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

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. 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. 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. The online version contains supplementary material available at 10.1186/s40793-022-00413-5.

深海海沟的超深渊带在极端的能量限制和环境条件下，如低温、高压以及低至海平面以下11000米的低有机质环境中，容纳着微生物生命。然而，其中微生物的致病性、抗性和适应性仍然未知。在此，我们采用不依赖培养的宏基因组学方法来探索马里亚纳海沟超深渊微生物群落中的毒力和抗生素抗性。 结果表明，与邻近但较浅的6038米陡壁位点以及更近岸的5856米太平洋盆地位点相比，10898米的挑战者深渊底部沉积物中含有丰富的微生物群落，其毒力因子和抗生素抗性特征存在差异。包括几种著名的大型易位毒力基因（如肉毒杆菌神经毒素、破伤风神经毒素和艰难梭菌毒素）在内的毒力基因在海沟底部被独特地检测到。然而，较浅且更近岸位点的沉积物中已知抗生素抗性基因（ARGs）的丰度更高且多样性更丰富，尤其是那些与临床相关的基因（如fosX、sul1和TEM家族超广谱β -内酰胺酶），这揭示了在人为压力下的抗性选择。对移动组（即移动遗传元件的集合，MGEs）的进一步分析表明，由噬菌体和整合酶介导的水平基因转移是马里亚纳海沟沉积物细菌进化的主要机制。值得注意的是，重叠群水平的共现和分类学分析显示出在超深渊沉积物中分类多样的细菌中毒力基因和ARGs大量共选择的新证据，特别是在挑战者深渊底部，移动的ARGs和毒力基因在很大程度上未被探索的细菌中富集。 这项研究报告了地球上最深海底的超深渊环境中沉积物和海水微生物群落中毒力因子、抗生素抗性组和移动组的情况。我们的工作揭示了马里亚纳海沟底部毒力基因、ARGs和MGEs的对比和独特特征，为超深渊环境中微生物致病性、抗性和适应性进化背后的生态环境和生物学过程提供了新的见解。 网络版包含补充材料，可在10.1186/s40793 - 022 - 00413 - 5获取。