Abstract
The ancestors of cyanobacteria generated Earth’s first biogenic molecular oxygen, but how they dealt with oxidative stress remains unconstrained. Here we investigate when superoxide dismutase enzymes (SODs) capable of removing superoxide free radicals evolved and estimate when Cyanobacteria originated. Our Bayesian molecular clocks, calibrated with microfossils, predict that stem Cyanobacteria arose 3300–3600 million years ago. Shortly afterwards, we find phylogenetic evidence that ancestral cyanobacteria used SODs with copper and zinc cofactors (CuZnSOD) during the Archaean. By the Paleoproterozoic, they became genetically capable of using iron, nickel, and manganese as cofactors (FeSOD, NiSOD, and MnSOD respectively). The evolution of NiSOD is particularly intriguing because it corresponds with cyanobacteria’s invasion of the open ocean. Our analyses of metalloenzymes dealing with reactive oxygen species (ROS) now demonstrate that marine geochemical records alone may not predict patterns of metal usage by phototrophs from freshwater and terrestrial habitats.
Highlights
The ancestors of cyanobacteria generated Earth’s first biogenic molecular oxygen, but how they dealt with oxidative stress remains unconstrained
To elucidate which transition metals cyanobacteria first used to protect themselves against the oxidative stress caused by O2.−, the evolutionary history of superoxide dismutase enzymes (SODs) genes was modeled and mapped onto an updated time-calibrated phylogeny
Previous estimates place the divergence of cyanobacteria and their closest relatives, vampirovibrionia[40,42], in the neoarchaean between 2.5 and 2.6 Ga55, but our molecular clock analyses point to an earlier origin where the cyanobacterial lineage emerges in the Paleoarchaean between 3.3 and 3.6 Ga based on mean predicted ages (95% confidence intervals range from 2.8 to 4.2 Ga) (Table 2)
Summary
The ancestors of cyanobacteria generated Earth’s first biogenic molecular oxygen, but how they dealt with oxidative stress remains unconstrained. Since O2 is highly reactive, early Cyanobacteria—the first producers of biogenic O2—likely experienced selective pressure, resulting in the evolution of more efficient antioxidants Such effects have been documented in the photosynthetic machinery, which has been evolving strategies of dealing with reactive oxygen species (ROS) throughout its history[11]. Peroxidases and catalases enhance the rate of removal of peroxides (such as H2O2 and R-O-O-H)[13], SORs and SODs remove superoxide free radicals (O2.−)[14] These O2.− are produced as a byproduct of photosynthetic and respiratory electron transport chains[12] as well as extracellular processes on the cell surface[15]. This is problematic because metal availability differs across oceanic and terrestrial environments[38,39]
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