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.

Fig. 1. Overview of sampling sites and microbiome novelty in Challenger Deep (CD) sediments.

a Sampling locations in CD (details of the sampling sites are in Supplementary Data 2). b Box plots showing the average percentage of novel 16S miTags in slope and bottom-axis CD sediment metagenomes (this study), deep-sea hydrothermal/cold-seep sediment metagenomes (Deep Sed), and CD hadal water column (CD water) metagenomes from public databases (p values were estimated using the two-sided Wilcoxon test for pairwise comparisons). Sequences and identity results are deposited in 10.6084/m9.figshare.12979709. c Pearson’s correlation analyses between the estimated novel 16S miTags and the different depths of the sampling sites (p value was calculated using the two-sided t test). d Microbiome novelty scores (MNS) for CD slope and bottom-axis sediments (p values estimated using the two-sided Wilcoxon test). e Pearson’s correlation analyses between the microbiome novelty scores and the different depths of the sampling sites (p values were calculated using the two-sided t test). In box plots (b, d), center lines indicate median values. The lower and upper bounds represent 25th and 75th percentiles, respectively. The lower/upper whiskers represent minima/maxima no further than 1.5 times the interquartile range from the hinge, and the points falling outside of the whiskers represent the outliers. The pink background at c, e indicates 95% confidence interval. Source data are provided as a Source data file.

Fig. 2. Phylogeny, taxonomy, and genome size of reconstructed metagenome-assembled genomes (MAGs).

a Maximum-likelihood phylogenomic tree of the 586 MAGs (green and orange clades present high and medium quality MAGs, respectively) and 255 reference genomes (black clades) from GTDB. The cyan dots present MAGs unique to slope sediments, the red shows MAGs unique to bottom-axis sediments, and the purple dots represent MAGs found in both slope and bottom-axis sediments (Trench). Gray bars show the prevalence of the MAGs in the 37 metagenomes. b PCoA ordination analysis using the relative abundance of MAGs and Bray-Curtis dissimilarity index. c Comparison of estimated genome size of the top 80 prevalent MAGs found in bottom-axis (Bottom), slope (Slope), and in both slope and bottom-axis sediments (Trench). p values were estimated with a two-sided t test analysis using the Trench MAGs as reference. In the box plot, center lines indicate median values. The lower and upper bounds represent 25th and 75th percentiles, respectively. The lower/upper whiskers represent minima/maxima no further than 1.5 times the interquartile range from the hinge, and the points falling outside of the whiskers represent the outliers. Source data are provided as a Source data file.

Fig. 3. Presence of selected metabolic genes in the 37 metagenomes and the three bottom-axis sediment metatranscriptomes.

a Heatmap of various metabolic genes across phyla (class level for Proteobacteria) found in the CD sediments. Light colors indicate genes present at 20–50% in the retrieved MAGs. Darker colors indicate genes present at 50–100% in the retrieved MAGs. The number of genomes per phylum is shown in the parentheses. The number of key genes present in <20% of genomes is given in the squares. b Mean relative gene abundances across the 37 metagenomes. The bars indicate the minima and maxima of the gene abundances. c Heatmap of the relative abundance of transcripts (TPM) in the three metatranscriptomes (6–9, 12–15, 15–21 cmbsf) from the bottom-axis sediment sample at the T3L11 site (10,908 m). Gl glycolysis and gluconeogenesis, TCA tricarboxylic acid cycle, rTCA reductive tricarboxylic acid cycle, Ace acetate metabolism, WL Wood–Ljungdahl pathway, 3HP/4HB 3-hydroxypropionate/4-hydroxybutyrate cycle, Cal Calvin cycle, Asr arsenate metabolism, Sel selenate metabolism, TPM transcripts per million. Details of the metabolic genes can be found in Supplementary Data 7. Source data are provided as a Source data file.

Fig. 4. Identification of potential microbial nitrogen releasers in CD.

a Heatmap of the relative abundance of MAGs involved in anaerobic ammonia oxidation (anammox) and denitrification in sediments from the slope and bottom-axis sites. The relative abundance of each MAG was transformed using the logarithmic scale of 10 (log10(abundance + 1‰)) and was estimated using CoverM. b Phylogenomic analyses of 40 concatenated conserved proteins identified in anammox bacteria. Bootstrap values (1000 replicates) ≥80% are indicated by dots on branches. c Hypothetical nitrogen release in CD sediments via anammox. The anammox genes presented are from the CD bottom-axis sediment MAGs. Source data are provided as a Source data file.

Fig. 5. Schematic representation of potential nitrogen and arsenic cycling in bottom-axis CD sediments.

The number of genomes that contain the genes involved in nitrogen and arsenic cycling steps is in parentheses. Source data can be found in Supplementary Data 7.