Anoxygenic phototrophic Chloroflexota member uses a Type I reaction center

Abstract

Scientific 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 the Chloroflexota phylum 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-utilizing Chloroflexota members. Despite using different reaction centers, our phylogenomic data provide strong evidence that RCI- and RCII-utilizing Chloroflexia members 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. The Chloroflexota phylum 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.