Oxygenic cyanobacteria emerged before the great oxidation event

Abstract

The rise of atmospheric oxygen fundamentally changed the evolutionary pathway of life on Earth. However, the fossil and molecular evidences gave inconsistent time for the emergence of oxygenic cyanobacteria. Though the onset of the oxidation of atmosphere is constrained to be 2.45-2.32 Gyr, the hitherto reliable evidence for the oldest oxygenic photosynthesis is about 2.15 Gyr. In this study, we report the identification of scytonemin, the sheath pigment only produced by cyanobacteria to shield them from the damage of strong ultraviolet radiations in the 2460 Myr Kuruman and possibly also in the 2728-Myr Abitibi banded iron formations. It is indicated that the oxygenic photosynthesis has developed earlier than the onset of the Great Oxidation Event (GOE) and we suggest that it was the bloom of cyanobacteria majorly contributed to the accumulation of atmospheric oxygen. Cyanobacteria are oxygenic photosynthetic phytoplanktonic prokaryotes hypothesized to have dominated the euphotic zone of the early Precambrian biosphere. As the continents probably only compressed <10% of Earth’s crust before 2.5 Ga, most of the biological zones would distribute in the vast epicontinental seawater without much shielding from the solar radiation. If cyanobacteria emerged before 2.32-2.45 Ga, the reduced atmosphere ([O2] <0.001% of present atmospheric level) should not have an ozonosphere to filter shortwave ultraviolet radiation (UVR) from reaching the surface of Earth. Cyanobacteria, along with the other phytoplanktons inhabited the surface of Earth had to develop strategies to resistant the UVR-damage. The inheritance of the ability of UVR-resistance by the diverse nowadays cyanobacteria implies they really did. Among the strategies developed by cyanobacteria, the synthesis of scytonemin is unique to cyanobacteria which not only allow cyanobacteria to effectively absorb UVB and UVA, but it may also effectively absorb UVC which was a much strong, shorter wavelengthed UVR that reached the surface of Earth before the formation of the ozonosphere after GOE. The high melting point of this molecule (>325 degree Celsius) allow it survive the low-grade metamorphism and the long geological evolution. We found firm evidences of the preservation of scytonemin in the 2460-Myr Kuruman BIF and its probably existence in the 2728-Myr Abitibi BIF which clearly indicated the existence of cyanobacteria before GOE. The Raman microbe analyses of the Kuruman BIF for the surface of magnetite crystals and the surface of the wall rocks of magnetite crystals detected the existence of Nu(CO) phenolic, Nu(CC) ring breathing pyrrole, Nu(CCH) p-disubstituted aromatic ring, which together indicated the existence of scytonemin in the 2460-Myr Kuruman BIF. In the Abitibi BIF, Nu(CN) indole ring can also be detected for strong signals instead of the Nu(CCH) vibrations in the Kuruman BIF. In both BIF samples, strong signals of kerogen can also be detected which does not have to be coexisting with scytonemin. The detection of scytonemin in the 2460-Myr Kuruman and possibly in the 2728-Myr Abitibi BIFs indicated the development of oxygenic photosynthesis before the onset of oxidation of the atmosphere and ocean. The result also implies that till 2460-Myr, the atmosphere could still penetrate by UVC. As the oxidation of the terrestrial surface began at about 2.45 Ga, the oxidation of the ocean and the atmosphere might only take a relatively short time (2.45-2.32 Ga). If cyanobacteria originated after GOE, UVC would not reach the surface of Earth and cyanobacteria did not have to make pigments such as scytonemin for absorbing UVC (wavelengths shorter than 280 nm). However, scytonemin produced by the modern cyanobacteria in the solar radiation without UVC can still absorb UVC which circumstantially indicates that cyanobacteria should have emerged before the Great Oxidation Event.