Key Laboratory of Urban Environment and Health, Ningbo Observation and Research Station, Institute of Urban Environment, Chinese Academy of Sciences, Xiamen, 361021, China.
Zhejiang Key Laboratory of Urban Environmental Processes and Pollution Control, CAS Haixi Industrial Technology Innovation Center in Beilun, Ningbo, 315830, China.
Microbiome. 2024 Nov 22;12(1):245. doi: 10.1186/s40168-024-01965-z.
The extensive use of antibiotics in the global livestock industry in recent decades has accelerated the accumulation and dissemination of antibiotic-resistance genes (ARGs) within terrestrial ecosystems. This occurs due to the limited absorption of most antibiotics, leading to their release into the environment through feces and urine. This poses a significant threat to both the environment and human health. However, the response of antibiotic-resistant microorganisms and their ARGs in grasslands to prolonged grazing, as well as the primary microbial taxa driving the ARG distribution, remain poorly understood, especially within various microhabitats. In this study, we characterized ARGs in the phyllosphere, litter, and soil after decades of livestock grazing in a meadow steppe. We particularly focused on identifying the major members of the microbial community influencing ARGs and the distinction between microbial generalists and specialists.
Our findings indicate that a core set of ARGs accounted for 90% of the abundance in this plant-soil ecosystem. While the soil exhibited the highest ARG abundance, the phyllosphere, and litter displayed higher ARG diversity and diverse distribution patterns after overgrazing. Grazing increased ARG abundance by elevating the proportion of core ARGs and suppressing stochastic ARGs in the phyllosphere and litter, while it had little effect on the ARGs in the soil. Additionally, microbial generalist abundance increased, but specialist abundance decreased in the phyllosphere and litter, with no effect in the soil, under grazed conditions. Ultimately, microbial microhabitats and grazing influenced ARG community characteristics through direct (i.e., feces and other exogenous ARG input) and indirect (i.e., trampling and selective feeding) effects on nutrient availability, microbial community composition, and mobile genetic elements. The generalist community, with its broad ecological niches and phylogenetic composition, made the most significant contribution to the ARG characteristics.
This study underscores the impact of environmental disturbances on the distributional patterns of ARGs in ecosystems, mediated by the regulation of microbial generalized species. These insights enhance our understanding of microbial control over ARGs and facilitate predictions regarding the dynamics and risk of ARGs in diverse ecological niches subjected to anthropogenic disturbances. Video Abstract.
近几十年来，全球畜牧业大量使用抗生素，加速了抗生素耐药基因（ARGs）在陆地生态系统中的积累和传播。这是由于大多数抗生素的吸收有限，导致它们通过粪便和尿液释放到环境中。这对环境和人类健康都构成了重大威胁。然而，抗生素耐药微生物及其 ARGs 对长期放牧的反应，以及驱动 ARG 分布的主要微生物分类群，在草地中仍知之甚少，特别是在各种微生境中。在这项研究中，我们在草原草甸中经过几十年的牲畜放牧后，对叶际、凋落物和土壤中的 ARGs 进行了特征描述。我们特别关注确定影响 ARGs 的主要微生物群落成员以及微生物广义种和专门种之间的区别。
我们的研究结果表明，一组核心 ARGs 占该植物-土壤生态系统丰度的 90%。虽然土壤表现出最高的 ARG 丰度，但叶际和凋落物在过度放牧后显示出更高的 ARG 多样性和多样化的分布模式。放牧通过提高核心 ARGs 的比例和抑制叶际和凋落物中的随机 ARGs 来增加 ARG 丰度，而对土壤中的 ARGs 影响不大。此外，在放牧条件下，叶际和凋落物中的微生物广义种丰度增加，而专门种丰度减少，而土壤中的微生物丰度没有变化。最终，微生物小生境和放牧通过直接（即粪便和其他外源性 ARG 输入）和间接（即踩踏和选择性喂养）影响养分供应、微生物群落组成和可移动遗传元件，对 ARG 群落特征产生影响。具有广泛生态位和系统发育组成的广义种群落对 ARG 特征的贡献最大。
本研究强调了环境干扰通过调节微生物广义种对生态系统中 ARG 分布模式的影响。这些见解增强了我们对微生物控制 ARGs 的理解，并有助于预测在受人为干扰的不同生态位中 ARGs 的动态和风险。
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