Type I photosynthetic reaction center in an anoxygenic phototrophic member of the Chloroflexota

Abstract

SummaryPhototrophic members of the Chloroflexota phylum are enigmas in the evolution of phototrophy. Although all previously characterized phototrophic Chloroflexota members use a Type II reaction center (RCII) to perform light energy conversion1,2, many members host chlorosomes, a light-harvesting apparatus only otherwise reported among Type I reaction center (RCI)-containing phototrophs3. Here we report the discovery and cultivation of “Candidatus Chlorohelix allophototropha”, the first known member of the Chloroflexota to use RCI, rather than RCII, for phototrophy. Cultivated from an iron-rich Boreal Shield lake, “Ca. Chx. allophototropha” cells contain chlorosomes and encode a novel fifth clade of RCI protein. Phylogenomic data demonstrate that “Ca. Chx. allophototropha” shares closest ancestry to RCII-utilizing relatives for multiple photosynthesis accessory genes, including chlorosomes. Thus, we propose that the enigmatic distribution of chlorosomes in the Chloroflexota phylum resulted from genetic interaction of RCI- and RCII-utilizing Chloroflexota members. Although undetected previously, metatranscriptome data demonstrate that RCI-utilizing Chloroflexota members can be among the most active populations in illuminated anoxic waters of Boreal Shield lakes, which number in the millions globally4. Our results establish the Chloroflexota as the only bacterial phylum containing RCI- and RCII-utilizing anoxygenic phototrophs, providing new context for understanding the origins of phototrophic life on Earth.