Temperature activation of organic matter and minerals during burial has the potential to sustain the deep biosphere over geological timescales

Recent research has shown that sub-surface sedimentary bacteria are widespread and that these bacteria, far from any photosynthetic energy supply, may be globally the majority of bacteria on Earth. However, it is unclear how they obtain energy over great depths and geological timescales, given that only recalcitrant organic matter would be expected to be available. We have investigated this question by conducting long term heating experiments (up to ∼500 days) with surface sediment slurries to model burial and the associated temperature increase in sub-surface sediments. In both static (thermal gradient system, 0–100°C) and sequential heating (30–90°C at different heating rates) experiments bacteria produced considerable concentrations of H2, CH4 and other hydrocarbons, as well as organic acids, thereby providing energy for themselves and other bacteria. With respect to deep sediments these compounds have previously been interpreted as being solely products of thermogenic origin, but the use of irradiated controls showed that they were predominantly of bacterial origin in the heating experiments. Even after 300 days at constant temperature (30 or 60°C) incremental heating to 90°C continuously stimulated bacterial activity, indicating temperature related activation of recalcitrant organic matter. Aromatization of organic matter is proposed as a source of the H2. Addition of magnetite to slurries at 60°C stimulated H2 production, suggesting reduction of water coupled to oxidation of the ferrous iron in magnetite. Therefore, magnetite and related iron oxide minerals may be a potential inorganic source of H2 in sub-seafloor sediments. Iron oxide minerals may, in addition, be involved in sufate formation, which also occurred above ∼60°C. Deep, hot sediments from the Nankai Trough also showed increases in acetate, H2 and sulfate, similar to the laboratory heating experiments. H2 formation at the higher temperatures in the experiments stimulated autotrophic bacterial populations and a similar situation may occur in deep sediments.