A Family of Viral Satellites Manipulates Invading Virus Gene Expression and Can Affect Cholera Toxin Mobilization.
A Family of Viral Satellites Manipulates Invading Virus Gene Expression and Can Affect Cholera Toxin Mobilization.
复制标题
一个家族的病毒囊泡操纵入侵病毒基因表达并可影响霍乱毒素动员。
DOI：
10.1128/msystems.00358-20
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发表时间：
2020-10-13
期刊：
影响因子：
6.4
通讯作者：
Seed KD
中科院分区：
文献类型：
--
作者：
Barth ZK;Netter Z;Angermeyer A;Bhardwaj P;Seed KD
病毒卫星存在于生命的各个领域，可以对它们寄生的病毒和它们所居住的细胞产生深远的适应性影响。在这项研究中，我们获得了植物外病毒卫星的第一个RNA测序(RNA-seq)转录本，以及霍乱弧菌的主要捕食者噬菌体ICP1的转录组。以前在一个不相关的噬菌体卫星中观察到的衣壳下调在噬菌体诱导的染色体岛状元件(PLE)中是保守的，这表明病毒卫星处于强大的选择压力下，以减少其较大宿主病毒的衣壳表达。尽管对衣壳蛋白的表达进行了保守的操作，但PLE对CTXΦ的转录和迁移率表现出不同的影响。我们的结果表明，PLE可以影响宿主对噬菌体的抵抗力和毒力编码元件的迁移性，这表明PLE在塑造霍乱弧菌进化过程中发挥了重要作用。许多病毒具有时间展开的基因表达模式，旨在颠覆宿主防御，侵占宿主新陈代谢，最终产生大量的子代病毒粒子。高通量组学工具，如RNA测序(RNA-seq)，极大地提高了感染期间表达模式的分辨率。研究较少的是病毒卫星，即寄生病毒的移动基因组。通过对感染时间进程进行RNA-SEQ，我们首次获得了裂解感染期间噬菌体卫星的时间分辨转录本。具体地说，我们已经获得了霍乱弧菌噬菌体ICP1和ICP1‘S寄生虫的所有五个已知变体的转录本，这些变体是噬菌体诱导的染色体岛状元件(PLE)。PLE依赖ICP1进行DNA复制和动员，并取消感染细胞中ICP1后代的产生。我们研究了PLES对ICP1基因表达的影响，发现PLES并不广泛地限制或降低ICP1基因的表达。一个主要的例外发生在ICP1‘S衣壳形态发生操纵子中，该操纵子被每个ple变异体下调。令人惊讶的是，PLE还被发现改变了ctxΦ的基因表达，ctx DNA是编码霍乱毒素的整合噬菌体，是产毒霍乱弧菌毒力所必需的。一个PLE，ple1，上调了参与复制和整合的CTxΦ基因，并在诱导Φ应答后提高了CTx DNA的迁移率。重要的是，病毒卫星存在于生命的各个领域，可以对它们寄生的病毒和它们所居住的细胞产生深远的适应性影响。在这项研究中，我们获得了植物外病毒卫星的第一个RNA测序(RNA-seq)转录本，以及霍乱弧菌的主要捕食者噬菌体ICP1的转录组。以前在一个不相关的噬菌体卫星中观察到的衣壳下调在噬菌体诱导的染色体岛状元件(PLE)中是保守的，这表明病毒卫星处于强大的选择压力下，以减少其较大宿主病毒的衣壳表达。尽管对衣壳蛋白的表达进行了保守的操作，但PLE对CTXΦ的转录和迁移率表现出不同的影响。我们的结果表明，PLE可以影响宿主对噬菌体的抵抗力和毒力编码元件的迁移性，这表明PLE在塑造霍乱弧菌进化过程中发挥了重要作用。
Viral satellites are found in all domains of life and can have profound fitness effects on both the viruses they parasitize and the cells they reside in. In this study, we have acquired the first RNA sequencing (RNA-seq) transcriptomes of viral satellites outside plants, as well as the transcriptome of the phage ICP1, a predominant predator of pandemic Vibrio cholerae. Capsid downregulation, previously observed in an unrelated phage satellite, is conserved among phage inducible chromosomal island-like elements (PLEs), suggesting that viral satellites are under strong selective pressure to reduce the capsid expression of their larger host viruses. Despite conserved manipulation of capsid expression, PLEs exhibit divergent effects on CTXΦ transcription and mobility. Our results demonstrate that PLEs can influence both their hosts’ resistance to phage and the mobility of virulence-encoding elements, suggesting that PLEs can play a substantial role in shaping Vibrio cholerae evolution. Many viruses possess temporally unfolding gene expression patterns aimed at subverting host defenses, commandeering host metabolism, and ultimately producing a large number of progeny virions. High-throughput omics tools, such as RNA sequencing (RNA-seq), have dramatically enhanced the resolution of expression patterns during infection. Less studied have been viral satellites, mobile genomes that parasitize viruses. By performing RNA-seq on infection time courses, we have obtained the first time-resolved transcriptomes for bacteriophage satellites during lytic infection. Specifically, we have acquired transcriptomes for the lytic Vibrio cholerae phage ICP1 and all five known variants of ICP1’s parasite, the phage inducible chromosomal island-like elements (PLEs). PLEs rely on ICP1 for both DNA replication and mobilization and abolish production of ICP1 progeny in infected cells. We investigated PLEs’ impact on ICP1 gene expression and found that PLEs did not broadly restrict or reduce ICP1 gene expression. A major exception occurred in ICP1’s capsid morphogenesis operon, which was downregulated by each of the PLE variants. Surprisingly, PLEs were also found to alter the gene expression of CTXΦ, the integrative phage that encodes cholera toxin and is necessary for virulence of toxigenic V. cholerae. One PLE, PLE1, upregulated CTXΦ genes involved in replication and integration and boosted CTXΦ mobility following induction of the SOS response. IMPORTANCE Viral satellites are found in all domains of life and can have profound fitness effects on both the viruses they parasitize and the cells they reside in. In this study, we have acquired the first RNA sequencing (RNA-seq) transcriptomes of viral satellites outside plants, as well as the transcriptome of the phage ICP1, a predominant predator of pandemic Vibrio cholerae. Capsid downregulation, previously observed in an unrelated phage satellite, is conserved among phage inducible chromosomal island-like elements (PLEs), suggesting that viral satellites are under strong selective pressure to reduce the capsid expression of their larger host viruses. Despite conserved manipulation of capsid expression, PLEs exhibit divergent effects on CTXΦ transcription and mobility. Our results demonstrate that PLEs can influence both their hosts’ resistance to phage and the mobility of virulence-encoding elements, suggesting that PLEs can play a substantial role in shaping Vibrio cholerae evolution.