Energetic constraints on life in deep marine sediments

Microorganisms are abundant in deep-sea sediments, but what percentage of cells is active, how fast do they grow, and what factors control their diversity and population size? Geochemical modelling of redox reaction energetics can help in answering these questions. Calculations of Gibbs energies reveal which reactions are thermodynamically possible, but they also highlight which geochemical variables (e.g., temperature, pressure, pH, composition) may control microbial activity and how the amount and type of biomass are affected by energy limitations. We will discuss recent results from sediment cores collected at the Peru Margin (active continental shelf with high primary productivity and significant organic matter accumulation), the South Pacific Gyre (ultra-slow sedimentation rate and low organic carbon content), and the Juan de Fuca Ridge flank (high rate of sedimentation influenced by hydrothermal circulation). However, this approach to evaluating bioenergetic potential and predicting microbial activity can be applied to any environment where the geochemistry is well characterized, even if microbiology data have not been collected. When Gibbs energies are calculated on a basis of per mole of electrons transferred (as is commonly done), aerobic oxidation of hydrogen and organic matter in South Pacific Gyre sediments is the most exergonic. Based on this, one might posit that the fastest catabolic rates and the largest biomass would be found there. However, cell counts at Juan de Fuca and the Peru Margin are several orders of magnitude higher. When recast as energy densities (in J per cm3 of sediment), we observe far more energy available in sediments at Juan de Fuca and the Peru Margin than at those in the South Pacific Gyre. We also note that the identity of the most exergonic reaction changes with depth, suggesting corresponding changes in the microbial community structure. The thermodynamic approach used here for energy supply can also be used for energy demand, including the often-considered minimum or threshold energy, also referred to as the biological energy quantum. Based on this energetic minimum theory, many reactions cannot support microbial communities because their energy yield is apparently too low. However, we show that when evaluated as energy densities, some energetically ';impossible' catabolisms become ';possible' and vice versa.