Oxygenation of Earth's atmosphere induced metabolic and ecologic transformations recorded in the Lomagundi-Jatuli carbon isotopic excursion.

ABSTRACT

The oxygenation of Earth's atmosphere represents the quintessential transformation of a planetary surface by microbial processes. In turn, atmospheric oxygenation transformed metabolic evolution; molecular clock models indicate the diversification and ecological expansion of respiratory metabolisms in the several hundred million years following atmospheric oxygenation. Across this same interval, the geological record preserves 13C enrichment in some carbonate rocks, called the Lomagundi-Jatuli excursion (LJE). By combining data from geologic and genomic records, a self-consistent metabolic evolution model emerges for the LJE. First, fermentation and methanogenesis were major processes remineralizing organic carbon before atmospheric oxygenation. Once an ozone layer formed, shallow water and exposed environments were shielded from UVB/C radiation, allowing the expansion of cyanobacterial primary productivity. High primary productivity and methanogenesis led to preferential removal of 12C into organic carbon and CH4. Extreme and variable 13C enrichments in carbonates were caused by 13C-depleted CH4 loss to the atmosphere. Through time, aerobic respiration diversified and became ecologically widespread, as did other new metabolisms. Respiration displaced fermentation and methanogenesis as the dominant organic matter remineralization processes. As CH4 loss slowed, dissolved inorganic carbon in shallow environments was no longer highly 13C enriched. Thus, the loss of extreme 13C enrichments in carbonates marks the establishment of a new microbial mat ecosystem structure, one dominated by respiratory processes distributed along steep redox gradients. These gradients allowed the exchange of metabolic by-products among metabolically diverse organisms, providing novel metabolic opportunities. Thus, the microbially induced oxygenation of Earth's atmosphere led to the transformation of microbial ecosystems, an archetypal example of planetary microbiology.IMPORTANCEThe oxygenation of Earth's atmosphere represents the most extensive known chemical transformation of a planetary surface by microbial processes. In turn, atmospheric oxygenation transformed metabolic evolution by providing oxidants independent of the sites of photosynthesis. Thus, the evolutionary changes during this interval and their effects on planetary-scale biogeochemical cycles are fundamental to our understanding of the interdependencies among genomes, organisms, ecosystems, elemental cycles, and Earth's surface chemistry through time.