Abstract
Precambrian Banded Iron Formation (BIF) deposition was conventionally attributed to the precipitation of iron-oxides resulting from the abiotic reaction of ferrous iron (Fe(II)) with photosynthetically produced oxygen. Earliest traces of oxygen date from 2.7 Ga, thus raising questions as to what may have caused BIF precipitation before oxygenic photosynthesis evolved. The discovery of anoxygenic phototrophic bacteria thriving through the oxidation of Fe(II) has provided support for a biological origin for some BIFs, but despite reports suggesting that anoxygenic phototrophs may oxidize Fe(II) in the environment, a model ecosystem of an ancient ocean where they are demonstrably active was lacking. Here we show that anoxygenic phototrophic bacteria contribute to Fe(II) oxidation in the water column of the ferruginous sulfate-poor, meromictic lake La Cruz (Spain). We observed in-situ photoferrotrophic activity through stimulation of phototrophic carbon uptake in the presence of Fe(II), and determined light-dependent Fe(II)-oxidation by the natural chemocline microbiota. Moreover, a photoferrotrophic bacterium most closely related to Chlorobium ferrooxidans was enriched from the ferruginous water column. Our study for the first time demonstrates a direct link between anoxygenic photoferrotrophy and the anoxic precipitation of Fe(III)-oxides in a ferruginous water column, providing a plausible mechanism for the bacterial origin of BIFs before the advent of free oxygen. However, photoferrotrophs represent only a minor fraction of the anoxygenic phototrophic community with the majority apparently thriving by sulfur cycling, despite the very low sulfur content in the ferruginous chemocline of Lake La Cruz.
Highlights
The chemistry of the anoxic Archean ocean was characterized by a low sulfate content and high concentrations of ferrous iron (Fe(II)) of probable hydrothermal origin (Holland, 1973; Anbar and Knoll, 2002; Canfield, 2005)
The evolution of photosynthesis is complex with horizontal gene transfer playing an important role, it is accepted that anoxygenic phototrophic bacteria evolved before oxygen-producing cyanobacteria (Xiong et al, 2000; Raymond et al, 2003)
Light intensity was measured as photosynthetically active radiation (PAR) scalar irradiance with a flat Li-Cor Quantum Sensor (Li 192 SA), which was vertically mounted on a lowering frame and connected to a LiCor data logger (L-1000)
Summary
The chemistry of the anoxic Archean ocean was characterized by a low sulfate content and high concentrations of ferrous iron (Fe(II)) of probable hydrothermal origin (Holland, 1973; Anbar and Knoll, 2002; Canfield, 2005) From this ferruginous water column, alternating sedimentary deposits of iron oxide minerals and silica precipitated between 3.8 and 1.8 Ga ago (Anbar and Knoll, 2002) and became preserved in the geological record as Banded Iron Formations (BIF). The presence of green anoxygenic phototrophic bacteria in the water column of a late Archean Ocean analog www.frontiersin.org
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