Timing the Evolution of Cyanobacterial Antioxidants: Superoxide Dismutases

Abstract

The ancestors of cyanobacteria generated Earth’s first biogenic molecular oxygen but how they dealt with its toxicity remains unconstrained. Here we investigated when superoxide dismutase enzymes (SODs) capable of removing superoxide free radicals evolved. We found 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 has been previously hypothesized that declining seawater Ni concentrations at the end of the Archaean caused a fundamental shift in the marine biosphere away from methanogenesis towards oxygenic photosynthesis. Our novel analyses of enzymes dealing with O2 toxicity now demonstrate that the beneficiaries of this chemical change - marine planktonic cyanobacteria - were able to utilize the remaining Ni from seawater 0.9-0.8 Ga to supplement their existing metabolic capabilities.

Molecular diversity and evolution of far-red light-acclimated photosystem I

“…A schematic tree based on that presented by Struneckýet al, 2023 highlighting some of the key orders as proposed by the authors. BASAL (gray shading) denotes the early diversification events, and MICRO (pale blue shading) and MACRO (pale pink shading) denote microcyanobacteria and macrocyanobacteria, respectively, as described previously (Sańchez-Baracaldo, 2015;Boden et al, 2021). The colored circles represent the presence of strains with the capacity to produce Chl f, d, or b within the respective order.…”

“…A complete gene cluster could have become assembled at around the time macrocyanobacteria began to diversify. Using some of the latest work attempting to time the diversification of cyanobacteria (Boden et al, 2021;Fournier et al, 2021), it is possible to assign some reasonable timings for these events (Figure 10). For example, assuming that ChlF and FRL-PsbA acquired their functions relatively soon after they duplicated from standard, but early forms of PsbA, prior to the MRCA of cyanobacteria, this would constrain their origin to before the Great Oxidation Event (GOE), in the range of 2.6 (Boden et al, 2021) to before 3.0 Ga (Fournier et al, 2021).…”

“…Using some of the latest work attempting to time the diversification of cyanobacteria (Boden et al, 2021;Fournier et al, 2021), it is possible to assign some reasonable timings for these events (Figure 10). For example, assuming that ChlF and FRL-PsbA acquired their functions relatively soon after they duplicated from standard, but early forms of PsbA, prior to the MRCA of cyanobacteria, this would constrain their origin to before the Great Oxidation Event (GOE), in the range of 2.6 (Boden et al, 2021) to before 3.0 Ga (Fournier et al, 2021). The duplication of FRL-PsbD and FRL-PsbC would be placed just before or at around the start of the GOE, while all duplications enabling the assembly of a FaRLiP cluster had already occurred by about 2.2 to 2.0 Ga, the time that extant macrocyanobacteria lineages began to radiate (Boden et al, 2021;Fournier et al, 2021).…”

“…For example, assuming that ChlF and FRL-PsbA acquired their functions relatively soon after they duplicated from standard, but early forms of PsbA, prior to the MRCA of cyanobacteria, this would constrain their origin to before the Great Oxidation Event (GOE), in the range of 2.6 (Boden et al, 2021) to before 3.0 Ga (Fournier et al, 2021). The duplication of FRL-PsbD and FRL-PsbC would be placed just before or at around the start of the GOE, while all duplications enabling the assembly of a FaRLiP cluster had already occurred by about 2.2 to 2.0 Ga, the time that extant macrocyanobacteria lineages began to radiate (Boden et al, 2021;Fournier et al, 2021). Remarkably, the MRCA of extant Nodosilineales is timed in the work by Boden et al (2021) to about 0.8 Ga. Boden et al (2021) performed the most taxa-rich molecular clock analysis of cyanobacterial evolution available, which contains several representatives from diverse Nodosilineales, including some of the FaRLiP strains.…”

“…A schematic and simplified representation of cyanobacterial phylogeny is shown in Figure 1 based on the recent taxonomic work by Struneckýet al, 2023, and some representative genera and strains are listed in Table 1. After the early diversification events leading to the basal clades, a large expansion of diversity occurred, which can be subdivided in two major radiation events; one leading to the microcyanobacteria and another to the macrocyanobacteria, as described previously (Sańchez-Baracaldo, 2015;Boden et al, 2021). The microcyanobacteria are characterized by having an overall small cell diameter, ranging from ca.…”