Timing the Evolutionary Advent of Cyanobacteria and the Later Great Oxidation Event Using Gene Phylogenies of a Sunscreen

Abstract

The biosynthesis of the unique cyanobacterial (oxyphotobacterial) indole-phenolic UVA sunscreen, scytonemin, is coded for in a conserved operon that contains both core metabolic genes and accessory, aromatic amino acid biosynthesis genes dedicated to supplying scytonemin’s precursors. Comparative genomics shows conservation of this operon in many, but not all, cyanobacterial lineages. Phylogenetic analyses of the operon’s aromatic amino acid genes indicate that five of them were recruited into the operon after duplication events of their respective housekeeping cyanobacterial cognates. We combined the fossil record of cyanobacteria and relaxed molecular clock models to obtain multiple estimates of these duplication events, setting a minimum age for the evolutionary advent of scytonemin at 2.1 ± 0.3 billion years. The same analyses were used to estimate the advent of cyanobacteria as a group (and thus the appearance of oxygenic photosynthesis), at 3.6 ± 0.2 billion years before present. Post hoc interpretation of 16S rRNA-based Bayesian analyses was consistent with these estimates. Because of physiological constraints on the use of UVA sunscreens in general, and the biochemical constraints of scytonemin in particular, scytonemin’s age must postdate the time when Earth’s atmosphere turned oxic, known as the Great Oxidation Event (GOE). Indeed, our biological estimate is in agreement with independent geochemical estimates for the GOE. The difference between the estimated ages of oxygenic photosynthesis and the GOE indicates the long span (on the order of a billion years) of the era of “oxygen oases,” when oxygen was available locally but not globally. IMPORTANCE The advent of cyanobacteria, with their invention of oxygenic photosynthesis, and the Great Oxidation Event are arguably among the most important events in the evolutionary history of life on Earth. Oxygen is a significant toxicant to all life, but its accumulation in the atmosphere also enabled the successful development and proliferation of many aerobic organisms, especially metazoans. The currently favored dating of the Great Oxidation Event is based on the geochemical rock record. Similarly, the advent of cyanobacteria is also often drawn from the same estimates because in older rocks paleontological evidence is scarce or has been discredited. Efforts to obtain molecular evolutionary alternatives have offered widely divergent estimates. Our analyses provide a novel means to circumvent these limitations and allow us to estimate the large time gap between the two events.

Loss of Filamentous Multicellularity in Cyanobacteria: the Extremophile Gloeocapsopsis sp. Strain UTEX B3054 Retained Multicellular Features at the Genomic and Behavioral Levels

“…Cyanobacteria represent one of the few prokaryotic phyla in which multicellularity evolved. Trait evolution analyses have shown that the earliest linages of Cyanobacteria were unicellular and the emergence of filamentous multicellular representatives occurred very early in the evolution of Cyanobacteria (2,(9)(10)(11)(12)(13). Among other characters, such transition required the emergence of a coordinated assembly of cells, cell-to-cell adhesion and intercellular communication leading to a coordinated activity (2,(14)(15)(16)(17).…”

Biological Soil Crusts as Modern Analogs for the Archean Continental Biosphere: Insights from Carbon and Nitrogen Isotopes

“…Indirect evidence for the presence of an Archean phototrophic biosphere is based on sedimentological observations of paleosols (3.0-3.2 Ga; Retallack et al, 2016) and geochemical arguments suggesting that microorganisms capable of photosynthesis colonized Archean continents prior to the Great Oxidation Event (e.g., Lalonde and Konhauser, 2015;Havig et al, 2019). An early timeline for land colonization, between 3.05 and 2.78 Ga, is also suggested by ancestral state 4 reconstruction and relaxed molecular clock analyses of cyanobacterial diversification (Blank and Sanchez-Baracaldo, 2010;Uyeda et al, 2016;Garcia-Pichel et al, 2019).…”

Analysis of molecular diversity within single cyanobacterial colonies from environmental samples

“…Cyanobacteria are a very special group of gram-negative prokaryotes. Because they developed the ability to use water as an electron donor in oxygenic photosynthesis, approximately 3.6 billion years ago 1 , they played an important role in the evolution of life on Earth, the subsequent generation of molecular O 2, and the oxygenation of the atmosphere 2 . Cyanobacteria are also the ancestors of chloroplasts 3 , 4 .…”