Abstract
Biological N2 fixation was key to the expansion of life on early Earth. The N2-fixing microorganisms and the nitrogenase type used in the Proterozoic are unknown, although it has been proposed that the canonical molybdenum-nitrogenase was not used due to low molybdenum availability. We investigate N2 fixation in Lake Cadagno, an analogue system to the sulfidic Proterozoic continental margins, using a combination of biogeochemical, molecular and single cell techniques. In Lake Cadagno, purple sulfur bacteria (PSB) are responsible for high N2 fixation rates, to our knowledge providing the first direct evidence for PSB in situ N2 fixation. Surprisingly, no alternative nitrogenases are detectable, and N2 fixation is exclusively catalyzed by molybdenum-nitrogenase. Our results show that molybdenum-nitrogenase is functional at low molybdenum conditions in situ and that in contrast to previous beliefs, PSB may have driven N2 fixation in the Proterozoic ocean.
Highlights
Biological N2 fixation was key to the expansion of life on early Earth
For the Proterozoic ocean, it is often assumed that cyanobacteria performing oxygenic photosynthesis were the key primary producers and N2-fixers[19], direct evidence linking cyanobacteria to ancient ocean N-input is lacking
In August 2018, the chemocline of Lake Cadagno was situated between 13.5 m and 14.5 m water depth (Fig. 1), which is consistent with previous observations for this season in recent years[36]
Summary
Biological N2 fixation was key to the expansion of life on early Earth. The N2-fixing microorganisms and the nitrogenase type used in the Proterozoic are unknown, it has been proposed that the canonical molybdenum-nitrogenase was not used due to low molybdenum availability. We investigate the organisms responsible for N2 fixation and the nitrogenase types used in the anoxic, low Mo chemocline of Lake Cadagno, by combining natural abundance isotope measurements with stable isotope incubations, metagenomics, metatranscriptomics, and single-cell analyses. To assess which of the potential N2-fixers identified in the metagenome from 2014 could be involved in active N2 fixation in the chemocline of Lake Cadagno, metatranscriptomes from our study in 2018 were sequenced.
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