A Linear Plasmid-Like Prophage of Actinomyces odontolyticus Promotes Biofilm Assembly

A Linear Plasmid-Like Prophage of Actinomyces odontolyticus Promotes Biofilm Assembly
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溶齿放线菌的线性质粒样原噬菌体促进生物膜组装

DOI:
10.1128/aem.01263-18
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发表时间:
2018-09-01
影响因子:
4.4
通讯作者:
He, Xuesong
He, Xuesong
中科院分区:
生物学2区
文献类型:
--
作者:
Shen, Mengyu;Yang, Yuhui;He, Xuesong

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作为人类口腔微生物组成员的噬菌体的生物学尚未得到充分研究。在这里,我们报告了 xhp1 的表征,xhp1 是一种从人类口腔分离物溶齿放线菌亚种中鉴定出的新型线性质粒样前噬菌体。放线杆菌菌株XH001。 xhp1 可以被诱导并重新感染 xhp1 治愈的 XH001。 xhp1 的自发诱导导致细菌宿主亚群的裂解和促进生物膜组装的 eDNA 的释放,从而可能有助于溶牙放线菌在口腔内的持久存在。摘要 人体口腔是大量细菌和噬菌体(噬菌体)的家园。然而,口腔噬菌体作为人类微生物组成员的生物学尚不清楚。最近,我们分离出溶齿放线菌亚种。来自人类口腔的放线菌菌株 XH001,基因组分析显示存在名为 xhp1 的完整原噬菌体。在这里,我们证明了xhp1是一种线性质粒样前噬菌体,它是新鉴定的溶牙放线菌噬菌体。原噬菌体 xhp1 基因组是 35 kb 线性双链 DNA,具有 10 bp 单链 3' 粘性末端。 xhp1存在于染色体外,估计拷贝数为5。xhp1的注释显示有54个开放阅读框,而系统发育分析表明它与其他噬菌体的相似性有限。根据透射电镜检查,xhp1噬菌体颗粒可以被丝裂霉素C诱导,属于Siphoviridae家族。释放的 xhp1 颗粒可以重新感染 xhp1 治愈的 XH001 菌株,并导致微小的模糊斑块。此外,xhp1 通过自发诱导和宿主细胞外 DNA (eDNA) 的释放来促进 XH001 生物膜的形成。总之,我们鉴定了溶齿放线菌的线性质粒样前噬菌体,它可以增强细菌宿主生物膜的组装,并且可能有利于宿主在口腔中的持久存在。重要性 噬菌体作为人类口腔微生物组成员的生物学尚未得到充分研究。在这里,我们报告了 xhp1 的表征,xhp1 是一种从人类口腔分离物溶齿放线菌亚种中鉴定出的新型线性质粒样前噬菌体。放线杆菌菌株XH001。 xhp1 可以被诱导并重新感染 xhp1 治愈的 XH001。 xhp1 的自发诱导导致细菌宿主亚群的裂解和促进生物膜组装的 eDNA 的释放,从而可能有助于溶牙放线菌在口腔内的持久存在。
The biology of phages as members of the human oral microbiome is understudied. Here, we report the characterization of xhp1, a novel linear plasmid-like prophage identified from a human oral isolate, Actinomyces odontolyticus subsp. actinosynbacter strain XH001. xhp1 can be induced and reinfect xhp1-cured XH001. The spontaneous induction of xhp1 leads to the lysis of a subpopulation of bacterial hosts and the release of eDNA that promotes biofilm assembly, thus potentially contributing to the persistence of A. odontolyticus within the oral cavity. ABSTRACT The human oral cavity is home to a large number of bacteria and bacteriophages (phages). However, the biology of oral phages as members of the human microbiome is not well understood. Recently, we isolated Actinomyces odontolyticus subsp. actinosynbacter strain XH001 from the human oral cavity, and genomic analysis revealed the presence of an intact prophage named xhp1. Here, we demonstrated that xhp1 is a linear plasmid-like prophage, which is a newly identified phage of A. odontolyticus. The prophage xhp1 genome is a 35-kb linear double-stranded DNA with 10-bp single-stranded, 3’ cohesive ends. xhp1 exists extrachromosomally, with an estimated copy number of 5. Annotation of xhp1 revealed 54 open reading frames, while phylogenetic analysis suggests that it has limited similarity with other phages. xhp1 phage particles can be induced by mitomycin C and belong to the Siphoviridae family, according to transmission electron microscopic examination. The released xhp1 particles can reinfect the xhp1-cured XH001 strain and result in tiny blurry plaques. Moreover, xhp1 promotes XH001 biofilm formation through spontaneous induction and the release of host extracellular DNA (eDNA). In conclusion, we identified a linear plasmid-like prophage of A. odontolyticus, which enhances bacterial host biofilm assembly and could be beneficial to the host for its persistence in the oral cavity. IMPORTANCE The biology of phages as members of the human oral microbiome is understudied. Here, we report the characterization of xhp1, a novel linear plasmid-like prophage identified from a human oral isolate, Actinomyces odontolyticus subsp. actinosynbacter strain XH001. xhp1 can be induced and reinfect xhp1-cured XH001. The spontaneous induction of xhp1 leads to the lysis of a subpopulation of bacterial hosts and the release of eDNA that promotes biofilm assembly, thus potentially contributing to the persistence of A. odontolyticus within the oral cavity.