Zhang Yiyue, Li Hong-Zhe, Breed Martin, Tang Zhonghui, Cui Li, Zhu Yong-Guan, Sun Xin
State Key Laboratory for Ecological Security of Regions and Cities, Ningbo Observation and Research Station, Institute of Urban Environment, Chinese Academy of Sciences, 1799 Jimei Road, Xiamen, 361021, People's Republic of China.
Zhejiang Key Laboratory of Urban Environmental Processes and Pollution Control, CAS Haixi Industrial Technology Innovation Center in Beilun, Ningbo, 315830, People's Republic of China.
Microbiome. 2025 Feb 6;13(1):42. doi: 10.1186/s40168-025-02044-7.
Global warming is redrawing the map for invasive species, spotlighting the globally harmful giant African snail as a major ecological disruptor and public health threat. Known for harboring extensive antibiotic resistance genes (ARGs) and human pathogens, it remains uncertain whether global warming exacerbates these associated health risks.
We use phenotype-based single-cell Raman with DO labeling (Raman-DO) and genotype-based metagenomic sequencing to investigate whether soil warming increases active antibiotic-resistant bacteria (ARBs) in the gut microbiome of giant African snails.
We show a significant increase in beta-lactam phenotypic resistance of active ARBs with rising soil temperatures, mirrored by a surge in beta-lactamase genes such as SHV, TEM, OCH, OKP, and LEN subtypes. Through a correlation analysis between the abundance of phenotypically active ARBs and genotypically ARG-carrying gut microbes, we identify species that contribute to the increased activity of antibiotic resistome under soil warming. Among 299 high-quality ARG-carrying metagenome-assembled genomes (MAGs), we further revealed that the soil warming enhances the abundance of "supercarriers" including human pathogens with multiple ARGs and virulence factors. Furthermore, we identified elevated biosynthetic gene clusters (BGCs) within these ARG-carrying MAGs, with a third encoding at least one BGC. This suggests a link between active ARBs and secondary metabolism, enhancing the environmental adaptability and competitive advantage of these organisms in warmer environments.
The study underscores the complex interactions between soil warming and antibiotic resistance in the gut microbiome of the giant African snail, highlighting a potential escalation in environmental health risks due to global warming. These findings emphasize the urgent need for integrated environmental and health strategies to manage the rising threat of antibiotic resistance in the context of global climate change. Video Abstract.
全球变暖正在重新绘制入侵物种的分布地图，使全球有害的非洲大蜗牛成为主要的生态破坏者和公共卫生威胁。非洲大蜗牛因携带大量抗生素抗性基因（ARGs）和人类病原体而闻名，全球变暖是否会加剧这些相关的健康风险仍不确定。
我们使用基于表型的带有DO标记的单细胞拉曼光谱（Raman-DO）和基于基因型的宏基因组测序，来研究土壤升温是否会增加非洲大蜗牛肠道微生物群中具有活性的抗生素抗性细菌（ARBs）。
我们发现，随着土壤温度升高，具有活性的ARBs的β-内酰胺表型抗性显著增加，同时SHV、TEM、OCH、OKP和LEN亚型等β-内酰胺酶基因激增。通过对表型活性ARBs的丰度与携带ARG的肠道微生物基因型之间的相关性分析，我们确定了在土壤升温条件下导致抗生素抗性组活性增加的物种。在299个高质量的携带ARG的宏基因组组装基因组（MAGs）中，我们进一步发现土壤升温会增加“超级携带者”的丰度，这些“超级携带者”包括携带多种ARGs和毒力因子的人类病原体。此外，我们在这些携带ARG的MAGs中发现了增加的生物合成基因簇（BGCs），其中三分之一编码至少一个BGC。这表明活性ARBs与次级代谢之间存在联系，增强了这些生物在温暖环境中的环境适应性和竞争优势。
该研究强调了土壤升温与非洲大蜗牛肠道微生物群中抗生素抗性之间的复杂相互作用，突出了全球变暖导致环境健康风险潜在升级的问题。这些发现强调了迫切需要制定综合的环境与健康策略，以应对全球气候变化背景下抗生素抗性日益增加的威胁。视频摘要。
