Molecular and Isotopic Investigations Into the Ecology of Marine Thaumarchaeota

Abstract

Ammonia-oxidizing Archaea affiliated with phylum Thaumarchaeota are among the most abundant microorganisms in the global oceans and are generally recognized as the drivers of marine nitrification. The glycerol dibiphytanyl glycerol tetraether (GDGT) membrane lipids of planktonic Thaumarchaeota are preserved in marine sediments from the Jurassic (>100 million years) to the present. GDGTs are used to reconstruct past ocean temperatures via the TEX86 temperature proxy. This paleothermometer assumes that temperature is the dominant factor driving the GDGT composition of planktonic Thaumarchaeota. However, GDGTs filtered directly from the marine water column show that apparent TEX86 temperatures can diverge strongly from corresponding in situ temperatures. We performed continuous culture experiments using the model thaumarchaeon Nitrosopumilus maritimus, to investigate the effect of ammonia oxidation rate on GDGT composition. We find that TEX86 is negatively correlated with ammonia oxidation rate, resulting in warmer TEX86 temperatures at slower oxidation rates and colder TEX86 temperatures at faster oxidation rates. Thus, our work reveals that ammonia oxidation rate is an additional, temperature-independent control on lipid composition in N. maritimus. In the water column, TEX86 depth profiles and GDGT concentrations are consistent with the activity pattern of ammonia oxidizing Thaumarchaeota, as indicated by measured nitrification rates. The primary NO2- maximum marks a significant transitional zone in which minimum TEX86 values occur just above maximum GDGT concentrations. When integrated through the water column, the vast majority of the GDGT inventory occurs at and below the depth of the primary NO2- maximum. Using paired water column and sediment locations, we find that GDGT export from this transitional zone is consistent with sediment lipid ratios. This indicates that local ammonia oxidation dynamics are important controls on GDGT ratios preserved in sediments. The stable carbon isotope ratios of GDGTs (δ13CGDGT) may provide powerful tools for reconstructing variations in the ocean carbon cycle, including paleoproductivity, if they can be related to values of δ13CDIC. We find a surprising correspondence between water column export productivity and apparent organic carbon assimilation by the archaeal community, indicating that δ13C values of archaeal lipids may be expected to track productivity variations resulting from changes in net upwelling intensity.