Disentangling abiotic and biotic effects of treated wastewater on stream biofilm resistomes enables the discovery of a new planctomycete beta-lactamase.

IF 13.8 1区 生物学 Q1 MICROBIOLOGY Microbiome Pub Date : 2024-09-06 DOI:10.1186/s40168-024-01879-w
Mustafa Attrah, Milo R Schärer, Mauro Esposito, Giulia Gionchetta, Helmut Bürgmann, Piet N L Lens, Kathrin Fenner, Jack van de Vossenberg, Serina L Robinson
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Abstract

Background: Environmental reservoirs of antibiotic resistance pose a threat to human and animal health. Aquatic biofilms impacted by wastewater effluent (WW) are known environmental reservoirs for antibiotic resistance; however, the relative importance of biotic factors and abiotic factors from WW on the abundance of antibiotic resistance genes (ARGs) within aquatic biofilms remains unclear. Additionally, experimental evidence is limited within complex aquatic microbial communities as to whether genes bearing low sequence similarity to validated reference ARGs are functional as ARGs.

Results: To disentangle the effects of abiotic and biotic factors on ARG abundances, natural biofilms were previously grown in flume systems with different proportions of stream water and either ultrafiltered or non-ultrafiltered WW. In this study, we conducted deep shotgun metagenomic sequencing of 75 biofilm, stream, and WW samples from these flume systems and compared the taxonomic and functional microbiome and resistome composition. Statistical analysis revealed an alignment of the resistome and microbiome composition and a significant association with experimental treatment. Several ARG classes exhibited an increase in normalized metagenomic abundances in biofilms grown with increasing percentages of non-ultrafiltered WW. In contrast, sulfonamide and extended-spectrum beta-lactamase ARGs showed greater abundances in biofilms grown in ultrafiltered WW compared to non-ultrafiltered WW. Overall, our results pointed toward the dominance of biotic factors over abiotic factors in determining ARG abundances in WW-impacted stream biofilms and suggested gene family-specific mechanisms for ARGs that exhibited divergent abundance patterns. To investigate one of these specific ARG families experimentally, we biochemically characterized a new beta-lactamase from the Planctomycetota (Phycisphaeraceae). This beta-lactamase displayed activity in the cleavage of cephalosporin analog despite sharing a low sequence identity with known ARGs.

Conclusions: This discovery of a functional planctomycete beta-lactamase ARG is noteworthy, not only because it was the first beta-lactamase to be biochemically characterized from this phylum, but also because it was not detected by standard homology-based ARG tools. In summary, this study conducted a metagenomic analysis of the relative importance of biotic and abiotic factors in the context of WW discharge and their impact on both known and new ARGs in aquatic biofilms. Video Abstract.

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厘清废水处理对溪流生物膜抗性组的非生物和生物影响,有助于发现一种新的平霉菌 beta-内酰胺酶。
背景:抗生素耐药性环境库威胁着人类和动物的健康。受废水(WW)影响的水生生物膜是已知的抗生素耐药性环境库;然而,WW 的生物因素和非生物因素对水生生物膜中抗生素耐药性基因(ARGs)丰度的相对重要性仍不清楚。此外,在复杂的水生微生物群落中,对于与有效参考 ARGs 序列相似度较低的基因是否具有 ARGs 功能,实验证据也很有限:为了区分非生物因素和生物因素对 ARG 丰度的影响,以前曾在水槽系统中培养过天然生物膜,水槽中含有不同比例的溪水和超滤或非超滤 WW。在这项研究中,我们对来自这些水槽系统的 75 个生物膜、溪水和 WW 样品进行了深度枪式元基因组测序,并比较了微生物组的分类和功能以及抗性组的组成。统计分析表明,抗药性组和微生物组的组成是一致的,并且与实验处理有显著关联。在非超滤 WW 百分比不断增加的生物膜中,几类 ARG 显示出归一化元基因组丰度的增加。相比之下,磺胺类和广谱β-内酰胺酶类 ARG 在超滤 WW 生长的生物膜中的丰度高于非超滤 WW。总之,我们的研究结果表明,在决定受 WW 影响的溪流生物膜中 ARG 的丰度方面,生物因素比非生物因素更重要,并提出了表现出不同丰度模式的 ARG 的基因家族特异性机制。为了对这些特定 ARG 家族之一进行实验研究,我们对 Planctomycetota(Phycisphaeraceae)中一种新的β-内酰胺酶进行了生物化学鉴定。尽管该β-内酰胺酶与已知的 ARGs 序列相似性较低,但它在头孢菌素类似物的裂解过程中显示出活性:结论:值得注意的是,发现了一种功能性的平真菌β-内酰胺酶ARG,这不仅是因为它是该门类中第一个具有生物化学特征的β-内酰胺酶,还因为标准的基于同源性的ARG工具没有检测到它。总之,本研究对WW排放背景下生物和非生物因素的相对重要性及其对水生生物膜中已知和新的ARGs的影响进行了元基因组分析。视频摘要。
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来源期刊
Microbiome
Microbiome MICROBIOLOGY-
CiteScore
21.90
自引率
2.60%
发文量
198
审稿时长
4 weeks
期刊介绍: Microbiome is a journal that focuses on studies of microbiomes in humans, animals, plants, and the environment. It covers both natural and manipulated microbiomes, such as those in agriculture. The journal is interested in research that uses meta-omics approaches or novel bioinformatics tools and emphasizes the community/host interaction and structure-function relationship within the microbiome. Studies that go beyond descriptive omics surveys and include experimental or theoretical approaches will be considered for publication. The journal also encourages research that establishes cause and effect relationships and supports proposed microbiome functions. However, studies of individual microbial isolates/species without exploring their impact on the host or the complex microbiome structures and functions will not be considered for publication. Microbiome is indexed in BIOSIS, Current Contents, DOAJ, Embase, MEDLINE, PubMed, PubMed Central, and Science Citations Index Expanded.
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