Intact polar lipids in the hadal seabed of the Atacama Trench point to lateral sediment transport and in situ production as key sources of labile organic matter

Elevated concentrations of organic matter are found in sediments of hadal trenches relative to those found in the abyssal seabed, but the origin of such biological material remains elusive. Here, we report the composition and distribution of cell membrane intact polar lipids (IPLs) in surface sediments around the deepest points of the Atacama Trench and adjacent bathyal depths to assess and constrain the sources of labile organic matter 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. While the overall number of unique IPL structures in hadal sediments is limited and they contribute a small fraction of the total IPL pool, they include a high contribution of phospholipids with mono- and di-unsaturated fatty acids that are not associated with photoautotrophic sources. The diversity of labile IPLs in hadal sediments of the Atacama Trench suggests the presence of in situ microbial production and biomass that resembles traits of physiological adaptation to high pressure and low temperature, and/or the transport of labile organic matter from shallower sediment. We argue that the export of the most labile lipid component of the organic matter pool from the euphotic zone and the overlying oxygen minimum zone into the hadal sediments is neglectable. Our results contribute to the understanding of the mechanisms that control the delivery of labile organic matter to this extreme deep-sea ecosystem, whereas they provide insights into some potential physiological adaptation of the in situ microbial community to high pressure and low temperature through lipid remodeling.