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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 extreme environment, this process can occur over millions of years1 and requires microbial communities to cope with limited sources of energy. Because of this scarcity, metabolic processes come at a high energetic cost, but the ways heterotrophic microbial communities develop to enable the least energy expenses for a maximized yield remain unclear. Here, we report molecular biomarker evidence for the recycling of archaeal cell wall constituents by bacteria in extreme evaporitic facies of the Dead Sea deep sediments. Isoprenoid wax esters (WE) derived from the recombination of hydrolyzed products of archaeal membrane lipids were retrieved in gypsum and/or halite sedimentary deposits down to 243 meters below the lake floor (mblf), implying the reutilization of archaeal necromass by deep subsurface bacteria. By recycling the building blocks of allegedly better adapted archaea, heterotrophic bacteria build up intracellular carbon stocks and gain access to free water in this deprived environment. This strategy illustrates a new pathway of carbon transformation in the subsurface and how life is maintained in extreme environments experiencing long-term isolation and minimal energetic resources.

The hypersaline Dead Sea and its sediments are natural laboratories for studying extremophile microorganism habitat response to environmental change. In modern times, increased freshwater runoff to the lake surface waters resulted in stratification and dilution of the upper water column followed by microbial blooms. However, whether these events facilitated a microbial response in the deep lake and sediments is obscure. Here we investigate archived evidence of microbial processes and changing regional hydroclimate conditions by reconstructing deep Dead Sea chemical compositions from pore fluid major ion concentration and stable S, O, and C isotopes, together with lipid biomarkers preserved in the hypersaline deep Dead Sea ICDP-drilled core sediments dating to the early Holocene (ca. 10,000 years BP). Following a significant negative lake water balance resulting in salt layer deposits at the start of the Holocene, there was a general period of positive net water balance at 9500-8300 years BP. The pore fluid isotopic composition of sulfate exhibit evidence of intensified microbial sulfate reduction, where both δ34S and δ18O of sulfate show a sharp increase from estimated base values of 15.0‰ and 13.9‰ to 40.2‰ and 20.4‰, respectively, and a δ34S vs. δ18O slope of 0.26. The presence of the n-C17 alkane biomarker in the sediments suggests an increase of cyanobacteria or phytoplankton contribution to the bulk organic matter that reached the deepest parts of the Dead Sea. Although hydrologically disconnected, both the Mediterranean Sea and the Dead Sea microbial ecosystems responded to increased freshwater runoff during the early Holocene, with the former depositing the organic-rich sapropel 1 layer due to anoxic water column conditions. In the Dead Sea prolonged positive net water balance facilitated primary production and algal blooms in the upper waters and intensified microbial sulfate reduction in the hypolimnion and/or at the sediment-brine interface.