Tank, M.

AbstractAquatic environments with high levels of dissolved ferrous iron and low levels of sulfate serve as an important systems for exploring biogeochemical processes relevant to the early Earth. Boreal Shield lakes, which number in the tens of millions globally, commonly develop seasonally anoxic waters that become iron rich and sulfate poor, yet the iron–sulfur microbiology of these systems has been poorly examined. Here we use genome-resolved metagenomics and enrichment cultivation to explore the metabolic diversity and ecology of anoxygenic photosynthesis and iron/sulfur cycling in the anoxic water columns of three Boreal Shield lakes. We recovered four high-completeness and low-contamination draft genome bins assigned to the class Chlorobia (formerly phylum Chlorobi) from environmental metagenome data and enriched two novel sulfide-oxidizing species, also from the Chlorobia. The sequenced genomes of both enriched species, including the novel “Candidatus Chlorobium canadense”, encoded the cyc2 gene that is associated with photoferrotrophy among cultured Chlorobia members, along with genes for phototrophic sulfide oxidation. One environmental genome bin also encoded cyc2. Despite the presence of cyc2 in the corresponding draft genome, we were unable to induce photoferrotrophy in “Ca. Chlorobium canadense”. Genomic potential for phototrophic sulfide oxidation was more commonly detected than cyc2 among environmental genome bins of Chlorobia, and metagenome and cultivation data suggested the potential for cryptic sulfur cycling to fuel sulfide-based growth. Overall, our results provide an important basis for further probing the functional role of cyc2 and indicate that anoxygenic photoautotrophs in Boreal Shield lakes could have underexplored photophysiology pertinent to understanding Earth’s early microbial communities.

AbstractScientific exploration of phototrophic bacteria over nearly 200 years has revealed large phylogenetic gaps between known phototrophic groups that limit understanding of how phototrophy evolved and diversified. Through Boreal Shield lake water incubations, we cultivated an anoxygenic phototrophic bacterium from a previously unknown order within theChloroflexotaphylum that represents a highly novel transition form in the evolution of photosynthesis. Unlike all other known phototrophs, this bacterium uses a Type I reaction center (RCI) for light energy conversion yet belongs to the same bacterial phylum as organisms that use a Type II reaction center (RCII) for phototrophy. Using physiological, phylogenomic, and environmental metatranscriptomic data, we demonstrate active RCI-utilizing metabolism by the strain alongside usage of chlorosomes and bacteriochlorophylls related to those of RCII-utilizingChloroflexotamembers. Despite using different reaction centers, our phylogenomic data provide strong evidence that RCI- and RCII-utilizingChloroflexiamembers inherited phototrophy from a most recent common phototrophic ancestor that used RCI, RCII, or both reaction center classes, substantially revising our view of the diversity and evolution of phototrophic life. TheChloroflexotaphylum preserves an evolutionary record of interaction between RCI and RCII among anoxygenic phototrophs that gives new context for exploring the origins of phototrophy on Earth.