Abstract

Hadal biosphere represents the deepest part of the ocean with water depth >6,000 m. Accumulating evidence suggests the existence of unique microbial communities dominated by heterotrophic processes in this environment. However, investigations of the microbial diversity and their metabolic potentials are limited because of technical constraints for sample collection. Here, we provide a detailed metagenomic analysis of three seawater samples at water depths 5,000–6,000 m below sea level (mbsl) and three surface sediment samples at water depths 4,435–6,578 mbsl at the Yap Trench of the western Pacific. Distinct microbial community compositions were observed with the dominance of Gammaproteobacteria in seawater and Thaumarchaeota in surface sediment. Comparative analysis of the genes involved in carbon, nitrogen and sulfur metabolisms revealed that heterotrophic processes (i.e., degradation of carbohydrates, hydrocarbons, and aromatics) are the most common microbial metabolisms in the seawater, while chemolithoautotrophic metabolisms such as ammonia oxidation with the HP/HB cycle for CO2 fixation probably dominated the surface sediment communities of the Yap Trench. Furthermore, abundant genes involved in stress response and metal resistance were both detected in the seawater and sediments, thus the enrichment of metal resistance genes is further hypothesized to be characteristic of the hadal microbial communities. Overall, this study sheds light on the metabolic versatility of microorganisms in the Yap Trench, their roles in carbon, nitrogen, and sulfur biogeochemical cycles, and how they have adapted to this unique hadal environment.

Highlights

  • Hadal biosphere is known as the deepest part of the ocean, which is >6,000 m below sea level

  • The reads were assembled into 41,218–166,805 contigs with the contig length of >2 Kbps, and metagenomic binning resulted in an average of 98 genomes for each sample

  • Based on the identified 16S rRNA gene reads from the six Yap Trench metagenomes, distinct microbial community structures were observed between the seawater and sediments, with the dominance of bacteria in the seawater (>98.1% in relative abundance) and archaea in the sediment (>32.7%), respectively (Table 1)

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Summary

Introduction

Hadal biosphere is known as the deepest part of the ocean, which is >6,000 m below sea level (mbsl). Some piezophilic strains of Gammaproteobacteria and Actinobacteria were isolated (Yayanos et al, 1981; Kato et al, 1998; Pathomaree et al, 2006), and microbial communities dominated by Gammaproteobacteria, Bacteroidetes, Deferribacteres, and Thaumarchaeota were identified in the trench seawater (Nunoura et al, 2015; Tarn et al, 2016); higher rates of microbial carbon turnover and higher abundance of microbial cells occurred in sediments at the Challenger Deep of the Mariana Trench (10,900 mbsl) as compared to that at a nearby 6,000 mbsl site (9.7 × 106 cells/cm−3 vs 1.4 × 106 cells/cm−3), revealing intensified microbial activity in this environment (Glud et al, 2013); analysis of 12 Parcubacteria single amplified genomes (SAGs) from the Challenger Deep sediments suggested their hadal adaptations to oxidative stress, polysaccharide modification and genes associated with respiratory nitrate reduction (León-Zayas et al, 2017). Few high-throughput metagenomic surveys have been conducted to examine the functional potentials of the hadal microbiome (Eloe et al, 2011a; Carvalho, 2013)

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