Potential recycling of thaumarchaeotal lipids by DPANN Archaea in seasonally hypoxic surface marine sediments

Abstract

Thaumarchaeota synthesize specific glycerol dibiphytanyl glycerol tetraethers (GDGTs), the distribution of which is affected by temperature, thereby forming the basis of the paleotemperature proxy, TEX86. Lipids in marine surface sediments are believed to be derived mainly from pelagic Thaumarchaeota; however, some studies have evaluated the possibility that benthic Archaea also contribute to the lipid fossil record. Here, we compared the archaeal abundance and composition from DNA-based methods with the archaeal intact polar lipid (IPL) diversity in surface sediments of a seasonally hypoxic marine lake to determine the potential biological sources of the sedimentary archaeal IPLs under changing environmental conditions. The archaeal community changed from March (oxic conditions) to August (euxinic) from a Thaumarchaeota-dominated community (up to 82%) to an archaeal community dominated by the DPANN super phylum (up to 95%). This marked change coincided with a one order of magnitude decrease in the total IPL-GDGT abundance. In addition, IPL-GDGTs with a glyco polar head group increased. This may indicate a transition to Thaumarchaeota growing in stationary phase or selective preservation of the GDGT pool. In addition, considering the apparent inability of the DPANN Archaea to synthesize their own membrane lipids, we hypothesize that the dominant DPANN Archaea population present in August use the lipids synthesized previously by the Thaumarchaeota or other Archaea to form their own cell membranes, which would indicate an active recycling of fossil IPLs in the marine surface sediment.