Microbial ecosystems and ecological driving forces in the deepest ocean sediments

Xiang Xiao; Weishu Zhao; Zewei Song; Qi Qi; Bo Wang; Jiahui Zhu; James Lin; Jing Wang; Aoran Hu; Shanshan Huang; Yinzhao Wang; Jianwei Chen; Chao Fang; Qianyue Ji; Nannan Zhang; Liang Meng; Xiaofeng Wei; Chuanxu Chen; Shanya Cai; Shun Chen; Kang Ding; Dong Li; Shuangquan Liu; Taoran Song; Liyang Tian; Haibin Zhang; Yu Zhang; Shiyu Xu; Jiayu Chen; Haixin Chen; Qian Cen; Fangfang Jiang; Guohai Hu; Chenguang Tang; Wu Guo; Xiaohan Wang; Liping Zhan; Jie Fan; Jun Wang; Changhao Zhou; Liuyang Li; Zhenbo Lv; Yaoxun Hu; Xiaonan Lin; Guoqiang Mai; Linlin Luo; Tao Yang; Weiwen Wang; Karsten Kristiansen; Liqun Chen; Huanming Yang; Ming Ni; Ying Gu; Feng Mu; Yunfeng Yang; Jizhong Zhou; Jian Wang; Wei Jia Zhang; Mo Han; Xun Xu; Shanshan Liu

doi:10.1016/j.cell.2024.12.036

Microbial ecosystems and ecological driving forces in the deepest ocean sediments

Xiang Xiao^*, Weishu Zhao, Zewei Song, Qi Qi, Bo Wang, Jiahui Zhu, James Lin, Jing Wang, Aoran Hu, Shanshan Huang, Yinzhao Wang, Jianwei Chen, Chao Fang, Qianyue Ji, Nannan Zhang, Liang Meng, Xiaofeng Wei, Chuanxu Chen, Shanya Cai, Shun ChenKang Ding, Dong Li, Shuangquan Liu, Taoran Song, Liyang Tian, Haibin Zhang, Yu Zhang, Shiyu Xu, Jiayu Chen, Haixin Chen, Qian Cen, Fangfang Jiang, Guohai Hu, Chenguang Tang, Wu Guo, Xiaohan Wang, Liping Zhan, Jie Fan, Jun Wang, Changhao Zhou, Liuyang Li, Zhenbo Lv, Yaoxun Hu, Xiaonan Lin, Guoqiang Mai, Linlin Luo, Tao Yang, Weiwen Wang, Karsten Kristiansen, Liqun Chen, Huanming Yang, Ming Ni, Ying Gu, Feng Mu, Yunfeng Yang, Jizhong Zhou, Jian Wang, Wei Jia Zhang, Mo Han, Xun Xu, Shanshan Liu

^*Corresponding author for this work

Genome Research and Molecular Bio Medicine

Research output: Contribution to journal › Journal article › Research › peer-review

Abstract

Systematic exploration of the hadal zone, Earth's deepest oceanic realm, has historically faced technical limitations. Here, we collected 1,648 sediment samples at 6–11 km in the Mariana Trench, Yap Trench, and Philippine Basin for the Mariana Trench Environment and Ecology Research (MEER) project. Metagenomic and 16S rRNA gene amplicon sequencing generated the 92-Tbp MEER dataset, comprising 7,564 species (89.4% unreported), indicating high taxonomic novelty. Unlike in reported environments, neutral drift played a minimal role, while homogeneous selection (HoS, 50.5%) and dispersal limitation (DL, 43.8%) emerged as dominant ecological drivers. HoS favored streamlined genomes with key functions for hadal adaptation, e.g., aromatic compound utilization (oligotrophic adaptation) and antioxidation (high-pressure adaptation). Conversely, DL promoted versatile metabolism with larger genomes. These findings indicated that environmental factors drive the high taxonomic novelty in the hadal zone, advancing our understanding of the ecological mechanisms governing microbial ecosystems in such an extreme oceanic environment.

