Background: The deep sea harbors the majority of the microbial biomass in the ocean and is a key site for organic matter (OM) remineralization and storage in the biosphere. Microbial metabolism in the deep ocean is greatly controlled by the generally depleted but periodically fluctuating supply of OM. Currently, little is known about metabolic potentials of dominant deep-sea microbes to cope with the variable OM inputs, especially for those living in the hadal trenches—the deepest part of the ocean.Results: In this study, we report the first extensive examination of the metabolic potentials of hadal sedimentChloroflexi, a dominant phylum in hadal trenches and the global deep ocean. In total, 62 metagenome-assembled-genomes (MAGs) were reconstructed from nine metagenomic datasets derived from sediments of the Mariana Trench. These MAGs represent six novel species, four novel genera, one novel family, and one novel order within the classesAnaerolineaeandDehalococcoidia. Fragment recruitment showed that these MAGs are globally distributed in deep-sea waters and surface sediments, and transcriptomic analysis indicated their in situ activities. Metabolic reconstruction showed that hadalChlorofleximainly had a heterotrophic lifestyle, with the potential to degrade a wide range of organic carbon, sulfur, and halogenated compounds. Our results revealed for the first time that hadalChloroflexiharbor pathways for the complete hydrolytic or oxidative degradation of various recalcitrant OM, including aromatic compounds (e.g., benzoate), polyaromatic hydrocarbons (e.g., fluorene), polychlorobiphenyl (e.g., 4-chlorobiphenyl), and organochlorine compounds (e.g., chloroalkanes, chlorocyclohexane). Moreover, these organisms showed the potential to synthesize energy storage compounds (e.g., trehalose) and had regulatory modules to respond to changes in nutrient conditions. These metabolic traits suggest thatChlorofleximay follow a “feast-or-famine” metabolic strategy, i.e., preferentially consume labile OM and store the energy intracellularly under OM-rich conditions, and utilize the stored energy or degrade recalcitrant OM for survival under OM-limited condition.Conclusion: This study expands the current knowledge on metabolic strategies in deep-oceanChlorolfexiand highlights their significance in deep-sea carbon, sulfur, and halogen cycles. The metabolic plasticity likely providesChloroflexiwith advantages for survival under variable and heterogenic OM inputs in the deep ocean.

Particle-attached (PA) and free-living (FL) microorganisms play significant but different roles in mineralization of organic matter (OM) in the ocean. Currently, little is known about PA and FL microbial communities in bathyal and abyssal pelagic waters, and understanding of their diversity and distribution in the water column and their interactions with environmental factors in the trench area is limited. We investigated for the first time the variations of abundance and diversities of the PA and FL bacterial communities in the epi-, bathy-, and abyssopelagic zones of the New Britain Trench (NBT). The PA communities showed decreasing species richness but increasing relative abundance with depth, suggesting the increasing ecological significance of the PA bacteria in the deep ocean. The abundance and diversity of PA and FL bacterial communities in the NBT water column appeared to be shaped by different sets of environment factors, which might be related to different micro-niches of the two communities. Analysis on species distribution suggested that the differences between PA and FL bacteria communities mainly resulted from the different relative abundance of the “shared taxa” in the two types of communities. These findings provide valuable information for understanding the relative ecological roles of the PA and FL bacterial communities and their interactions with environmental factors in different pelagic zones along the vertical profile of the NBT water column.

