Abbreviations used throughout text: Chl. = Chlorobium; Cba. = Chlorobaculum; Che. = 15 Chloroherpeton; Ptc. = ProsthecochlorisThe authors declare no competing financial interests. Abstract 20Photoferrotrophy, the direct photosynthetic oxidation of ferrous iron, is thought to have contributed to primary production within Earth's early anoxic oceans yet is presumed to be of little modern environmental relevance. Here we use genome-resolved metagenomics and enrichment cultivation to provide first functional gene evidence that photoferrotrophic bacteria are important photoautotrophs in the anoxic water columns of globally abundant Boreal Shield 25 lakes. We recovered six high-completeness, low-contamination draft genome bins belonging to the Chlorobia class. Half of these genome bins contained the cyc2 candidate gene marker for iron oxidation, and one containing cyc2 lacked the sulfur oxidation gene pathway altogether. Using a custom profile Hidden Markov Model, we recovered distinct cyc2 homologues from our metagenome data and doubled the known diversity of Chlorobia-associated cyc2 genes. 30Metagenome data also showed that potential photoferrotrophs co-occurred with sulfide-oxidizing populations of Chlorobia in one lake but that only sulfide-oxidizing populations were present in a neighboring lake, implying that strong ecological controls govern the favourability of photoferrotrophy in ferruginous lakes. Our results greatly expand knowledge of photoferrotroph ecology in natural aquatic systems, demonstrating modern environmental relevance for this iron-35 oxidizing photosynthetic mode and supporting future investigations into early Earth microbial communities. expands capabilities to explore the role of photoferrotrophy and other forms of iron cycling in nature.Additional photoferrotrophic bacteria are also being isolated in the laboratory. For example, among the Chlorobia class (i.e., "green sulfur bacteria"), the only known photoferrotroph was 65Chlorobium ferrooxidans strain KoFox, which was enriched from freshwater lake sediments [18].Recently, two additional Chlorobia-associated photoferrotrophs were cultivated. Chlorobium phaeoferrooxidans strain KB01, a bacteriochlorophyll e-containing member of the Chlorobia, was isolated from the anoxic water column of the meromictic and ferruginous Kabuno Bay (see below; [19]). In addition, Chlorobium sp. strain N1 was isolated from marine sediments [20]. 70Both Chl. ferrooxidans and Chl. phaeoferrooxidans oxidize ferrous iron as their sole photosynthetic electron donor, assimilating sulfur as sulfate [18,19]. Chl. sp. N1 is capable of oxidizing either ferrous iron or sulfide as the photosynthetic electron donor [20].Phylogenetically, Chl. ferrooxidans and Chl. phaeoferrooxidans are sister groups to one another, whereas Chl. sp. N1 is closely related to Chl. luteolum, a sulfide-oxidizing species of Chlorobia 75 with genomic potential for photoferrotrophy [19][20][21]. Draft genome sequences available for Chl. ferrooxidans, Chl. phaeoferrooxidans, and Chl. sp. N1 show that...
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