Original language	English
Journal	Cell
Volume	188
Issue number	5
Pages (from-to)	1363-1377.e9
Number of pages	15
ISSN	0092-8674
DOIs	https://doi.org/10.1016/j.cell.2024.12.036
Publication status	Published - 2025

Bibliographical note

Publisher Copyright:
© 2025 The Authors

Keywords

16S rRNA gene amplicon
adaptation strategies
community assembly
ecological processes
hadal microbiome
hadal zone
Mariana Trench
metagenomic sequencing

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10.1016/j.cell.2024.12.036Licence: CC BY

FulltextFinal published version, 11 MBLicence: CC BY

Cite this

Xiao, X, Zhao, W, Song, Z, Qi, Q, Wang, B, Zhu, J, Lin, J, Wang, J, Hu, A, Huang, S, Wang, Y, Chen, J, Fang, C, Ji, Q, Zhang, N, Meng, L, Wei, X, Chen, C, Cai, S, Chen, S, Ding, K, Li, D, Liu, S, Song, T, Tian, L, Zhang, H, Zhang, Y, Xu, S, Chen, J, Chen, H, Cen, Q, Jiang, F, Hu, G, Tang, C, Guo, W, Wang, X, Zhan, L, Fan, J, Wang, J, Zhou, C, Li, L, Lv, Z, Hu, Y, Lin, X, Mai, G, Luo, L, Yang, T, Wang, W, Kristiansen, K, Chen, L, Yang, H, Ni, M, Gu, Y, Mu, F, Yang, Y, Zhou, J, Wang, J, Zhang, WJ, Han, M, Xu, X & Liu, S 2025, 'Microbial ecosystems and ecological driving forces in the deepest ocean sediments', Cell, vol. 188, no. 5, pp. 1363-1377.e9. https://doi.org/10.1016/j.cell.2024.12.036

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title = "Microbial ecosystems and ecological driving forces in the deepest ocean sediments",

abstract = "Systematic exploration of the hadal zone, Earth's deepest oceanic realm, has historically faced technical limitations. Here, we collected 1,648 sediment samples at 6–11 km in the Mariana Trench, Yap Trench, and Philippine Basin for the Mariana Trench Environment and Ecology Research (MEER) project. Metagenomic and 16S rRNA gene amplicon sequencing generated the 92-Tbp MEER dataset, comprising 7,564 species (89.4% unreported), indicating high taxonomic novelty. Unlike in reported environments, neutral drift played a minimal role, while homogeneous selection (HoS, 50.5%) and dispersal limitation (DL, 43.8%) emerged as dominant ecological drivers. HoS favored streamlined genomes with key functions for hadal adaptation, e.g., aromatic compound utilization (oligotrophic adaptation) and antioxidation (high-pressure adaptation). Conversely, DL promoted versatile metabolism with larger genomes. These findings indicated that environmental factors drive the high taxonomic novelty in the hadal zone, advancing our understanding of the ecological mechanisms governing microbial ecosystems in such an extreme oceanic environment.",

keywords = "16S rRNA gene amplicon, adaptation strategies, community assembly, ecological processes, hadal microbiome, hadal zone, Mariana Trench, metagenomic sequencing",

author = "Xiang Xiao and Weishu Zhao and Zewei Song and Qi Qi and Bo Wang and Jiahui Zhu and James Lin and Jing Wang and Aoran Hu and Shanshan Huang and Yinzhao Wang and Jianwei Chen and Chao Fang and Qianyue Ji and Nannan Zhang and Liang Meng and Xiaofeng Wei and Chuanxu Chen and Shanya Cai and Shun Chen and Kang Ding and Dong Li and Shuangquan Liu and Taoran Song and Liyang Tian and Haibin Zhang and Yu Zhang and Shiyu Xu and Jiayu Chen and Haixin Chen and Qian Cen and Fangfang Jiang and Guohai Hu and Chenguang Tang and Wu Guo and Xiaohan Wang and Liping Zhan and Jie Fan and Jun Wang and Changhao Zhou and Liuyang Li and Zhenbo Lv and Yaoxun Hu and Xiaonan Lin and Guoqiang Mai and Linlin Luo and Tao Yang and Weiwen Wang and Karsten Kristiansen and Liqun Chen and Huanming Yang and Ming Ni and Ying Gu and Feng Mu and Yunfeng Yang and Jizhong Zhou and Jian Wang and Zhang, {Wei Jia} and Mo Han and Xun Xu and Shanshan Liu",