Background: The full biosphere structure and functional exploration of the microbial communities of the Challenger Deep of the Mariana Trench, the deepest known hadal zone on Earth, lag far behind that of other marine realms. Results: We adopt a deep metagenomics approach to investigate the microbiome in the sediment of Challenger Deep, Mariana Trench. We construct 178 metagenome-assembled genomes (MAGs) representing 26 phyla, 16 of which are reported from hadal sediment for the first time. Based on the MAGs, we find the microbial community functions are marked by enrichment and prevalence of mixotrophy and facultative anaerobic metabolism. The microeukaryotic community is found to be dominated by six fungal groups that are characterized for the first time in hadal sediment to possess the assimilatory and dissimilatory nitrate/sulfate reduction, and hydrogen sulfide oxidation pathways. By metaviromic analysis, we reveal novel hadal Caudovirales clades, distinctive virus-host interactions, and specialized auxiliary metabolic genes for modulating hosts’ nitrogen/sulfur metabolism. The hadal microbiome is further investigated by large-scale cultivation that cataloged 1070 bacterial and 19 fungal isolates from the Challenger Deep sediment, many of which are found to be new species specialized in the hadal habitat. Conclusion: Our hadal MAGs and isolates increase the diversity of the Challenger Deep sediment microbial genomes and isolates present in the public. The deep metagenomics approach fills the knowledge gaps in structure and diversity of the hadal microbiome, and provides novel insight into the ecology and metabolism of eukaryotic and viral components in the deepest biosphere on earth.

Surprisingly high rates of microbial respiration have recently been reported in hadal trench sediment, yet the potentially active microorganisms and specific microbe–microbe relationships in trench sediment are largely unknown. We investigated the bulk and active prokaryotic communities and co-occurrence interactions of different lineages in vertically sectioned sediment cores taken from the deepest points of the Mariana and Mussau Trenches. Analysis on species novelty revealed for the first time the high rate of novel lineages in the microbial communities of the hadal trenches. Using 95, 97, and 99% similarity as thresholds, averagely 22.29, 32.3, and 64.1% of total OTUs retrieved from sediments of the two trenches were identified as the potentially novel lineages, respectively. The compositions of the potentially active communities, revealed via ribosomal RNA (rRNA), were significantly different from those of bulk communities (rDNA) in all samples from both trenches. The dominant taxa in bulk communities generally accounted for low proportions in the rRNA libraries, signifying that the abundance was not necessarily related to community functions in the hadal sediments. The potentially active communities showed high diversity and composed primarily of heterotrophic lineages, supporting their potential contributions in organic carbon consumption. Network analysis revealed high modularity and non-random co-occurrence of phylogenetically unrelated taxa, indicating highly specified micro-niches and close microbial interactions in the hadal sediments tested. Combined analysis of activity potentials and network keystone scores revealed significance of phyla Chloroflexi and Gemmatimonadetes, as well as several potentially alkane-degrading taxa in maintaining microbial interactions and functions of the trench communities. Overall, our results demonstrate that the hadal trenches harbor diverse, closely interacting, and active microorganisms, despite the extreme environmental conditions.

Knowledge of sedimentary organic carbon (OC) in hadal trenches, the deepest ocean realm, is rudimentary. Here, we conducted a comprehensive analysis of total OC (TOC), stable and radio‐carbon isotopes (δ¹³C and Δ¹⁴C), and biomarkers (e.g., n‐alkanes, n‐alkanols and n‐fatty acids) in 12 sediment cores collected from hadal (trench axis) and non‐hadal (abyssal plains and slopes) settings of the Kermadec Trench (Southwestern Pacific) and Atacama Trench (Southeastern Pacific) regions. Our results show that the TOC in the Atacama Trench region (0.86% ± 0.69%) is significantly higher than that of the Kermadec Trench region (0.29% ± 0.08%), likely related to different surface primary productivity. In both trench regions, the hadal sites are generally characterized by more negative δ¹³C, higher TOC/TN ratio, and similar or higher abundance ratio of terrigenous/marine biomarkers as compared to the non‐hadal sites, suggesting the selective preservation of terrigenous biogenic/fossil OC at the hadal trench axis. The linear increase in ¹⁴C age with sediment depth in non‐hadal cores reflects steady depositional conditions, whereas seven out of eight hadal sediment cores show ¹⁴C age reversals presumably due to occasional mass‐transport deposits. Our results suggest (1) a strong heterogeneity in sedimentary OC characteristics between trenches and within each trench and (2) relatively high accumulation rates of terrigenous OC in both the Kermadec Trench (0.35 ± 0.04 g m⁻² yr⁻¹) and the Atacama Trench (1.4 ± 0.5 g m⁻² yr⁻¹). Thus, hadal trenches appear to represent an important environment for terrigenous carbon deposition in the deep ocean.