Composition and Ecological Roles of the Core Microbiome along the Abyssal-Hadal Transition Zone Sediments of the Mariana Trench

Abstract

The unique geological features of hadal trenches are known to influence both the structure and ecological function of microbial communities. It is also well known that heterotrophs and chemoautotrophs dominate the hadal and abyssal pelagic zones, respectively. Here, a metagenomic investigation was conducted on sediment samples obtained from the abyssal-hadal transition zone in the Mariana Trench to gain a better understanding of the general diversity and potential function of the core microbiome in this zone. A high level of cosmopolitanism existed in the core microbiome referred from a high community similarity among different stations. Niche differentiation along the fine-scale of different sediment layers was observed, especially for major archaeal groups, largely due to sediment depth and the source of organic matter. A prevalence of nitrogen biogeochemical cycles driven by various nitrifying groups with the capability of dark carbon fixation in the abyssal-hadal biosphere was also demonstrated. The predominance of heterotrophic over chemolithoautotrophic pathways in this transition zone was found, and a high abundance of genes related to respiration and carbon fixation (i.e., the intact Calvin and rTCA cycles) were detected as well, which might reflect the intensive microbial activities known to occur in this deep biosphere. The presence of those metabolic processes and associated microbes were reflected by functional and genetic markers generated from the metagenomic data in the current study. However, their roles and contributions to the nitrogen/carbon biogeochemical cycles and flux in the abyssal-hadal transition zone still need further analysis. IMPORTANCE The Mariana Trench is the deepest oceanic region on earth, its microbial ecological exploration has become feasible with the rapid progress of submersible and metagenomic sequencing. We investigated the community compositions and metabolic functions of the core microbiome along the abyssal-hadal transition zone of the Mariana Trench, although most studies by far were focused on the pelagic zone. We found a predominance of heterotrophic groups and related metabolic pathways, which were closely associated with nitrogen biogeochemical cycles driven by various nitrifying groups with the capability of dark carbon fixation.

Keywords: Mariana Trench; abyssal-hadal transition zone; core microbiome; metagenomics.

FIG 1

Location of the sampling stations in the Mariana Trench.

FIG 2

Venn diagram showing the overlap of prokaryotic sequences at the genus level (A) and the metabolic pathways at the module level based on the KEGG database (B) for the sediment samples collected at depths of 0 to 6 cm, 6 to 12 cm, and 12 to 18 cm in the Mariana Trench. Singletons were removed before analysis and both major and unique sequences were annotated.

FIG 3

The community composition of the core microbiome is based on the top 30 orders of bacteria (A) and the top 15 genera of archaea (B). In both cases, group abundance <1% was treated as a minor group.

FIG 4

Redundancy analysis integrating the environmental parameters and the relative abundance of prokaryotic taxa at the order level in the different sediment samples (*, P < 0.05).

FIG 5

(A) Schematic with pie charts showing the relative abundance of genes involved in the main metabolic pathways of nitrogen in the core microbiome. The abundance was calculated by dividing the sum of the coverage of a particular gene in an individual sample, by the sum of the coverage of that gene in all the samples. (B) The absolute abundance of each gene was shown by z-score heatmap boxes indicated in the nitrogen cycle. (C) The microbial taxa of typical genes and their relative abundance in the different depths of each region.

FIG 6

(A) Schematic with pie charts showing the relative abundance of genes involved in the main sulfur metabolic pathways in the core microbiome. The abundance was calculated by dividing the sum of the coverage of a particular gene in an individual sample, by the sum of the coverage of that gene in all the samples. (B) The absolute abundance of each gene was shown by z-score heatmap boxes indicated in the sulfur cycle. (C) The microbial taxa of typical genes and their relative abundance in the different depths of each region.

FIG 7

Schematics with pie charts showing the relative abundance of genes involved in the Calvin cycle (A) and rTCA (B) for the metabolism of carbon-fixation in the core microbiome. The abundance was calculated by dividing the sum of the coverage of a particular gene in an individual sample, by the sum of the coverage of that gene in all the samples. (C) The absolute abundance of each gene was shown by z-score heatmap boxes indicated in the Calvin cycle and rTCA cycle. (D) The microbial taxa of typical genes and their relative abundance in the different depths of each region.

FIG 8

Phylogenetic analysis based on conserved proteins (A) and overview of metabolic potentials (B) of MAGs.

FIG 9

Schematic demonstrating the interactions among the key pathways involved in energy-yielding processes derived from metagenomic information. Heterotrophic remineralization and energetic coupling of nitrogen, sulfur, and hydrogen-based chemotrophic energy metabolism with carbon fixation. Key microbial groups were illustrated, and the associated metabolic pathways are color-coded.