Archaeal tetraether lipids and their biphytane carbon isotope composition in sediments along an estuarine biogeochemical gradient

The stable carbon isotopic composition of Thaumarchaeota-produced crenarchaeol (delta C-13(cren)) is thought to reflect the delta C-13 of dissolved inorganic carbon (DIC) and is valuable in carbon cycle research. Recently, an isotope flux-balance model was proposed that delta C-13(cren) is dependent on passive CO2 uptake and a slow rate of intracellular conversion to HCO3-, which has been validated in open ocean environments. However, further studies are required in environments with larger ranges of aqueous CO2 and diverse archaeal communities to examine whether the delta C-13(cren) value could still be predicted by the model. Here, we report delta C-13 values of biphytanes chemically released from the archaeal tetraether lipids (i.e., GDGTs) in sediments along a transect exhibiting shifts in the archaeal community and showing gradients of salinity, pH, and CO2 in the Pearl River Estuary, South China. Methanogenic and methanotrophic Euryarchaeota are present in the upper estuary, although not significant, as revealed by the elevated relative abundances of GDGT-0 and higher values of methane index in suspended particulate matter (SPM) and surface sediments, as well as the more C-13-depleted C-40:0, C-40:1, and C-40:2 biphytanes than the C-40:3 biphytane released from sedimentary GDGTs. Toward the lower estuary and coastal sea, GDGT distributions in SPM and sediments tend to indicate archaeal communities under normal marine conditions. However, there are still differences in delta C-13 values between C-40:0 and C-40:3 biphytanes by up to 2.4 parts per thousand in sediments, although C-40:1, C-40:2, and C-40:3 were similar in delta C-13, likely due to the existence of marine group II Euryarchaeota. Along such a physicochemical and biogeochemical gradient, the values of sedimentary delta C-13(40:3) increase monotonically with the increase of mean annual pH and the decrease of mean annual CO2. This phenomenon resembles the reported delta C-13(GDGT) profiles, along with the variations in pH and CO2, in water column in the open ocean, and hence consistent in direction with the isotope flux-balance model for Thaumarchaeota lipids. However, our estimated apparent biosynthetic isotope effect (epsilon(Ar)) of crenarchaeol, ranging from 15.2 parts per thousand to 19.7 parts per thousand, is mostly lower than those estimated in the open ocean. With the constraints of thaumarchaeal growth rates in such a dynamic estuarine environment as well as those in the open ocean, we suggest slight reductions in catalytic efficiency and intracellular kinetic isotope effect of intracellular CO2 hydration relative to previously employed values. Such modifications would slightly change the sensitivities of epsilon(Ar) to archaeal growth rate and ambient CO2 concentration but might be more suitable for variable hydrology and community environments. (C) 2021 Elsevier Ltd. All rights reserved.