Staphylococcus epidermidis Phages Transduce Antimicrobial Resistance Plasmids and Mobilize Chromosomal Islands.
Staphylococcus epidermidis Phages Transduce Antimicrobial Resistance Plasmids and Mobilize Chromosomal Islands.
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DOI：
10.1128/msphere.00223-21
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发表时间：
2021-05-12
期刊：
影响因子：
4.8
通讯作者：
Doškař J
中科院分区：
文献类型：
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作者：
Fišarová L;Botka T;Du X;Mašlaňová I;Bárdy P;Pantůček R;Benešík M;Roudnický P;Winstel V;Larsen J;Rosenstein R;Peschel A;Doškař J
表皮葡萄球菌的多重耐药菌株作为凝固酶阴性葡萄球菌中最重要的病原体出现在医院和牲畜环境中。噬菌体转导的研究对于了解毒力和抗菌素耐药性基因如何在最初的共生细菌群体中传播至关重要。表皮葡萄球菌是一种导致医院感染的主要机会性病原体，以其形成生物膜的能力和高抗生素耐药性而著称。它是多种抗菌素耐药基因的储存库，通过水平基因转移（例如转导）在葡萄球菌群体中传播。虽然噬菌体介导的转导在金黄色葡萄球菌中得到了充分研究，但表皮葡萄球菌转导噬菌体尚未得到详细描述。在这里，我们报告了先前用于表皮葡萄球菌噬菌体分型的四种噬菌体 27、48、456 和 459 以及来自临床表皮葡萄球菌菌株的新分离的噬菌体 E72 的特征。这些噬菌体属于 Siphoviridae 科和 Phietavirus 属，具有表皮葡萄球菌特异性宿主范围，它们总共感染了 35 种测试菌株中的 49%。全基因组比较揭示了转导金黄色葡萄球菌 phietaviruses 的进化相关性。据此，所有测试的噬菌体都能够在来自不同克隆复合体的表皮葡萄球菌菌株之间进行高达 10−4 的高频转导。编码链霉素、四环素和氯霉素抗性的大小为4至19kb的质粒被转移。我们在此提供了表皮葡萄球菌中噬菌体诱导的染色体岛转移的第一个证据。与金黄色葡萄球菌致病岛类似，转移伴随着噬菌体衣壳重塑；然而，该岛编码的干扰蛋白是不同的。我们的研究结果强调了表皮葡萄球菌温带噬菌体通过水平基因转移在表皮葡萄球菌菌株进化中的作用，这也可用于表皮葡萄球菌遗传学研究。重要性 表皮葡萄球菌的多重耐药菌株作为凝固酶阴性葡萄球菌中最重要的病原体出现在医院和牲畜环境中。噬菌体转导的研究对于了解毒力和抗菌素耐药性基因如何在最初的共生细菌群体中传播至关重要。在这项工作中，我们提供了转导表皮葡萄球菌噬菌体的详细描述。抗菌素耐药性质粒的高转导频率和染色体岛转移的第一个证据强调了表皮葡萄球菌噬菌体在获得宿主菌株更高致病潜力方面的决定性作用。迄今为止，这种重要性仅归因于金黄色葡萄球菌噬菌体，而不是凝固酶阴性葡萄球菌的噬菌体。这项研究还证明，所描述的转导噬菌体代表了表皮葡萄球菌菌株中有价值的基因修饰工具，而其他基因转移方法则失败了。
Multidrug-resistant strains of S. epidermidis emerge in both nosocomial and livestock environments as the most important pathogens among coagulase-negative staphylococcal species. The study of transduction by phages is essential to understanding how virulence and antimicrobial resistance genes spread in originally commensal bacterial populations. Staphylococcus epidermidis is a leading opportunistic pathogen causing nosocomial infections that is notable for its ability to form a biofilm and for its high rates of antibiotic resistance. It serves as a reservoir of multiple antimicrobial resistance genes that spread among the staphylococcal population by horizontal gene transfer such as transduction. While phage-mediated transduction is well studied in Staphylococcus aureus, S. epidermidis transducing phages have not been described in detail yet. Here, we report the characteristics of four phages, 27, 48, 456, and 459, previously used for S. epidermidis phage typing, and the newly isolated phage E72, from a clinical S. epidermidis strain. The phages, classified in the family Siphoviridae and genus Phietavirus, exhibited an S. epidermidis-specific host range, and together they infected 49% of the 35 strains tested. A whole-genome comparison revealed evolutionary relatedness to transducing S. aureus phietaviruses. In accordance with this, all the tested phages were capable of transduction with high frequencies up to 10−4 among S. epidermidis strains from different clonal complexes. Plasmids with sizes from 4 to 19 kb encoding resistance to streptomycin, tetracycline, and chloramphenicol were transferred. We provide here the first evidence of a phage-inducible chromosomal island transfer in S. epidermidis. Similarly to S. aureus pathogenicity islands, the transfer was accompanied by phage capsid remodeling; however, the interfering protein encoded by the island was distinct. Our findings underline the role of S. epidermidis temperate phages in the evolution of S. epidermidis strains by horizontal gene transfer, which can also be utilized for S. epidermidis genetic studies. IMPORTANCE Multidrug-resistant strains of S. epidermidis emerge in both nosocomial and livestock environments as the most important pathogens among coagulase-negative staphylococcal species. The study of transduction by phages is essential to understanding how virulence and antimicrobial resistance genes spread in originally commensal bacterial populations. In this work, we provide a detailed description of transducing S. epidermidis phages. The high transduction frequencies of antimicrobial resistance plasmids and the first evidence of chromosomal island transfer emphasize the decisive role of S. epidermidis phages in attaining a higher pathogenic potential of host strains. To date, such importance has been attributed only to S. aureus phages, not to those of coagulase-negative staphylococci. This study also proved that the described transducing bacteriophages represent valuable genetic modification tools in S. epidermidis strains where other methods for gene transfer fail.