Early anaerobic metabolisms

Abstract

Before the advent of oxygenic photosynthesis, the biosphere was driven by anaerobic metabolisms. We catalogue and quantify the source strengths of the most probable electron donors and electron acceptors that would have been available to fuel early-Earth ecosystems. The most active ecosystems were probably driven by the cycling of H2 and Fe2+ through primary production conducted by anoxygenic phototrophs. Interesting and dynamic ecosystems would have also been driven by the microbial cycling of sulphur and nitrogen species, but their activity levels were probably not so great. Despite the diversity of potential early ecosystems, rates of primary production in the early-Earth anaerobic biosphere were probably well below those rates observed in the marine environment. We shift our attention to the Earth environment at 3.8Gyr ago, where the earliest marine sediments are preserved. We calculate, consistent with the carbon isotope record and other considerations of the carbon cycle, that marine rates of primary production at this time were probably an order of magnitude (or more) less than today. We conclude that the flux of reduced species to the Earth surface at this time may have been sufficient to drive anaerobic ecosystems of sufficient activity to be consistent with the carbon isotope record. Conversely, an ecosystem based on oxygenic photosynthesis was also possible with complete removal of the oxygen by reaction with reduced species from the mantle.

Figure 1

Early-Earth microbial ecosystem driven by hydrogen-based anoxygenic photosynthesis. The primary sources of hydrogen are subaqueous and subaerial volcanoes. The organic matter produced by photosynthesis is decomposed by methanogenesis, a fraction of which, x, is buried in sediments. Methane is reconverted to hydrogen by photolysis reactions in the atmosphere. See text for details.

Figure 2

Early-Earth microbial ecosystem driven by hydrogen-based methanogenesis. Similar to the case outlined in figure 1, the primary sources of hydrogen are subaqueous and subaerial volcanoes. The organic matter is produced as methanogen cell biomass with the growth yield, y. Organic matter is decomposed by methanogenesis, a fraction of which, x, is buried in sediments. Methane is reconverted to hydrogen by photolysis reactions in the atmosphere. See text for details.

Figure 3

The early-Earth sulphur cycle. Sulphide enters the cycle from a number of sources including mid-ocean ridge hydrothermal systems, terrestrial hydrothermal systems and volcanic emanations. The sulphide coming from mid-ocean ridge systems would have likely precipitated as iron sulphide minerals in an iron-containing ocean. The sulphur species coming from subaerial volcanics would have been converted to a mix of reaction products through photolysis reactions in the atmosphere.

Figure 4

The sulphur cycle associated with a sulphuretum. Hydrothermal sulphide is oxidized by anoxygenic phototrophs producing sulphate. As the microbial mat accretes, organic matter buried below the photic zone will be oxidized by sulphate reduction, recycling the sulphate produced by photosynthesis. Some methanogenesis is also likely to occur, and anaerobic methane oxidation would have occurred at the sulphate–methane transition zone.

Figure 5

The early-Earth cycle of elemental sulphur. Elemental sulphur would have been produced by the photolysis of SO₂ gas. The sulphur would have settled into the ocean, some of which would have been oxidized by anoxygenic phototrophs. Some sulphur might also have settled below the euphotic zone into iron-containing waters, where sulphur reduction and sulphur disproportionation would have occurred.

Figure 6

The early-Earth iron cycle. Iron would have entered the oceans from continental weathering (although this may not have been a major source, see text) and mid-ocean ridge hydrothermal vents. The iron within the ocean would have been oxidized by anoxygenic phototrophs producing iron oxides and organic matter. The organic matter and iron oxides would have settled into the deep ocean, with iron reduction reducing the iron oxides and oxidizing the organic matter. Subduction and metamorphism would have regenerated reduced iron.

Figure 7

The early-Earth nitrogen cycle. NO would have been produced by lightning, and settled into the oceans where nitrate and nitrite would have formed. Nitrate and nitrite would have been used in both the denitrification and the anammox reaction. Anammox is a source of primary production, where the ammonia would have come from hydrothermal vents.