note = "Publisher Copyright: {\textcopyright} 2025 The Authors",

year = "2025",

doi = "10.1016/j.cell.2024.12.036",

language = "English",

volume = "188",

pages = "1363--1377.e9",

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AU - Xiao, Xiang

AU - Zhao, Weishu

AU - Song, Zewei

AU - Qi, Qi

AU - Wang, Bo

AU - Zhu, Jiahui

AU - Lin, James

AU - Wang, Jing

AU - Hu, Aoran

AU - Huang, Shanshan

AU - Wang, Yinzhao

AU - Chen, Jianwei

AU - Fang, Chao

AU - Ji, Qianyue

AU - Zhang, Nannan

AU - Meng, Liang

AU - Wei, Xiaofeng

AU - Chen, Chuanxu

AU - Cai, Shanya

AU - Chen, Shun

AU - Ding, Kang

AU - Li, Dong

AU - Liu, Shuangquan

AU - Song, Taoran

AU - Tian, Liyang

AU - Zhang, Haibin

AU - Zhang, Yu

AU - Xu, Shiyu

AU - Chen, Jiayu

AU - Chen, Haixin

AU - Cen, Qian

AU - Jiang, Fangfang

AU - Hu, Guohai

AU - Tang, Chenguang

AU - Guo, Wu

AU - Wang, Xiaohan

AU - Zhan, Liping

AU - Fan, Jie

AU - Wang, Jun

AU - Zhou, Changhao

AU - Li, Liuyang

AU - Lv, Zhenbo

AU - Hu, Yaoxun

AU - Lin, Xiaonan

AU - Mai, Guoqiang

AU - Luo, Linlin

AU - Yang, Tao

AU - Wang, Weiwen

AU - Kristiansen, Karsten

AU - Chen, Liqun

AU - Yang, Huanming

AU - Ni, Ming

AU - Gu, Ying

AU - Mu, Feng

AU - Yang, Yunfeng

AU - Zhou, Jizhong

AU - Wang, Jian

AU - Zhang, Wei Jia

AU - Han, Mo

AU - Xu, Xun

AU - Liu, Shanshan

PY - 2025

Y1 - 2025

N2 - Systematic exploration of the hadal zone, Earth's deepest oceanic realm, has historically faced technical limitations. Here, we collected 1,648 sediment samples at 6–11 km in the Mariana Trench, Yap Trench, and Philippine Basin for the Mariana Trench Environment and Ecology Research (MEER) project. Metagenomic and 16S rRNA gene amplicon sequencing generated the 92-Tbp MEER dataset, comprising 7,564 species (89.4% unreported), indicating high taxonomic novelty. Unlike in reported environments, neutral drift played a minimal role, while homogeneous selection (HoS, 50.5%) and dispersal limitation (DL, 43.8%) emerged as dominant ecological drivers. HoS favored streamlined genomes with key functions for hadal adaptation, e.g., aromatic compound utilization (oligotrophic adaptation) and antioxidation (high-pressure adaptation). Conversely, DL promoted versatile metabolism with larger genomes. These findings indicated that environmental factors drive the high taxonomic novelty in the hadal zone, advancing our understanding of the ecological mechanisms governing microbial ecosystems in such an extreme oceanic environment.

AB - Systematic exploration of the hadal zone, Earth's deepest oceanic realm, has historically faced technical limitations. Here, we collected 1,648 sediment samples at 6–11 km in the Mariana Trench, Yap Trench, and Philippine Basin for the Mariana Trench Environment and Ecology Research (MEER) project. Metagenomic and 16S rRNA gene amplicon sequencing generated the 92-Tbp MEER dataset, comprising 7,564 species (89.4% unreported), indicating high taxonomic novelty. Unlike in reported environments, neutral drift played a minimal role, while homogeneous selection (HoS, 50.5%) and dispersal limitation (DL, 43.8%) emerged as dominant ecological drivers. HoS favored streamlined genomes with key functions for hadal adaptation, e.g., aromatic compound utilization (oligotrophic adaptation) and antioxidation (high-pressure adaptation). Conversely, DL promoted versatile metabolism with larger genomes. These findings indicated that environmental factors drive the high taxonomic novelty in the hadal zone, advancing our understanding of the ecological mechanisms governing microbial ecosystems in such an extreme oceanic environment.

KW - 16S rRNA gene amplicon

KW - adaptation strategies

KW - community assembly

KW - ecological processes

KW - hadal microbiome

KW - hadal zone

KW - Mariana Trench

KW - metagenomic sequencing

U2 - 10.1016/j.cell.2024.12.036

DO - 10.1016/j.cell.2024.12.036

M3 - Journal article

C2 - 40054447

AN - SCOPUS:85218963294

SN - 0092-8674

VL - 188

SP - 1363-1377.e9

JO - Cell

JF - Cell

IS - 5

ER -