Microbiomes in the Challenger Deep slope and bottom-axis sediments

Abstract

Hadal trenches are the deepest and most remote regions of the ocean. The 11-kilometer deep Challenger Deep is the least explored due to the technical challenges of sampling hadal depths. It receives organic matter and heavy metals from the overlying water column that accumulate differently across its V-shaped topography. Here, we collected sediments across the slope and bottom-axis of the Challenger Deep that enable insights into its in situ microbial communities. Analyses of 586 metagenome-assembled genomes retrieved from 37 metagenomes show distinct diversity and metabolic capacities between bottom-axis and slope sites. 26% of prokaryotic 16S rDNA reads in metagenomes were novel, with novelty increasing with water and sediment depths. These predominantly heterotrophic microbes can recycle macromolecules and utilize simple and complex hydrocarbons as carbon sources. Metagenome and metatranscriptome data support reduction and biotransformation of arsenate for energy gain in sediments that present a two-fold greater accumulation of arsenic compared to non-hadal sites. Complete pathways for anaerobic ammonia oxidation are predominantly identified in genomes recovered from bottom-axis sediments compared to slope sites. Our results expand knowledge of microbially-mediated elemental cycling in hadal sediments, and reveal differences in distribution of processes involved in nitrogen loss across the trench.

Ecogenomics reveals viral communities across the Challenger Deep oceanic trench

“…The in silico host prediction indicated that CD viruses may infect 42 of our CD MAGs, assigned at 27 taxa at the species level (spanning seven phyla). These taxa include heterotrophs (e.g., Proteobacteria) and chemoautotrophs (e.g., Thaumarchaeota, Planctomycetota) involved in nitrogen and carbon cycling whose taxonomic signatures were abundant in CD sediments 39 , but with different relative abundances (7% to 43%) across the discrete sampling sites (bottom-axis vs. slope) (Supplementary Data 7 ). Indeed, Proteobacteria, Thaumarchaeota, and Planctomycetota were the most frequently predicted hosts in CD sediments (Fig.…”

“…3). This can be attributed to differences in the geographical isolation and nutrient availability between slope and bottom-axis sites that have been suggested to affect the distribution of prokaryotic communities across the V-shaped CD trench 38,39 . Differences in viral communities at discrete depths observed in this study and between this study and upper CD slope 48 15 and three hadal trenches 30 ), wetland 46 , thawed permafrost 47 , and pelagic seawater (Global Ocean Viromes 2.0) 7 .…”

“…We collected 586 MAGs 39 recovered from the metagenomes used for prediction of viruses in this study. Virus-host interaction was predicted by four different in silico methods 47 , 51 that include: 1. search for sequence homology by calculating the nucleotide identity of vOTUs and prokaryotic MAG sequences using BLASTn (v2.9.0+, setting: -evalue 0.001 -perc_identity 70).…”

“…The metagenomic analyses of viral communities collected from (hado) pelagic sediments in the northwest Pacific, including CD, showed that those viral communities were distinct from other marine habitats, with evidence for high endemicity 28,30 . Our previous study of microbial diversity in CD sediments revealed distinct prokaryotic communities between slope and bottom-axis sites 38,39 , which leaves an open question of whether the spatial distribution of hosts influences the distribution of viruses in CD. Using in silico phage identification pipelines, we identified 1628 virus operational taxonomic units (vOTUs) within the 37 metagenomes and examined their taxonomy, viral community structure, and linkages to prokaryotic hosts.…”

Virioplankton assemblages from challenger deep, the deepest place in the oceans

“…Except participating in the energy metabolism, viruses also encode unique antibiotic gene (PrnA) and virulence factors for bacterial immune reaction (Figures 6B and 6C). In addition, viruses in deep and hadal zones might be involved in the arsenic-related biological process (Figure 6), which was recently detected in the metagenomic assembled microbial genomes and proposed to relate to the biotransformation of arsenate for energy gain in the hadal sediments (Zhou et al, 2022). Comprehensive, viruses might influence the hadal microbial community structure and metabolism through the expression of AMG relating to antibiotic biosynthesis and nutrient metabolism to elevate the microbial adaption to the extreme environment in the hadal oceans (Figure 6).…”