Redox-dependent niche differentiation provides evidence for multiple bacterial sources of glycerol tetraether lipids in lakes

Terrestrial paleoclimate archives such as lake sediments are essential for our understanding of the continental climate system and for the modeling of future climate scenarios. However, quantitative proxies for the determination of paleotemperatures are sparse. The relative abundances of certain bacterial lipids, i.e., branched glycerol dialkyl glycerol tetraethers (brGDGTs), respond to changes in environmental temperature, and thus have great potential for climate reconstruction. Their application to lake deposits, however, is hampered by the lack of fundamental knowledge on the ecology of brGDGT-producing microbes in lakes. Here, we show that brGDGTs are synthesized by multiple groups of bacteria thriving under contrasting redox regimes in a deep meromictic Swiss lake (Lake Lugano). This niche partitioning is evidenced by highly distinct brGDGT inventories in oxic vs. anoxic water masses, and corresponding vertical patterns in bacterial 16S rRNA gene abundances, implying that sedimentary brGDGT records are affected by temperature-independent changes in the community composition of their microbial producers. Furthermore, the stable carbon isotope composition (δ(13)C) of brGDGTs in Lake Lugano and 34 other (peri-)Alpine lakes attests to the widespread heterotrophic incorporation of (13)C-depleted, methane-derived biomass at the redox transition zone of mesotrophic to eutrophic lake systems. The brGDGTs produced under such hypoxic/methanotrophic conditions reflect near-bottom water temperatures, and are characterized by comparatively low δ(13)C values. Depending on climate zone and water depth, lake sediment archives predominated by deeper water/low-(13)C brGDGTs may provide more reliable records of climate variability than those where brGDGTs derive from terrestrial and/or aquatic sources with distinct temperature imprints.