Recycling of archaeal biomass as a new strategy for extreme life in Dead Sea deep sediments

Abstract

Archaea and Bacteria that inhabit the deep subsurface (known as the deep biosphere) play a prevalent role in the recycling of sedimentary organic carbon. In such environments, this process can occur over millions of years and requires microbial communities to cope with extremely limited sources of energy. Because of this scarcity, metabolic processes come at a high energetic cost, but the ways heterotrophic microbial communities develop to minimize energy expenses for a maximized yield remain unclear. Here, we report molecular biomarker evidence for the recycling of archaeal cell wall constituents in extreme evaporitic facies of Dead Sea deep sediments. Wax esters derived from the recombination of hydrolyzed products of archaeal membrane lipids were observed in gypsum and/or halite sedimentary deposits down to 243 m below the lake floor, implying the reutilization of archaeal necromass possibly by deep subsurface bacteria. By recycling the building blocks of putatively better-adapted archaea, heterotrophic bacteria may build up intracellular carbon stocks and mitigate osmotic stress in this energy-deprived environment. This mechanism illustrates a new pathway of carbon transformation in the subsurface and demonstrates how life can be maintained in extreme environments characterized by long-term isolation and minimal energetic resources.