Thermophilic Dehalococcoidia with unusual traits shed light on an unexpected past

Abstract The phylum Chloroflexota is ubiquitous; however, its biology and evolution are poorly understood due to limited cultivability. Here, we isolated two motile, thermophilic bacteria from hot spring sediments belonging to the class Dehalococcoidia within the phylum Chloroflexota. A combination of cryo-electron tomography, exometabolomics, and cultivation experiments using stable isotopes of carbon revealed three unusual traits: flagellar motility; a peptidoglycan-containing cell envelope; and heterotrophic activity on aromatics and plant-associated compounds. Although these traits are unusual among cultivated Chloroflexota and Dehalococcoidia, ancestral character state reconstructions showed flagellar motility and peptidoglycan-containing cell envelopes were ancestral within the Dehalococcoidia and subsequently lost prior to a major adaptive radiation of Dehalococcoidia into marine environments. This evolutionary past explains the widespread genomic potential to degrade terrestrial organic matter among marine Dehalococcoidia and raises new questions about the timing and selective forces driving their successful niche expansion into the global oceans.