Chloroflexi are widespread in energy-limited subseafloor sediments, but how Chloroflexi respond to subseafloor energy limitation under oxic and anoxic conditions is poorly understood. Here, we characterize the diversity, abundance, activity, and metabolic potential of Chloroflexi in oxic and anoxic abyssal clay from three deep-sea cores covering up to 15 million years of sediment deposition, where Chloroflexi are a major component of the community throughout the entire cored sequence at all

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... s. In oxic red clay at two different sites, Chloroflexi communities exhibit net death over both 10-15 million year cored sequences, and gene expression was below detection despite the availability of oxygen as a high energy electron acceptor, indicating a reduced level of activity. In contrast at the anoxic site, Chloroflexi abundance and gene expression increase below the seafloor and peak in 2 to 3 million year old sediment. The anaerobic subseafloor Chloroflexi exhibited a homoacetogenic metabolism and potential for energetically efficient intracellular H2 recycling that have been proposed to confer a fitness advantage in energy-limited subseafloor habitats. Our findings indicate that the expression of this energy efficient metabolism in Chloroflexi coincides with net growth over million year timescales in deep-sea anoxic clay.