Ammonia Oxidation Rate is a Fundamental Control on Thaumarchaeal Lipid Composition and the TEX86 Proxy

Planktonic Thaumarchaeota are the ocean’s major aerobic oxidizers of ammonia and produce membrane lipids known as GDGTs. These lipids are the basis of the TEX₈₆ sea surface temperature (SST) proxy – a geochemical paleothermometer used to reconstruct SST from the Jurassic to the present. However the mechanistic underpinning of the TEX₈₆-SST proxy remains a mystery: How do GDGT lipids predict SST, when the maximum activity of Thaumarchaeota occurs below the surface mixed layer? Here we investigated the influence of ammonia oxidation rate on the distribution of GDGT lipids using isothermal studies of the model thaumarchaeon Nitrosopumilus maritimus SCM1. The results show that TEX₈₆ values scale inversely with the ammonia oxidation rate, indicating that this proxy depends on available reducing power. The TEX₈₆ ratio decreases by 5.4°C of SST-calibrated temperature over a 5.5 fmol cell^-1 day^-1 decrease in ammonia oxidation rate. Depth profiles from the marine water column show similar patterns of minimum TEX₈₆ values at the depth of maximum ammonia oxidation rates, consistent with the chemostat results. Our findings suggest that the integrated signal of archaeal membrane lipids reaching the sediments is a function of the dynamics of ammonia oxidation in the overlying water column. The TEX₈₆-SST calibration is therefore likely governed by the structure of the nutricline and its relationship to ocean thermal properties. This attribute of the TEX₈₆ ratio may make it a promising tracer for understanding the ocean’s nutrient dynamics and patterns of paleoproductivity.