Distinctive signatures of pathogenic and antibiotic resistant potentials in the hadal microbiome

Liuqing He; Xinyu Huang; Guoqing Zhang; Ling Yuan; Enhui Shen; Lu Zhang; Xiao-Hua Zhang; Tong Zhang; Liang Tao; Feng Ju

doi:10.1186/s40793-022-00413-5

Distinctive signatures of pathogenic and antibiotic resistant potentials in the hadal microbiome

Environ Microbiome. 2022 Apr 25;17(1):19. doi: 10.1186/s40793-022-00413-5.

Authors

Liuqing He^#^{1

2

3

4}, Xinyu Huang^#^{1

2

5}, Guoqing Zhang^{2

5}, Ling Yuan^{2

5}, Enhui Shen^{1

3

4}, Lu Zhang^{2

5}, Xiao-Hua Zhang⁶, Tong Zhang⁷, Liang Tao^{8

9

10

11}, Feng Ju^{12

13

14}

Affiliations

¹ Center for Infectious Disease Research, Westlake Laboratory of Life Sciences and Biomedicine, Hangzhou, 310024, Zhejiang, China.
² Key Laboratory of Coastal Environment and Resources of Zhejiang Province, School of Engineering, Westlake University, Hangzhou, 310024, Zhejiang, China.
³ Key Laboratory of Structural Biology of Zhejiang Province, School of Life Sciences, Westlake University, Hangzhou, 310024, Zhejiang, China.
⁴ Institute of Basic Medical Sciences, Westlake Institute for Advanced Study, Hangzhou, 310024, Zhejiang, China.
⁵ Institute of Advanced Technology, Westlake Institute for Advanced Study, Hangzhou, 310024, Zhejiang, China.
⁶ College of Marine Life Sciences, and Institute of Evolution & Marine Biodiversity, Ocean University of China, Qingdao, 266003, Shandong, China.
⁷ Environmental Microbiome Engineering and Biotechnology Laboratory, The University of Hong Kong, Hong Kong SAR, China.
⁸ Center for Infectious Disease Research, Westlake Laboratory of Life Sciences and Biomedicine, Hangzhou, 310024, Zhejiang, China. taoliang@westlake.edu.cn.
⁹ Key Laboratory of Coastal Environment and Resources of Zhejiang Province, School of Engineering, Westlake University, Hangzhou, 310024, Zhejiang, China. taoliang@westlake.edu.cn.
¹⁰ Key Laboratory of Structural Biology of Zhejiang Province, School of Life Sciences, Westlake University, Hangzhou, 310024, Zhejiang, China. taoliang@westlake.edu.cn.
¹¹ Institute of Basic Medical Sciences, Westlake Institute for Advanced Study, Hangzhou, 310024, Zhejiang, China. taoliang@westlake.edu.cn.
¹² Center for Infectious Disease Research, Westlake Laboratory of Life Sciences and Biomedicine, Hangzhou, 310024, Zhejiang, China. jufeng@westlake.edu.cn.
¹³ Key Laboratory of Coastal Environment and Resources of Zhejiang Province, School of Engineering, Westlake University, Hangzhou, 310024, Zhejiang, China. jufeng@westlake.edu.cn.
¹⁴ Institute of Advanced Technology, Westlake Institute for Advanced Study, Hangzhou, 310024, Zhejiang, China. jufeng@westlake.edu.cn.

^# Contributed equally.

Abstract

Background: Hadal zone of the deep-sea trenches accommodates microbial life under extreme energy limitations and environmental conditions, such as low temperature, high pressure, and low organic matter down to 11,000 m below sea level. However, microbial pathogenicity, resistance, and adaptation therein remain unknown. Here we used culture-independent metagenomic approaches to explore the virulence and antibiotic resistance in the hadal microbiota of the Mariana Trench.

Results: The results indicate that the 10,898 m Challenger Deep bottom sediment harbored prosperous microbiota with contrasting signatures of virulence factors and antibiotic resistance, compared with the neighboring but shallower 6038 m steep wall site and the more nearshore 5856 m Pacific basin site. Virulence genes including several famous large translocating virulence genes (e.g., botulinum neurotoxins, tetanus neurotoxin, and Clostridium difficile toxins) were uniquely detected in the trench bottom. However, the shallower and more nearshore site sediment had a higher abundance and richer diversity of known antibiotic resistance genes (ARGs), especially for those clinically relevant ones (e.g., fosX, sul1, and TEM-family extended-spectrum beta-lactamases), revealing resistance selection under anthropogenic stresses. Further analysis of mobilome (i.e., the collection of mobile genetic elements, MGEs) suggests horizontal gene transfer mediated by phage and integrase as the major mechanism for the evolution of Mariana Trench sediment bacteria. Notably, contig-level co-occurring and taxonomic analysis shows emerging evidence for substantial co-selection of virulence genes and ARGs in taxonomically diverse bacteria in the hadal sediment, especially for the Challenger Deep bottom where mobilized ARGs and virulence genes are favorably enriched in largely unexplored bacteria.

Conclusions: This study reports the landscape of virulence factors, antibiotic resistome, and mobilome in the sediment and seawater microbiota residing hadal environment of the deepest ocean bottom on earth. Our work unravels the contrasting and unique features of virulence genes, ARGs, and MGEs in the Mariana Trench bottom, providing new insights into the eco-environmental and biological processes underlying microbial pathogenicity, resistance, and adaptative evolution in the hadal environment.

Abstract

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