Abstract
BackgroundThe full biosphere structure and functional exploration of the microbial communities of the Challenger Deep of the Mariana Trench, the deepest known hadal zone on Earth, lag far behind that of other marine realms.ResultsWe adopt a deep metagenomics approach to investigate the microbiome in the sediment of Challenger Deep, Mariana Trench. We construct 178 metagenome-assembled genomes (MAGs) representing 26 phyla, 16 of which are reported from hadal sediment for the first time. Based on the MAGs, we find the microbial community functions are marked by enrichment and prevalence of mixotrophy and facultative anaerobic metabolism. The microeukaryotic community is found to be dominated by six fungal groups that are characterized for the first time in hadal sediment to possess the assimilatory and dissimilatory nitrate/sulfate reduction, and hydrogen sulfide oxidation pathways. By metaviromic analysis, we reveal novel hadal Caudovirales clades, distinctive virus-host interactions, and specialized auxiliary metabolic genes for modulating hosts’ nitrogen/sulfur metabolism. The hadal microbiome is further investigated by large-scale cultivation that cataloged 1070 bacterial and 19 fungal isolates from the Challenger Deep sediment, many of which are found to be new species specialized in the hadal habitat.ConclusionOur hadal MAGs and isolates increase the diversity of the Challenger Deep sediment microbial genomes and isolates present in the public. The deep metagenomics approach fills the knowledge gaps in structure and diversity of the hadal microbiome, and provides novel insight into the ecology and metabolism of eukaryotic and viral components in the deepest biosphere on earth.
Highlights
The full biosphere structure and functional exploration of the microbial communities of the Challenger Deep of the Mariana Trench, the deepest known hadal zone on Earth, lag far behind that of other marine realms
The values of δ13C (− 21.41 to − 21.53‰) and δ15N (5.42 to 6.69‰) were within the ranges of the commonly observed values for marine organic matter [17]. This agrees with the results of recent studies that marine algae were the dominant source of sedimentary organic matter in the southern Mariana Trench [18, 19]
The results suggested that they were piezotolerant, which are likely derived from the microbes that descended from the water column, contributing to the diversity and metabolic functions of the hadal sediment microbiome
Summary
The full biosphere structure and functional exploration of the microbial communities of the Challenger Deep of the Mariana Trench, the deepest known hadal zone on Earth, lag far behind that of other marine realms. The microbial abundance in hadal trenches was related to the availability of sedimentary organic matter, which reached the deep hadal environments by sinking via the funneling effect and by occasional landslides induced by deep ocean earthquakes [4,5,6]. A great deal of effort has been focused on the Mariana Trench system in the Western Pacific ocean where two tectonic plates, the Philippine Sea plate and the Pacific plate, collide [7, 8]. It contains the deepest habitat known on earth, the Challenger Deep, ~ 11,000 m below the ocean surface [9]. In a comparison of microbes between Mariana and Kermadec trench habitats, they comprised cosmopolitan taxa with different abundances, in addition to some autochthonous microbes associated with unique and rare OTUs [15, 16]
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