Pelagic photoferrotrophy and iron cycling in a modern ferruginous basin

Iron-rich (ferruginous) ocean chemistry prevailed throughout most of Earth’s early history. Before
the evolution and proliferation of oxygenic photosynthesis, biological production in the ferruginous
oceans was likely driven by photoferrotrophic bacteria that oxidize ferrous iron {Fe(II)} to harness
energy from sunlight, and fix inorganic carbon into biomass. Photoferrotrophs may thus have fuelled
Earth’s early biosphere providing energy to drive microbial growth and evolution over billions of
years. Yet, photoferrotrophic activity has remained largely elusive on the modern Earth, leaving
models for early biological production untested and imperative ecological context for the evolution
of life missing. Here, we show that an active community of pelagic photoferrotrophs comprises up
to 30% of the total microbial community in illuminated ferruginous waters of Kabuno Bay (KB), East
Africa (DR Congo). These photoferrotrophs produce oxidized iron {Fe(III)} and biomass, and support
a diverse pelagic microbial community including heterotrophic Fe(III)-reducers, sulfate reducers,
fermenters and methanogens. At modest light levels, rates of photoferrotrophy in KB exceed
those predicted for early Earth primary production, and are sufficient to generate Earth’s largest
sedimentary iron ore deposits. Fe cycling, however, is efficient, and complex microbial community
interactions likely regulate Fe(III) and organic matter export from the photic zone.