Bacterial and eukaryotic intact polar lipids point to in situ production as a key source of labile organic matter in hadal surface sediment of the Atacama Trench

Abstract

Elevated organic matter (OM) concentrations are found in hadal surface sediments relative to the surrounding abyssal seabed. However, the origin of this biological material remains elusive. Here, we report on the composition and distribution of cellular membrane intact polar lipids (IPLs) extracted from surface sediments around the deepest points of the Atacama Trench and adjacent bathyal margin to assess and constrain the sources of labile OM in the hadal seabed. Multiscale bootstrap resampling of IPLs' structural diversity and abundance indicates distinct lipid signatures in the sediments of the Atacama Trench that are more closely related to those found in bathyal sediments than to those previously reported for the upper ocean water column in the region. Whereas the overall number of unique IPL structures in hadal sediments contributes a small fraction of the total IPL pool, we also report a high contribution of phospholipids with mono- and di-unsaturated fatty acids that are not associated with photoautotrophic sources and that resemble traits of physiological adaptation to high pressure and low temperature. Our results indicate that IPLs in hadal sediments of the Atacama Trench predominantly derive from in situ microbial production and biomass, whereas the export of the most labile lipid component of the OM pool from the euphotic zone and the overlying oxygen minimum zone is neglectable. While other OM sources such as the downslope and/or lateral transport of labile OM cannot be ruled out and remain to be studied, they are likely less important in view of the lability of ester-bond IPLs. Our results contribute to the understanding of the mechanisms that control the delivery of labile OM to this extreme deep-sea ecosystem. Furthermore, they provide insights into some potential physiological adaptation of the in situ microbial community to high pressure and low temperature through lipid remodeling.