Seasonal and multi-annual variation in the abundance of isoprenoid GDGT membrane lipids and their producers in the water column of a meromictic equatorial crater lake (Lake Chala, East Africa)
Baxter, A.J.; van Bree, L.G.J.; Peterse, F.; Hopmans, E.C.; Villanueva, L.; Verschuren, D.; Sinninghe Damste, J.S. (2021). Seasonal and multi-annual variation in the abundance of isoprenoid GDGT membrane lipids and their producers in the water column of a meromictic equatorial crater lake (Lake Chala, East Africa). Quat. Sci. Rev. 273: 107263. https://dx.doi.org/10.1016/j.quascirev.2021.107263
Isoprenoid glycerol dialkyl glycerol tetraethers (isoGDGTs) are membrane lipids of Archaea. Organic biomarker proxies associated with these lipids, such as the TEX86 paleothermometer and Branched and Isoprenoid Tetraether (BIT) index, are often used in paleoenvironmental reconstructions for the marine environment, but their general applicability in lacustrine settings is hampered by limited understanding of the biological sources and environmental drivers influencing isoGDGT production. To validate the use of isoGDGT proxies in lakes, we studied the occurrence of isoGDGTs in Lake Chala, a permanently stratified (meromictic) crater lake in equatorial East Africa. We analyzed the abundance and distribution of isoGDGTs in 17 depth profiles of suspended particulate matter (SPM) collected monthly between September 2013 and January 2015, and compared this with the abundance and composition of archaea based on 16S rRNA gene and quantitative PCR analysis. Both isoGDGTs and archaeal abundance in the SPM were exceptionally low throughout the study period. In the oxygenated part of the water column, higher fractional abundances of crenarchaeol are matched by a predominance of the ammonia-oxidizing Thaumarchaeota I.1b that are known to produce this GDGT, whereas deep anoxic water layers are characterized by high fractional abundances of GDGT-0 as well as the anaerobic heterotrophic Group C3 MCG Bathyarchaea and specific euryarchaeotal methanogens. Analysis of intact polar lipid (IPL) isoGDGTs using SPM depth profiles from three months representing distinct seasons during the study period revealed the presence of several IPLs of GDGT-0 in the anoxic lower water column, which are rarely found in natural settings. IPL GDGT-0 with a phosphatidylglycerol (PG-), monohexose-phosphatidylglycerol (MH-PG-) and dihexose-phosphatidylglycerol (DH-PG-) head-group was typically only present just above the lake bottom at 90 m depth and probably reflect specific communities of anaerobic archaea. We also determined the flux and distribution of isoGDGTs in settling particles collected monthly between November 2006 and January 2015 from a sediment trap suspended at 35 m water depth to assess seasonal and inter-annual variability in surface-water isoGDGT production, and compared this with the temporal distribution of isoGDGTs in the 25,000-year long sediment record from Lake Chala. Monthly variation of isoGDGTs in the 98-month settling-particles record did not show a strong annual pattern related to seasonal water-column mixing and stratification, likely because the oxycline was regularly situated below sediment-trap depth. Episodes of high GDGT-0 concentrations relative to crenarchaeol in the settling particles can therefore be linked to periods of exceptionally shallow oxycline depth, which suppresses the thaumarchaeotal bloom. During such intervals, TEX86-based paleotemperatures are not reliable because isoGDGT input from other archaeal sources disproportionally influences TEX86 values and creates a cold-temperature bias. Additionally, the abundance of the crenarchaeol isomer relative to crenarchaeol (f[CREN']) gradually increases during such episodes of high GDGT-0/crenarchaeol ratio, suggesting increasing dominance of Group I.1b over Group I.1a Thaumarchaeota, and might prove a good marker for prolonged shallow-oxycline conditions. Most importantly, the associated near-absence of crenarchaeol during times of strong upper-water-column stratification results in high BIT-index values. We propose that this suppression mechanism may be the principal driver of BIT-index variation in the sediment record of Lake Chala, and the main source of observed congruence between the BIT index and climate-driven lake-level variation on long time scales.
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