Pulses of labile carbon cause transient decoupling of fermentation and respiration in permeable sediments

Dihydrogen (H₂) is an important intermediate in anaerobic microbial processes, and concentrations are tightly controlled by thermodynamic limits of consumption and production. However, recent studies reported unusual H₂ accumulation in permeable marine sediments under anoxic conditions, suggesting decoupling of fermentation and sulfate reduction, the dominant respiratory process in anoxic permeable marine sediments. Yet, the extent, prevalence and potential triggers for such H₂ accumulation and decoupling remain unknown. We surveyed H₂ concentrations in situ at different settings of permeable sand and found that H₂ accumulation was only observed during a coral spawning event on the Great Barrier Reef. A flume experiment with organic matter addition to the water column showed a rapid accumulation of hydrogen within the sediment. Laboratory experiments were used to explore the effect of oxygen exposure, physical disturbance and organic matter inputs on H₂ accumulation. Oxygen exposure had little effect on H₂ accumulation in permeable sediments suggesting both fermenters and sulfate reducers survive and rapidly resume activity after exposure to oxygen. Mild physical disturbance mimicking sediment resuspension had little effect on H₂ accumulation; however, vigorous shaking led to a transient accumulation of H₂ and release of dissolved organic carbon suggesting mechanical disturbance and cell destruction led to organic matter release and transient decoupling of fermenters and sulfate reducers. In summary, the highly dynamic nature of permeable sediments and its microbial community allows for rapid but transient decoupling of fermentation and respiration after a C pulse, leading to high H₂ levels in the sediment.