Photoferrotrophy and Fe-cycling in a freshwater column

Emerging evidence shows that ferruginous (anoxic and iron-rich) conditions dominated ocean chemistry throughout the first 3.5 billion years of the Earth’s evolution. Modern ferruginous water masses are rare, but detailed examination of these oddities, especially of the photoferrotrophic microbes developing there, could yield important insights into the early evolution of life on Earth and its impact on global element cycles.Here, we describe an abundant microbial community of pelagic photoferrotrophic and Fe-reducing microbes in a ferruginous freshwater basin in East Africa (Kabuno Bay, DR Congo). The application of culture–dependent and –independent techniques allowed the identification of active photoferrotrophic microbes genetically similar to laboratory cultures of Chlorobium ferrooxidans, the only member of the Chlorobi previously known to conduct photoferrotrophy. The Kabuno Bay photoferrotrophic Green Sulfur Bacteria (GSB) community ranged between the 16.2% and the 38.3% of the entire bacterial community retrieved by 454 pyrotag analyses of the euphotic Fe-rich chemocline of Kabuno bay. The maximum in GSB population size coincided with high rates of ferrous Fe oxidation and thymidine uptake. Approximately the 33% of depth-integrated thymidine incorporation is carried out at the depths where photoferrotrophic GSB dominate. Bacterial groups involved in methanogenesis were also recovered from the upper oxic-anoxic transition zone, but in contrast to the GSB community, other microorganisms typically implicated in the sulfur cycle were only present at low relative abundances. Reactive iron oxides, however, are exhausted within the chemocline and excess organic matter is thus channelled through mineralization by methanogenesis directly in the water column.Our study documents for the first time that photoferrotrophs microbes, together with other microbes yielding a full Fe cycle, are suited to pelagic environments. Fe oxides, however, are not completely reduced in the anoxic water column, with substantial organic carbon mineralization also channelled through methanogenesis. Thus, ferric iron is exported to the sediments as was also true in the ancient Banded Iron Formations. In this way, photoferrotrophs could contribute to the overall oxidation of the Earth’s surface prior to the oxygenation of the atmosphere.