A new lipid-based proxy for the reconstruction of past phytoplankton ecological dynamics

The composition of lacustrine phytoplankton communities plays a key role for biogeochemical cycling of carbon, nitrogen, and phosphorus. Through the linkage between lakes and terrestrial ecosystems, especially via carbon cycling and freshwater supply, changes in algal ecology can affect even non-aquatic habitats. To investigate past phytoplankton dynamics, paleolimnologists often rely on microscopic algal remains preserved in the sediment, e.g., diatom frustules. However, only few taxa produce fossil remains, and might not be fully representative for the phytoplankton community. Other studies have reconstructed phytoplankton dynamics based on source-specific algal lipids, but many lipids are not as source-specific as initially thought. Rather than focusing on specific lipid biomarkers, a more holistic analysis of algal lipid distributions and their isotopic composition might highlight shifts in the past phytoplankton community with a greater robustness.

In this study, we introduce a new lipid-based proxy to reconstruct past phytoplankton community changes based on the abundance and hydrogen isotope ratios (δ²H) of short-chain fatty acids, phytosterols and phytol. Previous culturing and mesocosm experiments have shown that the relative offset between δ²H values of different algal lipids (ε_{lipid1-lipid2}) strongly differs among phytoplankton groups. For instance, ε_{palmitic acid-phytol} values for green algae and cyanobacteria were ~150 ‰ higher than for other taxa. To validate these results in a natural system, we collected algal biomass samples from the water column of Lake Rot, a small eutrophic lake in central Switzerland, every second week from 2019 to 2020. Phytoplankton and microplankton cell counts were conducted for every sampling date. ε_{lipid1-lipid2} values and algal lipid distributions were measured and related to biovolume changes of different algal groups. We used algal δ²H_lipid values from previous culturing studies weighted by phytoplankton biovolume in Lake Rot to model algal ε_{lipid1-lipid2} values. To assess the potential heterotrophic impact on ε_{lipid1-lipid2} values, we created a second model to simulate ε_{lipid1-lipid2} values incorporating δ²H_lipid values from algae and microplankton. For this, we included hydrogen isotope fractionation between algal and plankton lipids as well as microplankton biovolume in Lake Rot. Modeled ε_{lipid1-lipid2} values showed generally a good agreement with measured ε_{lipid1-lipid2} values, validating ε_{lipid1-lipid2} values as a potential proxy for phytoplankton dynamics. Moreover, measured ε_{lipid1-lipid2} values were clearly represented by modeled algal ε_{lipid1-lipid2} values suggesting that δ²H_lipid values in eutrophic lakes primarily reflect phytoplankton community composition with a negligible impact from microplankton. Our analysis of algal lipid distributions in the water column of Lake Rot revealed a significant positive correlation between the ratios of phytol and phytosterols (phytol:sterol ratio) as well as the sum of C18 fatty acids and C16:0 (C18:C16 ratio) and cyanobacterial biovolume.

We further apply our new lipid-based approach to a ~14 m long sediment core from Lake Rot, enabling a paleoecological reconstruction of phytoplankton community dynamics during the past ~13 kyr. Sedimentary phytol:sterol ratios, C18:C16 ratios, and ε_{palmitic acid-phytol} indicate rising cyanobacterial biovolume during the last ~4000 years. Moreover, we compare the magnitude of change in the algal community in response to 20^th century eutrophication with the natural variability throughout the Holocene.