GENOMIC ANALYSES IMPLICATE KEY METABOLIC PATHWAYS FOR PELAGIC PHOTOFERROTROPHY

Photoferrotrophy is photosynthesis using divalent iron as the electron donor—it likely supported global biological production in the iron-rich (ferruginous) oceans of the Precambrian Eon. Photoferrotrophy would therefore have played a pivotal role in ocean ecology, driving the co-evolution of life and Earth surface chemistry. A handful of extant photoferrotrophs have been brought into laboratory culture, but relatively little is known about their physiology and genetics. Furthermore, all previously isolated cultures were enriched from ephemeral benthic environments, unlikely habitats for their Precambrian pelagic ancestors. To gain insight into the physiology and genetic capacity that supports pelagic photoferrotropy and to infer its evolutionary history, we isolated into axenic culture a photoferrotrophic green sulfur bacterium (GSB) from the water column of Kabuno Bay (KB), a ferruginous sub-basin of Lake Kivu in East Africa. The closest relative of the KB strain based on small subunit ribosomal RNA gene sequence similarity is Chlorobium ferrooxidans strain KoFox, a photoferrotroph enriched from a drainage ditch in Germany. Unlike strain KoFox, however, the KB strain grows without a co-culture partner, and is specifically adapted to a pelagic habitat. We also sequenced the genome of the KB strain, and at the nucleotide level, there is little similarity between strains KB and KoFox. Metabolic pathways predicted from the genome sequence were compared to the entire predicted GSB pathway space based on the 10 GSB genomes sequenced to date. This comparison reveals that the KB strain is highly enriched in open reading frames belonging to pathways related to both lipid and cofactor biosynthesis relative to other GSB. These enrichments in specific metabolic capacities relative to non-photoferrotrophic GSB implicate the biosynthetic products of these pathways in a pelagic photoferrotrophic lifestyle.