Dataset Information

A unique subseafloor microbiosphere in the Mariana Trench driven by episodic sedimentation.

ABSTRACT: Hadal trenches are characterized by enhanced and infrequent high-rate episodic sedimentation events that likely introduce not only labile organic carbon and key nutrients but also new microbes that significantly alter the subseafloor microbiosphere. Currently, the role of high-rate episodic sedimentation in controlling the composition of the hadal subseafloor microbiosphere is unknown. Here, analyses of carbon isotope composition in a ~ 750 cm long sediment core from the Challenger Deep revealed noncontinuous deposition, with anomalous ¹⁴C ages likely caused by seismically driven mass transport and the funneling effect of trench geomorphology. Microbial community composition and diverse enzyme activities in the upper ~ 27 cm differed from those at lower depths, probably due to sudden sediment deposition and differences in redox condition and organic matter availability. At lower depths, microbial population numbers, and composition remained relatively constant, except at some discrete depths with altered enzyme activity and microbial phyla abundance, possibly due to additional sudden sedimentation events of different magnitude. Evidence is provided of a unique role for high-rate episodic sedimentation events in controlling the subsurface microbiosphere in Earth's deepest ocean floor and highlight the need to perform thorough analysis over a large depth range to characterize hadal benthic populations. Such depositional processes are likely crucial in shaping deep-water geochemical environments and thereby the deep subseafloor biosphere.

Supplementary information

The online version contains supplementary material available at 10.1007/s42995-023-00212-y.

SUBMITTER: Liu J

PROVIDER: S-EPMC10902237 | biostudies-literature | 2024 Feb

REPOSITORIES: biostudies-literature

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A unique subseafloor microbiosphere in the Mariana Trench driven by episodic sedimentation.

Liu Jiwen J Li Da-Wei DW He Xinxin X Liu Ronghua R Cheng Haojin H Su Chenglong C Chen Mengna M Wang Yonghong Y Zhao Zhongsheng Z Xu Hanyue H Cheng Zhangyu Z Wang Zicheng Z Pedentchouk Nikolai N Lea-Smith David J DJ Todd Jonathan D JD Liu Xiaoshou X Zhao Meixun M Zhang Xiao-Hua XH

Marine life science & technology 20240123 1

Hadal trenches are characterized by enhanced and infrequent high-rate episodic sedimentation events that likely introduce not only labile organic carbon and key nutrients but also new microbes that significantly alter the subseafloor microbiosphere. Currently, the role of high-rate episodic sedimentation in controlling the composition of the hadal subseafloor microbiosphere is unknown. Here, analyses of carbon isotope composition in a ~ 750 cm long sediment core from the Challenger Deep revealed ...[more]

PMID: 38433963

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Project description:Dimethylsulfoniopropionate (DMSP) and related organic sulfur compounds play key roles in global sulfur cycling. Bacteria have been found to be important DMSP producers in seawater and surface sediments of the aphotic Mariana Trench (MT). However, detailed bacterial DMSP cycling in the Mariana Trench subseafloor remains largely unknown. Here, the bacterial DMSP-cycling potential in a Mariana Trench sediment core (7.5 m in length) obtained at a 10,816-m water depth was investigated using culture-dependent and -independent methods. The DMSP content fluctuated along the sediment depth and reached the highest concentration at 15 to 18 cm below the seafloor (cmbsf). dsyB was the dominant known DMSP synthetic gene, existing in 0.36 to 1.19% of the bacteria, and was identified in the metagenome-assembled genomes (MAGs) of previously unknown bacterial DMSP synthetic groups such as Acidimicrobiia, Phycisphaerae, and Hydrogenedentia. dddP, dmdA, and dddX were the major DMSP catabolic genes. The DMSP catabolic activities of DddP and DddX retrieved from Anaerolineales MAGs were confirmed by heterologous expression, indicating that such anaerobic bacteria might participate in DMSP catabolism. Moreover, genes involved in methanethiol (MeSH) production from methylmercaptopropionate (MMPA) and dimethyl sulfide (DMS), MeSH oxidation, and DMS production were highly abundant, suggesting active conversions between different organic sulfur compounds. Finally, most culturable DMSP synthetic and catabolic isolates possessed no known DMSP synthetic and catabolic genes, and actinomycetes could be important groups involved in both DMSP synthesis and catabolism in Mariana Trench sediment. This study extends the current understanding of DMSP cycling in Mariana Trench sediment and highlights the need to uncover novel DMSP metabolic genes/pathways in extreme environments. IMPORTANCE Dimethylsulfoniopropionate (DMSP) is an abundant organosulfur molecule in the ocean and is the precursor for the climate-active volatile gas dimethyl sulfide. Previous studies focused mainly on bacterial DMSP cycling in seawater, coastal sediment, and surface trench sediment samples, but DMSP metabolism in the Mariana Trench (MT) subseafloor sediments remains unknown. Here, we describe the DMSP content and metabolic bacterial groups in the subseafloor of the MT sediment. We found that the tendency for vertical variation of the DMSP content in the MT was distinct from that of the continent shelf sediment. Although dsyB and dddP were the dominant DMSP synthetic and catabolic genes in the MT sediment, respectively, both metagenomic and culture methods revealed multiple previously unknown DMSP metabolic bacterial groups, especially anaerobic bacteria and actinomycetes. The active conversion of DMSP, DMS, and methanethiol may also occur in the MT sediments. These results provide novel insights for understanding DMSP cycling in the MT.

Project description:BackgroundThe Mariana Trench is the deepest known site in the Earth's oceans, reaching a depth of ~ 11,000 m at the Challenger Deep. Recent studies reveal that hadal waters harbor distinctive microbial planktonic communities. However, the genetic potential of microbial communities within the hadal zone is poorly understood.ResultsHere, implementing both culture-dependent and culture-independent methods, we perform extensive analysis of microbial populations and their genetic potential at different depths in the Mariana Trench. Unexpectedly, we observed an abrupt increase in the abundance of hydrocarbon-degrading bacteria at depths > 10,400 m in the Challenger Deep. Indeed, the proportion of hydrocarbon-degrading bacteria at > 10,400 m is the highest observed in any natural environment on Earth. These bacteria were mainly Oleibacter, Thalassolituus, and Alcanivorax genera, all of which include species known to consume aliphatic hydrocarbons. This community shift towards hydrocarbon degraders was accompanied by increased abundance and transcription of genes involved in alkane degradation. Correspondingly, three Alcanivorax species that were isolated from 10,400 m water supplemented with hexadecane were able to efficiently degrade n-alkanes under conditions simulating the deep sea, as did a reference Oleibacter strain cultured at atmospheric pressure. Abundant n-alkanes were observed in sinking particles at 2000, 4000, and 6000 m (averaged 23.5 μg/gdw) and hadal surface sediments at depths of 10,908, 10,909, and 10,911 m (averaged 2.3 μg/gdw). The δ2H values of n-C16/18 alkanes that dominated surface sediments at near 11,000-m depths ranged from - 79 to - 93‰, suggesting that these sedimentary alkanes may have been derived from an unknown heterotrophic source.ConclusionsThese results reveal that hydrocarbon-degrading microorganisms are present in great abundance in the deepest seawater on Earth and shed a new light on potential biological processes in this extreme environment.

Dataset Information

A unique subseafloor microbiosphere in the Mariana Trench driven by episodic sedimentation.

Supplementary information

Publications

A unique subseafloor microbiosphere in the Mariana Trench driven by episodic sedimentation.

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