Physiological limits to life in anoxic subseafloor sediment

Abstract

In subseafloor sediment, microbial cell densities exponentially decrease with depth into the fermentation zone. Here, we address the classical question of 'why are cells dying faster than they are growing?' from the standpoint of physiology. The stoichiometries of fermentative ATP production and consumption in the fermentation zone place bounds on the conversion of old cell biomass into new. Most fermentable organic matter in deep subseafloor sediment is amino acids from dead cells because cells are mostly protein by weight. Conversion of carbon from fermented dead cell protein into methanogen protein via hydrogenotrophic and acetoclastic methanogenesis occurs at ratios of ~200:1 and 100:1, respectively, while fermenters can reach conversion ratios approaching 6:1. Amino acid fermentations become thermodynamically more efficient at lower substrate and product concentrations, but the conversion of carbon from dead cell protein into fermenter protein is low because of the high energetic cost of translation. Low carbon conversion factors within subseafloor anaerobic feeding chains account for exponential declines in cellular biomass in the fermentation zone of anoxic sediments. Our analysis points to the existence of a life-death transition zone in which the last biologically catalyzed life processes are replaced with purely chemical reactions no longer coupled to life.