Liu Lele, Zou Xinyi, Cheng Yuan, Li Huihui, Zhang Xueying, Yuan Qingbin
College of Environmental Science and Engineering, Nanjing Tech University, Nanjing 211816, China.
State Key Laboratory of Pollution Control and Resource Reuse, School of the Environment, Nanjing University, Nanjing 210023, China.
Antibiotics (Basel). 2024 Aug 28;13(9):817. doi: 10.3390/antibiotics13090817.
The propagation of antibiotic resistance in environments, particularly aquatic environments that serve as primary pathways for antibiotic resistance genes (ARGs), poses significant health risks. The impact of nutrients, as key determinants of bacterial growth and metabolism, on the propagation of ARGs, particularly extracellular ARGs (eARGs), remains poorly understood. In this study, we collected microorganisms from the Yangtze River and established a series of microcosms to investigate how variations in nutrient levels and delivery frequency affect the relative abundance of intracellular ARGs (iARGs) and eARGs in bacterial communities. Our results show that the relative abundance of 7 out of 11 representative eARGs in water exceeds that of iARGs, while 8 iARGs dominate in biofilms. Notably, iARGs and eARGs consistently exhibited opposite responses to nutrient variation. When nutrient levels increased, iARGs in the water also increased, with the polluted group (COD = 333.3 mg/L, COD:N:P = 100:3:0.6, m/m) and the eutrophic group (COD = 100 mg/L, COD:N:P = 100:25:5, m/m) showing 1.2 and 3.2 times higher levels than the normal group (COD = 100 mg/L, COD:N:P = 100:10:2, m/m), respectively. In contrast, eARGs decreased by 6.7% and 8.4% in these groups. On the other hand, in biofilms, higher nutrient levels led to an increase in eARGs by 1.5 and 1.7 times, while iARGs decreased by 17.5% and 50.1% in the polluted and eutrophic groups compared to the normal group. Moreover, while increasing the frequency of nutrient delivery (from 1 time/10 d to 20 times/10 d) generally did not favor iARGs in either water or biofilm, it selectively enhanced eARGs in both. To further understand these dynamics, we developed an ARGs-nutrient model by integrating the Lotka-Volterra and Monod equations. The results highlight the complex interplay of bacterial growth, nutrient availability, and mechanisms such as horizontal gene transfer and secretion influencing ARGs' propagation, driving the opposite trend between these two forms of ARGs. This contrasting response between iARGs and eARGs contributes to a dynamic balance that stabilizes bacterial resistance levels amid nutrient fluctuations. This study offers helpful implications regarding the persistence of bacterial resistance in the environment.
抗生素耐药性在环境中传播,尤其是在作为抗生素耐药基因(ARGs)主要传播途径的水生环境中传播,会带来重大健康风险。营养物质作为细菌生长和代谢的关键决定因素,对ARGs尤其是细胞外ARGs(eARGs)传播的影响,目前仍知之甚少。在本研究中,我们从长江采集微生物,并建立了一系列微观生态系统,以研究营养水平和添加频率的变化如何影响细菌群落中细胞内ARGs(iARGs)和eARGs的相对丰度。我们的结果表明,水中11种代表性eARGs中有7种的相对丰度超过了iARGs,而在生物膜中8种iARGs占主导地位。值得注意的是,iARGs和eARGs对营养变化始终表现出相反的反应。当营养水平增加时,水中的iARGs也会增加,污染组(化学需氧量[COD]=333.3mg/L,COD:N:P=100:3:0.6,质量比)和富营养化组(COD=100mg/L,COD:N:P=100:25:5,质量比)的iARGs水平分别比正常组(COD=100mg/L,COD:N:P=100:10:2,质量比)高1.2倍和3.2倍。相比之下,这些组中的eARGs分别下降了6.7%和8.4%。另一方面,在生物膜中,较高的营养水平导致eARGs增加了1.5倍和1.7倍,而与正常组相比,污染组和富营养化组的iARGs分别下降了17.5%和50.1%。此外,虽然增加营养添加频率(从1次/10天增加到20次/10天)一般对水中或生物膜中的iARGs不利,但它在两者中都选择性地增强了eARGs。为了进一步了解这些动态变化,我们通过整合洛特卡-沃尔泰拉方程和莫诺德方程建立了一个ARGs-营养模型。结果突出了细菌生长、营养可利用性以及水平基因转移和分泌等机制之间复杂的相互作用,这些机制影响着ARGs的传播,导致这两种形式的ARGs呈现相反的趋势。iARGs和eARGs之间这种截然不同的反应有助于形成一种动态平衡,在营养波动的情况下稳定细菌的耐药水平。本研究为环境中细菌耐药性的持续存在提供了有益的启示。