Phage preferential infection of antibiotic-susceptible bacteria enriches antibiotic-resistant bacteria in activated sludge microbiomes

IF 12.8 1区环境科学与生态学 Q1 ENGINEERING, ENVIRONMENTAL

Water Research Pub Date : 2027-01-15 Epub Date: 2026-10-17 DOI:10.1016/j.watres.2026.127160

Bing Li, Haopeng Pang, Dan Huang, Chujin Ruan, Umer Zeeshan Ijaz, Huabing Yin, Hai Lin, Yong Qiu, Pingfeng Yu

{"title":"Phage preferential infection of antibiotic-susceptible bacteria enriches antibiotic-resistant bacteria in activated sludge microbiomes","authors":"Bing Li, Haopeng Pang, Dan Huang, Chujin Ruan, Umer Zeeshan Ijaz, Huabing Yin, Hai Lin, Yong Qiu, Pingfeng Yu","doi":"10.1016/j.watres.2026.127160","DOIUrl":null,"url":null,"abstract":"<div><div>Despite the significance of phages in microbial ecosystems, the contribution of lytic phages to the propagation of antibiotic resistance genes (ARGs) within activated sludge microbiomes remains unclear. By integrating global metadata analysis and metagenomics, we first demonstrated that lytic phages exhibit a strong infection preference for antibiotic-susceptible bacteria (ASB, 70.84%) over antibiotic-resistant bacteria (ARB, 29.16%). This preferential phage infection was consistent with ARB carrying an exceptionally higher abundance of antiviral defense systems than ASB (averaging 1.83 versus 0.03 systems per whole genome). Furthermore, phage transplant experiments revealed that elevated phage predation pressure (phage-to-bacteria ratios ≥100) drove significant shifts in community composition toward highly defended lineages, thereby enriching the relative abundance of ARGs and mobile genetic elements (MGEs) by 25∼30-fold compared to controls. Additionally, real-time microfluidic tracking confirmed a “Kill-the-Winner” ecological dynamic, where phages selectively eradicate fast-growing ASB, thereby indirectly promoting ARB survival and increasing ARG transfer frequency. Overall, these findings highlight an underappreciated ecological risk driven by selective predation of lytic phages, which indirectly accelerates ARG dissemination in complex environmental microbiomes.</div></div>","PeriodicalId":443,"journal":{"name":"Water Research","volume":"309 ","pages":"Article 127160"},"PeriodicalIF":12.8000,"publicationDate":"2027-01-15","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Water Research","FirstCategoryId":"93","ListUrlMain":"https://www.sciencedirect.com/science/article/pii/S0043135426018324","RegionNum":1,"RegionCategory":"环境科学与生态学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"2026/10/17 0:00:00","PubModel":"Epub","JCR":"Q1","JCRName":"ENGINEERING, ENVIRONMENTAL","Score":null,"Total":0}

引用次数: 0

Abstract

Despite the significance of phages in microbial ecosystems, the contribution of lytic phages to the propagation of antibiotic resistance genes (ARGs) within activated sludge microbiomes remains unclear. By integrating global metadata analysis and metagenomics, we first demonstrated that lytic phages exhibit a strong infection preference for antibiotic-susceptible bacteria (ASB, 70.84%) over antibiotic-resistant bacteria (ARB, 29.16%). This preferential phage infection was consistent with ARB carrying an exceptionally higher abundance of antiviral defense systems than ASB (averaging 1.83 versus 0.03 systems per whole genome). Furthermore, phage transplant experiments revealed that elevated phage predation pressure (phage-to-bacteria ratios ≥100) drove significant shifts in community composition toward highly defended lineages, thereby enriching the relative abundance of ARGs and mobile genetic elements (MGEs) by 25∼30-fold compared to controls. Additionally, real-time microfluidic tracking confirmed a “Kill-the-Winner” ecological dynamic, where phages selectively eradicate fast-growing ASB, thereby indirectly promoting ARB survival and increasing ARG transfer frequency. Overall, these findings highlight an underappreciated ecological risk driven by selective predation of lytic phages, which indirectly accelerates ARG dissemination in complex environmental microbiomes.

查看原文本刊更多论文

抗生素敏感菌的噬菌体优先感染丰富了活性污泥微生物群中的抗生素耐药菌

尽管噬菌体在微生物生态系统中具有重要意义，但裂解噬菌体对活性污泥微生物群中抗生素耐药基因（ARGs）繁殖的贡献尚不清楚。通过整合全球元数据分析和宏基因组学，我们首次证明了溶噬菌体对抗生素敏感菌（ASB, 70.84%）比耐药菌（ARB, 29.16%）具有强烈的感染偏好。这种优先噬菌体感染与ARB携带抗病毒防御系统的丰度比ASB高一致（平均每个全基因组1.83个系统对0.03个系统）。此外，噬菌体移植实验显示，噬菌体捕食压力的升高（噬菌体与细菌的比率≥100）推动了群落组成向高度防御谱系的显著转变，从而使ARGs和移动遗传元件（MGEs）的相对丰度比对照提高了25 ~ 30倍。此外，实时微流控追踪证实了一种“Kill-the-Winner”的生态动态，噬菌体选择性地消灭快速生长的ASB，从而间接促进ARB的存活，增加ARG的转移频率。总的来说，这些发现强调了一种被低估的生态风险，这种风险是由选择性捕食溶解噬菌体驱动的，它间接加速了ARG在复杂环境微生物群中的传播。

本文章由计算机程序翻译，如有差异，请以英文原文为准。

求助全文

约1分钟内获得全文求助全文

来源期刊

Water Research 环境科学-工程：环境

CiteScore

20.80

自引率

9.40%

发文量

1307

审稿时长

38 days

期刊介绍： Water Research, along with its open access companion journal Water Research X, serves as a platform for publishing original research papers covering various aspects of the science and technology related to the anthropogenic water cycle, water quality, and its management worldwide. The audience targeted by the journal comprises biologists, chemical engineers, chemists, civil engineers, environmental engineers, limnologists, and microbiologists. The scope of the journal include: •Treatment processes for water and wastewaters (municipal, agricultural, industrial, and on-site treatment), including resource recovery and residuals management; •Urban hydrology including sewer systems, stormwater management, and green infrastructure; •Drinking water treatment and distribution; •Potable and non-potable water reuse; •Sanitation, public health, and risk assessment; •Anaerobic digestion, solid and hazardous waste management, including source characterization and the effects and control of leachates and gaseous emissions; •Contaminants (chemical, microbial, anthropogenic particles such as nanoparticles or microplastics) and related water quality sensing, monitoring, fate, and assessment; •Anthropogenic impacts on inland, tidal, coastal and urban waters, focusing on surface and ground waters, and point and non-point sources of pollution; •Environmental restoration, linked to surface water, groundwater and groundwater remediation; •Analysis of the interfaces between sediments and water, and between water and atmosphere, focusing specifically on anthropogenic impacts; •Mathematical modelling, systems analysis, machine learning, and beneficial use of big data related to the anthropogenic water cycle; •Socio-economic, policy, and regulations studies.