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. 2024 Aug;16(4):e13314.
doi: 10.1111/1758-2229.13314.

Microbial communities reveal niche partitioning across the slope and bottom zones of the challenger deep

Aoran Hu  1   2 , Weishu Zhao  1   2   3 , Jing Wang  2   3   4 , Qi Qi  1   2 , Xiang Xiao  1   2   4   5 , Hongmei Jing  5   6
Affiliations

Microbial communities reveal niche partitioning across the slope and bottom zones of the challenger deep

Aoran Hu et al. Environ Microbiol Rep. 2024 Aug.

Abstract

Widespread marine microbiomes exhibit compositional and functional differentiation as a result of adaptation driven by environmental characteristics. We investigated the microbial communities in both seawater and sediments on the slope (7-9 km) and the bottom (9-11 km) of the Challenger Deep of the Mariana Trench to explore community differentiation. Both metagenome-assembled genomes (MAGs) and 16S rRNA amplicon sequence variants (ASVs) showed that the microbial composition in the seawater was similar to that of sediment on the slope, while distinct from that of sediment in the bottom. This scenario suggested a potentially stronger community interaction between seawater and sediment on the slope, which was further confirmed by community assembly and population movement analyses. The metagenomic analysis also indicates a specific stronger potential of nitrate reduction and sulphate assimilation in the bottom seawater, while more versatile nitrogen and sulphur cycling pathways occur on the slope, reflecting functional differentiations among communities in conjunction with environmental features. This work implies that microbial community differentiation occurred in the different hadal niches, and was likely an outcome of microbial adaptation to the extreme hadal trench environment, especially the associated hydrological and geological conditions, which should be considered and measured in situ in future studies.

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Conflict of interest statement

The authors declare no conflicts of interest.

Figures

FIGURE 1
FIGURE 1
Sampling sites, depth, locations, and grouping. Seawater samples are collected from the slope and bottom of the Mariana Trench near the seabed in the hadal zone; sediment samples are referenced from Zhou et al. (2022) and Wang et al. (2022).
FIGURE 2
FIGURE 2
Taxonomy prevalence and abundance of classes in seawater and sediment samples at the slope and bottom of the Mariana Trench. (A) NMDS plot of binary Jaccard distance according to MAGs and 16S samples at the class level. (B) NMDS plot of Bray–Curtis distance according to MAGs and 16S samples at the class level. (C) Microbial community composition of all metagenome samples in this study. In (C), classes in the same phylum are coloured with the same colour, except for some specific abundant clades at the class level (e.g., Alphaproteobacteria and Gammaproteobacteria from Proteobacteria, Dehalococcoidia from Chloroflexota, and Bacteroidia from Bacteroidota) and the only classes of the phylum in this study (e.g., UBA1144 from Desulfobacterota_D, Nitrososphaeria from Thermoproteota, and Nanoarchaeia from Nanoarchaeota).
FIGURE 3
FIGURE 3
Phylogeny of metagenome‐assembled genomes (MAGs) from seawater and sediment samples from the bottom (A) and slope (B) in the Mariana Trench. Assembled genomes are dereplicated and annotated with GTDBTK (Chaumeil et al., 2019). Genomes that appeared only in sediment are marked with red, those that appeared only in seawater are marked with blue, and those that occurred across seawater and sediment at the bottom or slope are marked with pink.
FIGURE 4
FIGURE 4
Relative abundance of metabolic genes involved in nitrogen metabolism from seawater and sediment samples collected at the slope and the bottom of the Mariana Trench. Gene abundance from different samples was estimated by the GPM method. (A) Total relative abundance of genes in different samples. (B) Average relative abundance and difference of genes in nitrogen metabolism in MAGs. The significance of differences between groups was examined by the Wilcox test; ‘.’, ‘*’, ‘**’, and ‘***’ indicate statistical significance at the FDR‐adjusted p < 0.1, 0.05, 0.01, and 0.001 levels, respectively.
FIGURE 5
FIGURE 5
Schematic diagram of nitrogen cycling pathways in the seawater and sediments at the bottom and slope of the Challenger Deep. (A) The schematic diagram in slope seawater, slope sediment, bottom seawater, and bottom sediment. (B) The relative abundance of key metabolic genes. Detailed nitrogen‐related pathways: ① assimilatory and dissimilatory nitrate reduction; ② assimilatory and dissimilatory nitrite reduction; ③ nitrite oxidation; ④ nitrite reduction and nitrogen oxide reduction in denitrification; ⑤ nitrous oxide reduction; ⑥ ammonia oxidation; ⑦ nitrogen fixation; ⑧ nitrate transport; ⑨ ammonia transport and utilization. The thickness of the arrows indicates the potential capability (i.e., the relative abundance of genes) of the metabolic function, and the dashed arrows indicate the function/process for which no gene was detected but which is expected to occur.
FIGURE 6
FIGURE 6
Schematic diagram of the taxonomic composition of the microbial community in the slope and bottom of the Mariana Trench. The dashed line indicates genome sets detected in different environments, and the colour blocks indicate the size of the subset shared across environments according to Figure S3. The ring plot shows the driving force shaping the community in the environment. The two wider arrows indicate the direction of estimated water flux, and the thinner arrow indicates the estimated net microbial population movement.
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