Intact Ether Lipids in Trench Sediments Related to Archaeal Community and Environmental Conditions in the Deepest Ocean.

Archaea play an important role in marine biogeochemical cycle; however, their phylogenetic distribution and lipid composition in the hadal zone (6–11 km water depth) are poorly known. Here, we analyzed archaeal membrane lipids and 16S rRNA gene sequences in sediments from Mariana Trench (MT), Massau Trench (MS), and New Britain Trench (NBT), varying from 1,560 to 10,840 m depth. Forty‐two intact polar lipids (IPLs) were identified, including glycerol dialkyl glycerol tetraethers (GDGTs), OH‐GDGTs, glycerol dialkyl diethers (GDDs), and archaeol (AR) with polar headgroups of monohexose (1G), dihexose (2G), trihexose (3G), and hexose‐phosphohexose (HPH). Compositional and spatial distribution patterns of archaeal lipids suggest benthic Thaumarchaeota as a major source for IPLs, consistent with the predominance of Thaumarchaeota genes (>80%). The redundancy analysis (RDA) based on lipid and 16S rRNA data separates samples into three groups: extremely deep water (MT), significant terrestrial influence (NBT 1, 4, and 6), and predominant marine influence (MS, NBT 2, 3, 7, and 10). 1G‐GDDs and 1G‐AR positively correlate with water depth, likely reflecting the adaptation of benthic archaea to elevated hydrostatic pressure or variation of archaeal community in trench sediments. Bathyarchaeota are more abundant in sediments receiving terrestrial input; this pattern was attributed to their capability of utilizing terrestrial organic matter as an energy source. Our study highlights important environmental influences (e.g., pressure and organic matter quality and quantity) on benthic archaeal community and archaeal IPL compositions, which should be considered when IPLs and core lipids are applied as chemotaxonomic markers and paleo‐proxies. Key Points: Benthic archaea are a major source for IPLs in trench sedimentsSome IPLs positively correlate with water depth, reflecting adaption of archaea to hydrostatic pressure or changes of archaeal communityBathyarchaeota are more abundant in sediments receiving terrestrial input, attributed to utilization of terrestrial organic matter Plain Language Summary: This work is the first report on intact polar lipids (IPLs) of archaea in the hadal trenches, the deepest ocean realm with water depth exceeding 6,000 m. We have investigated in IPL biomarker 16S rRNA gene sequences and biogeochemical parameters in 19 sediments from the Mariana Trench, Massau Trench, and New Britain Trench. These samples are characterized by different water depth (1,560 to 10,840 m), net primary productivity (48 to 123 C m−2 year−1), and terrestrial influence. By comparing biomarker, gene data, and bulk geochemical parameters, we have achieved three key findings: (1) Benthic Thaumarchaeota are a major source for IPLs in hadal sediments; (2) Some IPLs positively correlate with water depth, likely reflecting an adaption mechanism of benthic archaea to elevated hydrostatic pressure or variation of archaeal community in different environments; and (3) Bathyarchaeota are more abundant in sediments receiving terrestrial input (New Britain Trench); this pattern is attributed to their capability of utilizing terrestrial organic matter as an energy source. Our findings provide important information toward understanding of the distribution and adaptation of hadal microbes to extremely high pressure, dark, and food‐depleted environments. [ABSTRACT FROM AUTHOR]

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