Fujian Provincial Key Laboratory of Soil Environmental Health and Regulation, College of Resources and Environment, Fujian Agriculture and Forestry University, Fuzhou, China.
Guangdong Provincial Engineering and Technology Research Center for Agricultural Land Pollution Prevention and Control, Zhongkai University of Agriculture and Engineering, Guangzhou, China.
Appl Environ Microbiol. 2024 Aug 21;90(8):e0069524. doi: 10.1128/aem.00695-24. Epub 2024 Jul 30.
While the distribution of extracellular ARGs (eARGs) in the environment has been widely reported, the factors governing their release remain poorly understood. Here, we combined multi-omics and direct experimentation to test whether the release and transmission of eARGs are associated with viral lysis and heat during cow manure composting. Our results reveal that the proportion of eARGs increased 2.7-fold during composting, despite a significant and concomitant reduction in intracellular ARG abundances. This relative increase of eARGs was driven by composting temperature and viral lysis of ARG-carrying bacteria based on metagenome-assembled genome (MAG) analysis. Notably, thermal lysis of mesophilic bacteria carrying ARGs was a key factor in releasing eARGs at the thermophilic phase, while viral lysis played a relatively stronger role during the non-thermal phase of composting. Furthermore, MAG-based tracking of ARGs in combination with direct transformation experiments demonstrated that eARGs released during composting pose a potential transmission risk. Our study provides bioinformatic and experimental evidence of the undiscovered role of temperature and viral lysis in co-driving the spread of ARGs in compost microbiomes via the horizontal transfer of environmentally released DNA.
The spread of antibiotic resistance genes (ARGs) is a critical global health concern. Understanding the factors influencing the release of extracellular ARGs (eARGs) is essential for developing effective strategies. In this study, we investigated the association between viral lysis, heat, and eARG release during composting. Our findings revealed a substantial increase in eARGs despite reduced intracellular ARG abundance. Composting temperature and viral lysis were identified as key drivers, with thermal lysis predominant during the thermophilic phase and viral lysis during non-thermal phases. Moreover, eARGs released during composting posed a transmission risk through horizontal gene transfer. This study highlights the significance of temperature and phage lysis in ARG spread, providing valuable insights for mitigating antibiotic resistance threats.
虽然环境中外源抗生素耐药基因（eARGs）的分布已被广泛报道，但控制其释放的因素仍知之甚少。在这里，我们结合多组学和直接实验来测试 eARGs 的释放和传播是否与奶牛粪便堆肥过程中的病毒裂解和热有关。我们的结果表明，尽管细胞内 ARG 丰度显著且同时减少，但在堆肥过程中 eARGs 的比例增加了 2.7 倍。基于宏基因组组装基因组（MAG）分析，这种 eARGs 的相对增加是由堆肥温度和携带 ARG 的细菌的病毒裂解驱动的。值得注意的是，携带 ARGs 的嗜温细菌的热裂解是在高温阶段释放 eARGs 的关键因素，而病毒裂解在堆肥的非热阶段发挥了相对更强的作用。此外，基于 MAG 的 ARG 追踪与直接转化实验相结合，证明了堆肥过程中释放的 eARGs 具有潜在的传播风险。本研究提供了有关温度和病毒裂解在通过环境释放的 DNA 进行水平转移共同驱动堆肥微生物组中 ARGs 传播的未被发现的作用的生物信息学和实验证据。
抗生素耐药基因（ARGs）的传播是一个全球性的健康关注焦点。了解影响细胞外抗生素耐药基因（eARGs）释放的因素对于制定有效的策略至关重要。在这项研究中，我们研究了堆肥过程中病毒裂解、热量和 eARG 释放之间的关联。我们的发现表明，尽管细胞内 ARG 丰度减少，但 eARGs 大量增加。堆肥温度和病毒裂解被确定为关键驱动因素，其中热裂解在高温阶段占主导地位，而病毒裂解在非热阶段占主导地位。此外，堆肥过程中释放的 eARGs 通过水平基因转移具有传播风险。这项研究强调了温度和噬菌体裂解在 ARG 传播中的重要性，为减轻抗生素耐药性威胁提供了有价值的见解。
