Responses of viral communities in aerobic biofilms under antibiotic stress

IF 11.4 1区环境科学与生态学 Q1 ENGINEERING, ENVIRONMENTAL

Water Research Pub Date : 2025-06-24 DOI:10.1016/j.watres.2025.124099

Chen Wang , Xiao Luan , Junya Zhang , Hong Zhang , Yu Zhang , Min Yang , Zhe Tian

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Abstract

Bacteriophages are pivotal in shaping microbial communities, but their structural and functional responses to antibiotic stress in aerobic biofilms remain underexplored. This study aims to fill this void by providing a comprehensive understanding of how viral communities in aerobic biofilms adapt to increasing antibiotic pressures through interactions with their bacterial hosts. Three lab-scale aerobic biofilm systems were established and operated for 577 days, two of those were exposed to increasing influent concentrations of oxytetracycline (OTC) and streptomycin (STM), respectively. The dynamics of the biofilm virome under antibiotic stress was revealed by metagenomic sequencing. Results showed that the virome in aerobic biofilms displayed a high percentage (98.7 %) of unknown bacteriophages, indicating considerable viral diversity. As for the hosts of phages, a total of 1741 bacteriophage contigs were associated with 660 distinct bacterial hosts. In antibiotic-treated systems, broad-host-range generalist bacteriophages accounted for over 17.95 % (STM) and 17.90 % (OTC), compared to 14.32 % in the control. Furthermore, viral community did not carry diverse antibiotic resistance genes, which only accounted for 0.34 % of the resistome. Additionally, it did not regulate the number of resistant bacteria by activating the lytic and lysogenic cycles in this study. This indicated that the contribution of transduction to the horizontal spread of resistant determinants is very limited in the aerobic biofilm. Under antibiotic stress, viral auxiliary metabolic genes compensated for incomplete metabolic pathways in host cells, particularly those related to carbohydrate, amino acid, and cofactor metabolism. These genes likely offer dual benefits to bacterial hosts by repairing antibiotic-induced cellular damage and supporting energy generation, thereby providing adaptive advantages for bacterial survival and proliferation under antibiotic selection pressure. This study uncovers the complex interactions between bacteriophages, their hosts, and environmental pressures. It suggests that viral communities in these environments compensate for functional metabolism rather than promote resistance development under antibiotic stress, providing new insights into the potential roles of bacteriophages in the regulation of microbial-driven processes.

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抗生素胁迫下好氧生物膜中病毒群落的反应

噬菌体是形成微生物群落的关键，但它们在有氧生物膜中对抗生素应激的结构和功能反应仍未得到充分研究。这项研究旨在填补这一空白，全面了解好氧生物膜中的病毒群落如何通过与细菌宿主的相互作用来适应不断增加的抗生素压力。建立了三个实验室规模的好氧生物膜系统，并运行了577天，其中两个分别暴露于不断增加的进水浓度的土霉素（OTC）和链霉素（STM）。宏基因组测序揭示了生物膜病毒组在抗生素胁迫下的动态变化。结果表明，需氧生物膜中的病毒组中未知噬菌体的比例很高（98.7%），表明病毒具有相当的多样性。在噬菌体宿主方面，共有1741个噬菌体contigs与660个不同的细菌宿主相关。在抗生素处理的系统中，宽宿主多面体噬菌体占17.95% （STM）和17.90% (OTC)，而对照组为14.32%。此外，病毒群落没有携带多种抗生素耐药基因，仅占抗性组的0.34%。此外，在本研究中，它没有通过激活裂解和溶原循环来调节耐药菌的数量。这表明，在好氧生物膜中，对抗性决定因子水平传播的转导作用非常有限。在抗生素胁迫下，病毒辅助代谢基因补偿了宿主细胞中不完整的代谢途径，特别是与碳水化合物、氨基酸和辅因子代谢相关的代谢途径。这些基因可能通过修复抗生素诱导的细胞损伤和支持能量生成，为细菌宿主提供了双重益处，从而为细菌在抗生素选择压力下的生存和增殖提供了适应性优势。这项研究揭示了噬菌体、它们的宿主和环境压力之间复杂的相互作用。这表明，这些环境中的病毒群落补偿了功能性代谢，而不是促进抗生素应激下的耐药性发展，这为噬菌体在调节微生物驱动过程中的潜在作用提供了新的见解。

本文章由计算机程序翻译，如有差异，请以英文原文为准。

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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.