenated world that eventually lead to complex life. Anoxygenic photosynthesis predates oxygen-evolving photosynthesis and played a key role in developing and fine-tuning the photosystem architecture of modern oxygenic phototrophs. The release of oxygen as a by-product of metabolic activity would have caused oxidative damage to anaerobic microbiota that evolved under the anoxic, reducing conditions of early Earth. Photosynthetic machinery is particularly susceptible to the adverse effects of oxygen and reactive oxygen species and these effects are compounded by light. As a result, phototrophs employ additional detoxification mechanisms to mitigate oxidative stress and have evolved alternative oxygen-dependent enzymes for chlorophyll biosynthesis. Phylogenetic reconstruction studies and biochemical characterization suggest photosynthetic reactions centers, particularly in Cyanobacteria, evolved to both increase efficiency of electron transfer and avoid photodamage caused by chlorophyll radicals that is acute in the presence of oxygen. Here we review the oxygen and reactive oxygen species detoxification mechanisms observed in extant anoxygenic and oxygenic photosynthetic bacteria as well as the emergence of these mechanisms over evolutionary time. We examine the distribution of phototrophs in modern systems and phylogenetic reconstructions to evaluate the emergence of mechanisms to mediate oxidative damage and highlight changes in photosystems and reaction centers, chlorophyll biosynthesis, and niche space in response to oxygen production. This synthesis supports an emergence of H₂S-driven anoxygenic photosynthesis in Cyanobacteria prior to the evolution of oxygenic photosynthesis and underscores a role for the former metabolism in fueling fine-tuning of the oxygen evolving complex and mechanisms to repair oxidative damage. In contrast, we note the lack of elaborate mechanisms to deal with oxygen in non-cyanobacterial anoxygenic phototrophs suggesting these microbes have occupied similar niche space throughout Earth's history.

Keywords: Anoxygenic; Archean; Bacteriochlorophyll; Chlorophyll; Evolution; Light; Niche; Oxygenic; PSI; PSII; Photosynthesis; Photosystem; Phototroph; RCI; RCII; Reaction center; Reactive oxygen species; Sulfide.