Abstract

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.

Highlights

  • The deep ocean has been classically considered a vast "biological desert" (Danovaro et al, 2003) due to the attenuation of organic matter fluxes with increasing ocean depth (Wakeham et al, 1984; Martin et al, 1987;c Author(s) 2021

  • We evaluated the chemical characteristics and potential biological provenance of labile intact polar lipids (IPLs) in the hadal zone of

  • Since PGs play an essential role in photosynthesis (Wada and Murata, 2007), they have been mainly identified in algal and bacterial photoautotrophs (Dowhan, 1997; Sato et al, 2000; Gombos et al, 2002)

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Summary

Introduction

The deep ocean has been classically considered a vast "biological desert" (Danovaro et al, 2003) due to the attenuation of organic matter fluxes with increasing ocean depth Pacific (Schubotz et al, 2018a; Cantarero et al, 2020) and the Arabian Sea (Pitcher, 2011), as well as in surface open ocean waters of the eastern south Pacific (Van Mooy and Fredricks, 2010), the northwestern Atlantic (Popendorf et al, 2011b), and the Mediterranean Sea (Popendorf et al, 2011a), to name a few Their utility as markers of microbial diversity and processes has been tested in marine sediments (Liu et al, 2011, 2012; Sturt et al, 2004), such as along the Peru Margin, Equatorial Pacific, Hydrate Ridge, and Juan de Fuca Ridge (Lipp and Hinrichs, 2009a) and in subsurface sediment layers from the Peru Margin (Biddle et al, 2006). With an extension of ~5,900 km, the AT is the world’s largest trench (Sabbatini et al, 2002), whereas it is geographically isolated from other trenches in the Pacific Ocean

Study areas and sampling
Lipid extraction
IPLs in surface sediments of the
Distribution of IPL classes by polar head groups
Unique IPLs in hadal sediments of the Atacama
Potential sources of phospholipids
Potential biological sources of betaine lipids
Potential biological sources of other lipids
Allochthonous versus autochthonous IPLs in the Atacama
Findings
Do IPLs reveal homeoviscous adaptation to the deep-sea environment?
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