Raman spectroscopic investigations of scytonemin : a new molecular biomarker for the search of the origin of oxygenic photosynthesis in Archean

Abstract

The advent of oxygenic photosynthesis in ancient cyanobacteria is one of the most important events in the evolutionary history of life, which lead to the oxidation of atmosphere and improved efficiency in biological energy yielding. However, when oxygenic photosynthesis originated remains a matter of debate. The existence of atmospheric oxygen since 2.45-2.32 Ga, known as the Great Oxidation Event (GOE), suggests that origin of oxygenic photosynthesis was surely before 2.45 Ga. Geochemical evidence including carbon isotopic compositions, nitrogen isotopic biogeochemistry, and transition metal isotopic compositions indicates that oxygenic photosynthesis might have emerged around 2.7 Ga in Neoarchaean. Besides, geobiological records such as microbially laminatd stromatolites, cyanobacterial microbial fossils, and molecular biomarkers suggest that the cyanobacterial records extend back to as early as ~3,500 million years ago. Scytonemin is a yellow-brown UV filter pigment widely distributed in cyanobacteria species, which possess stable physical and chemical properties against sedimentary degradation. Therefore, scytonemin is expected to be a biomarker for the origin and early evolution of cyanobacteria. In this study, I use electronic microscopy and Raman spectroscopy to search for scytonemin in a suite of sedimentary rocks, including stromatolites, banded iron formations and Precambrian phosphates. Though the kerogen and amorphous carbonaceous matter are clearly observed, the identification of scytonemin in these samples by experimental Raman spectroscopy is demonstrated to be difficult. Therefore, I further simulate the evolution of scytonemin under burial condition by using theoretical molecular calculations. Based on my assumptions, the molecular structure of scytonemin evolves owing to the degradation mechanisms such as aromatization, oxidation, reduction and polymerization, and a series of monomers and polymers could be theoretically extrapolated. The calculated Raman spectra of these derivatives show significant differences from those of the molecule scytonemin, which could explain the absence of diagnostic signals of scytonemin in Raman spectra of sedimentary rocks. It is also interesting that there is good consistency between the highly evolved scytonemin derivatives and kerogen in terms of elementary compositions, functional groups and their final profiles in Raman spectra, which implies cyanobacterial UV-screening pigments including scytonemin were possibly a major precursor of kerogen commonly preserved in the sedimentary rocks through time. Besides, ab initio calculations are carried out to investigate the UVR absorbing properties of scytonemin and its structural derivatives, including two putative precursors and the oxidized/reduced transformations. Both scytonemin and its derivatives have significant absorptions in the UVC region, which suggests the oceanic and terrestrial surfaces of Earth could be habitable for Archean life with sheath pigments without the need for an atmospheric UVR shield. With the combined high-resolution electron microscopic, Raman spectroscopic and molecular theoretical investigations, scytonemin as the novel molecular biomarker for oxygenic photosynthesis in Archean is characterized. These experimental results, along with theoretical calculations on scytonemin’s UV-absorbing properties and Raman activities, clearly illustrate the evolutionary history of scytonemin in sedimentary environments and demonstrate its important role as key biochemical UV-screening material for early Earth’s photosynthetic ecosystems.