Unusually high production of C37:4 alkenone by an Arctic Gephyrocapsa huxleyi strain grown under nutrient-replete conditions

Abstract

The percentage of C37:4 alkenone relative to total C37 alkenones (C37:4%) in northern high-latitude ocean waters and surface sediments, which can be up to 77%, has been recently found to correlate strongly with annual mean sea ice coverage. Genomic data and culture experiments suggest these high percentage of C37:4 alkenones may be mainly attributed to the production by Group 2i Isochrysidales, because the cosmopolitan Isochrysidales, Emiliania huxleyi (recently renamed to Gephyrocapsa huxleyi) typically does not produce significant amount of C37:4 alkenone in laboratory cultures. However, the presence of significant amounts of C38 methyl alkenones in high-latitude ocean sediments and suspended particulate samples suggests possible contributions from G. huxleyi as well. Here we performed the first culture experiments on G. huxleyi strain NIES3366 from the Chukchi Sea. This strain was isolated from the coldest and highest latitude ocean waters known for G. huxleyi strains so far. NIES1312 from the Bering Sea was also cultured under identical conditions for comparison. We show that, in f/2 growth media, NIES3366 was capable of producing unusually large amounts of C37:4 alkenone reaching 12.8% at 12 °C and up to 20% between 6 °C and 9 °C. In comparison, NIES1312 only produced 3.6% C37:4 at 12 °C. Our results suggest that Arctic strains of G. huxleyi may have also contribute to the inventory of the high-C37:4 alkenone profile in northern high-latitude oceans. Importantly, however, when NIES3366 was grown in 10 times lower nutrient (f/20) at 12 °C, the C37:4% decreased by ∼ 50% (to 6%), indicating a strong impact of nutrients on the production of C37:4 alkenone. In contrast, salinity levels had a negligible impact on the percentage of C37:4 for both strains, indicating an absence of a physiological effect of salinity. We also demonstrate that at low temperatures, tetra-unsaturated alkenones must be included for calculating unsaturation indices to achieve strong linear correlation with temperatures for NIES3366, a feature contrary to other G. huxleyi strains isolated from mid- and low- latitude oceans. Our findings provide a refined mechanistic explanation for the application of alkenone C37:4% as a quantitative sea ice proxy in high-latitude oceans.