The Potential Role of Marine Biogenic Methane Cycling on the Early Earth Biosphere: Insights from Green Lake in Fayetteville, New York

Earth has experienced significant shifts in its ecosystems over its long history, propelled by microbial metabolic diversification in its ancient oceans. However, unraveling the contribution of the earliest forms of life to planetary evolution poses a persistent challenge because of limited physical and chemical records. Hindered by the lack of well-preserved rocks and microbial fossils from the Archean and Proterozoic Eons, ancient Earth analog sites have deepened our knowledge of early life and its co-evolving environments. Modern stratified euxinic water bodies are particularly relevant, given the evidence in the rock record that portions of the Earth's oceans were at least intermittently euxinic during the Proterozoic eon (2.5 to 0.541 Ga). Because early oxygen levels were very low, the role of biogenic methane cycling between the ocean and atmosphere as a potential regulator of atmospheric oxygen levels takes on special importance. Anaerobic methanogenesis is regarded as one of the oldest microbial metabolisms, with carbon isotope fractionation measurements and phylogenomic estimates suggesting its existence deep in Earth history during the Archean eon (4 to 2.5 Ga). As methane accumulated in the environment, it may have also facilitated the evolution of anaerobic methanotrophy. The relevance of modern analogs is elevated because of remaining uncertainties in methane’s early role in the primitive biosphere. Green Lake near Fayetteville, New York, is an exceptional analog site given its persistent anoxic/euxinic conditions and productive shallow chemocline. Using a combination of sediment and water column analysis across the chemocline, potential electron acceptors and donors (sulfur, nitrogen, iron, and carbon-species) were constrained. Relevant methane cycling metabolic rates were investigated using radiotracer techniques, specifically, incubations with 14C-methane, 14C-mono-methylamine, and 35S-sulfate were conducted ex-situ. Water column methane increased significantly below the chemocline (1.3 to 5.6 μM from 19.5 to 35m depth) and sulfate (~11.5 mM) fueled high rates of sulfate reduction (400 nmol/L/day) and methanotrophy (360 nmol/L/day). 14C-mono-methylamine incubations revealed concurrent methanogenesis below the chemocline. Microbial population analysis and visualization through Next-generation sequencing and microscopy identified the presence of aerobic and anaerobic methanotrophs, as well as methanogens and potential syntrophic sulfate-reducing partners. Methanotrophy and sulfate reduction rates decreased in the upper sediment, while sequencing indicated the presence of pertinent methane cycling organisms. The evidence examined from Green Lake supports the notion of productive biogenic methane cycling in early euxinic settings with important implications for climate regulation and biosignatures that are relevant within and beyond our solar system. Further, demonstrated involvement of symbiotic microorganisms highlights the possibility of similar pathways in modulating oxygenation of Earth's early surface oceans.