Chlorophyll-based phototrophy is performed using quinone and/or Fe-S type reaction centers. Unlike oxygenic phototrophs, where both reaction center classes are used in tandem as Photosystem II and Photosystem I, anoxygenic phototrophs use only one class of reaction center, termed Type II (RCII) or Type I (RCI) reaction centers, separately for phototrophy. Here we report the cultivation and characterization of a filamentous anoxygenic phototroph within the Chloroflexota (formerly Chloroflexi)

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... lum, provisionally named 'Candidatus Chlorohelix allophototropha', that performs phototrophy using a distinct fourth clade of RCI protein, despite placing sister taxonomically to RCII-utilizing Chloroflexota members. 'Ca. Chx. allophototropha' contains chlorosomes, uses bacteriochlorophyll c, and encodes the FMO protein like other RCI-utilizing phototrophs in the Chlorobiales and Chloracidobacterales orders. 'Ca. Chx. allophototropha' also encodes the potential for carbon fixation using the Calvin-Benson-Bassham (CBB) cycle, unlike all known RCI-utilizing phototrophs. The discovery of 'Ca. Chx. allophototropha', as the first representative of a novel Chloroflexota order (i.e., 'Ca. Chloroheliales'), sheds light on longstanding questions about the evolution of photosynthesis, including the origin of chlorosomes among RCII-utilizing Chloroflexota members. The Chloroflexota is now the only phylum outside the Cyanobacteria containing genomic potential for both quinone and Fe-S type reaction centers and can thus serve as an additional system for exploring fundamental questions about the evolution of photosynthesis.