Hadal trenches are considered as depocenters for organic matter and hotspots for microbial diagenetic activity. Here, we explore the sources, degradation, and transport of organic matter in the shelf‐trench continuum using seven short sediment cores collected along two transects with water depths ranging between 1,553 and 8,901 m in the New Britain Trench area, Papua New Guinea. Carbon isotopic compositions (δ¹³C) and radiocarbon contents (Δ¹⁴C) of sedimentary organic matter accompanied by total organic carbon/total nitrogen ratios suggest an important contribution from the preaged soil organic matter mixed by the marine algae and terrigenous C₃ vascular plants. In addition, the trench axis sites are characterized by elevated accumulation of terrigenous organic materials. Rates of organic matter mineralization approximated by dissolved inorganic carbon fluxes at the sediment‐water interface reveal an approximately threefold higher rate at the trench axis sites than the abyssal sites. ²¹⁰Pb_xs profiles and burial of carbonate (up to 50%) at both trench axis sites reflect recent occurrence of mass‐wasting events possibly induced by earthquakes, which is responsible for the transport of preaged, terrigenous organic matter to the trench bottom. This tectonically triggered deposition event, which was also shown to occur in the Japan Trench, the Tonga Trench, and probably in many other trenches, is likely to efficiently transport terrigenous organic matter to hadal trenches, thereby underpinning the importance of terrigenous organic matter burial in hadal trenches for the ocean organic carbon budget. Furthermore, we hypothesize that hadal trenches may host a distinct microbial community that is capable of feeding on old, refractory terrigenous organic matter.

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.

Hadal trenches are a unique habitat with high hydrostatic pressure, low temperature and scarce food supplies. Amphipods are the dominant scavenging metazoan species in this ecosystem. Trimethylamine (TMA) and trimethylamine oxide (TMAO) have been shown to play important roles in regulating osmotic pressure in mammals, hadal dwellers and even microbes. However, the distributions of TMAO and TMA concentrations of hadal animals among different tissues have not been reported so far. Here, the TMAO and TMA contents of eight tissues of two hadal amphipods, Hirondellea gigas and Alicella gigantea from the Mariana Trench and the New Britain Trench, were detected by using the ultrahigh performance liquid chromatography–mass spectrometry (UPLC-MS/MS) method. Compared with the shallow water Decapoda, Penaeus vannamei, the hadal amphipods possessed significantly higher TMAO concentrations and a similar level of TMA in all the detected tissues. A higher level of TMAO was detected in the external organs (such as the eye and exoskeleton) for both of the two hadal amphipods, which indicated that the TMAO concentration was not evenly distributed, although the same hydrostatic pressure existed in the outer and internal organs. Moreover, a strong positive correlation was found between the concentrations of TMAO and TMA in the two hadal amphipods. In addition, evolutionary analysis regarding FMO3, the enzyme to convert TMA into TMAO, was also conducted. Three positive selected sites in the conserved region and two specific mutation sites in two conserved motifs were found in the A. gigantea FMO3 gene. Combined together, this study supports the important role of TMAO for the environmental adaptability of hadal amphipods and speculates on the molecular evolution and protein structure of FMO3 in hadal species.