Abstract
Life originated in Archaean oceans, almost 4 billion years ago, in the absence of oxygen and the presence of high dissolved iron concentrations. Early Earth oxidation is marked globally by extensive banded iron formations but the contributing processes and timing remain controversial. Very few aquatic habitats have been discovered that match key physico-chemical parameters of the early Archaean Ocean. All previous whole ecosystem Archaean analogue studies have been confined to rare, low sulfur, and permanently stratified lakes. Here we provide first evidence that millions of Boreal Shield lakes with natural anoxia offer the opportunity to constrain biogeochemical and microbiological aspects of early Archaean life. Specifically, we combined novel isotopic signatures and nucleic acid sequence data to examine processes in the anoxic zone of stratified boreal lakes that are naturally low in sulfur and rich in ferrous iron, hallmark characteristics predicted for the Archaean Ocean. Anoxygenic photosynthesis was prominent in total water column biogeochemistry, marked by distinctive patterns in natural abundance isotopes of carbon, nitrogen, and iron. These processes are robust, returning reproducibly after water column re-oxygenation following lake turnover. Evidence of coupled iron oxidation, iron reduction, and methane oxidation affect current paradigms of both early Earth and modern aquatic ecosystems.
Highlights
Ancient oceans on Earth were rich in iron, low in sulfur, and free of oxygen
Photoferrotrophy could be responsible for a large part of early Earth oxidation leading to the mixed iron oxidation states that have proven difficult to explain in globally occurring banded iron formations (BIFs), deposited when oxygen was still absent from the atmosphere[4,5]
Our results provide first evidence for potential photoferrotrophy in Boreal Shield lakes, showing how distinct isotopic and chemical indicators can be used to prospect for corresponding microbial consortia
Summary
Ancient oceans on Earth were rich in iron, low in sulfur, and free of oxygen. Oxidation of Earth’s early oceans and atmosphere, concurrent with the early evolution of life and onset of photosynthesis, has long fostered intense scientific debate. In a pioneering whole ecosystem study in Lake Matano, Indonesia, large populations of photosynthetic green sulfur bacteria (GSB) were found just below the permanent chemocline at 120 metres depth, including a close relative of Chlorobium ferrooxidans, a known photoferrotroph[3] This bacterium uses light to fix inorganic carbon, with reduced iron (Fe2+) as the electron donor, thereby producing oxidized iron: Fe2+ + HCO3− + 10 H2O →hv CH2O + 4 Fe(OH)3 + 7 H+. No other examples of such microbial consortia in natural aquatic systems have yet been reported All of these systems are meromictic and have low sulfate and high iron due to their origins as volcanic craters or rift lakes. We test the hypothesis that the bottom anoxic layers of seasonally stratified lakes on the Boreal Shield could provide modern in situ laboratories for advancing the scientific understanding of microbial metabolic pathways in both the Archaean Ocean and in modern lake environments
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