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Abstract Alkenones are biomarkers produced solely by algae in the order Isochrysidales that have been used to reconstruct sea surface temperature (SST) since the 1980s. However, alkenone-based SST reconstructions in the northern high latitude oceans show significant bias towards warmer temperatures in core-tops, diverge from other SST proxies in down core records, and are often accompanied by anomalously high relative abundance of the C₃₇tetra-unsaturated methyl alkenone (%C_37:4). Elevated %C_37:4is widely interpreted as an indicator of low sea surface salinity from polar water masses, but its biological source has thus far remained elusive. Here we identify a lineage of Isochrysidales that is responsible for elevated C_37:4methyl alkenone in the northern high latitude oceans through next-generation sequencing and lab-culture experiments. This Isochrysidales lineage co-occurs widely with sea ice in marine environments and is distinct from other known marine alkenone-producers, namelyEmiliania huxleyiandGephyrocapsa oceanica. More importantly, the %C_37:4in seawater filtered particulate organic matter and surface sediments is significantly correlated with annual mean sea ice concentrations. In sediment cores from the Svalbard region, the %C_37:4concentration aligns with the Greenland temperature record and other qualitative regional sea ice records spanning the past 14 kyrs, reflecting sea ice concentrations quantitatively. Our findings imply that %C_37:4is a powerful proxy for reconstructing sea ice conditions in the high latitude oceans on thousand- and, potentially, on million-year timescales. 

Abstract Members of the order Isochrysidales are unique among haptophyte lineages in being the exclusive producers of alkenones, long‐chain ketones that are commonly used for paleotemperature reconstructions. Alkenone‐producing haptophytes are divided into three major groups based largely on molecular ecological data: Group I is found in freshwater lakes, GroupIIcommonly occurs in brackish and coastal marine environments, and GroupIIIconsists of open ocean species. Each group has distinct alkenone distributions; however, only GroupsIIandIIIIsochrysidales currently have cultured representatives. The uncultured Group I Isochrysidales are distinguished geochemically by the presence of tri‐unsaturated alkenone isomers (C_37:3bMe, C_38:3bEt, C_38:3bMe, C_39:3bEt) present in water column and sediment samples, yet their genetic diversity, morphology, and environmental controls are largely unknown. Using small‐subunit (SSU) ribosomalRNA(rRNA) marker gene amplicon high‐throughput sequencing of environmental water column and sediment samples, we show that Group I is monophyletic with high phylogenetic diversity and contains a well‐supported clade separating the previously described “EV” clade from the “Greenland” clade. We infer the first partial large‐subunit (LSU)rRNAgene Group I sequence phylogeny, which uncovered additional well‐supported clades embedded within Group I. Relative to GroupII, Group I revealed higher levels of genetic diversity despite conservation of alkenone signatures and a closer evolutionary relationship with GroupIII. In Group I, the presence of the tri‐unsaturated alkenone isomers appears to be conserved, which is not the case for GroupII. This suggests differing environmental influences on Group I andIIand perhaps uncovers evolutionary constraints on alkenone biosynthesis. 

Key Points Group 1 alkenones are reliable indicators of cold‐season temperatures Pre‐industrial cold‐season warmth between 1750 and 1850 CE in northeastern China Relatively warm cold season may be related to positive cold‐season Arctic Oscillation conditions