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