The Global Reciprocal Reprogramming between Mycobacteriophage SWU1 and Mycobacterium Reveals the Molecular Strategy of Subversion and Promotion of Phage Infection

Fan, Xiangyu; Duan, Xiangke; Tong, Yan; Huang, Qinqin; Zhou, Mingliang; Wang, Huan; Zeng, Lanying; Young, Ry; Xie, Jianping

doi:10.3389/fmicb.2016.00041

Cited by 9 publications

(13 citation statements)

References 64 publications

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“…Based on the replication cycle of JD032 ( Fig. 4), four time points (30,45,75, and 135 min) that span the entire replication cycle of the phage were selected for exploring the transcriptomic profiles of both JD032 and host C. difficile strain TW11 by RNA-seq, with the phageuninfected host cells at 0 min as a control. Each experiment was repeated three times.…”

Section: Resultsmentioning

confidence: 99%

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Isolation and Characterization of the Novel Phage JD032 and Global Transcriptomic Response during JD032 Infection of Clostridioides difficile Ribotype 078

Zhang

Dong

et al. 2020

mSystems

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Insights into the interaction between phages and their bacterial hosts are crucial for the development of phage therapy. However, only one study has investigated global gene expression of Clostridioides (formerly Clostridium) difficile carrying prophage, and transcriptional reprogramming during lytic infection has not been studied. Here, we presented the isolation, propagation, and characterization of a newly discovered 35,109-bp phage, JD032, and investigated the global transcriptomes of both JD032 and C. difficile ribotype 078 (RT078) strain TW11 during JD032 infection. Transcriptome sequencing (RNA-seq) revealed the progressive replacement of bacterial host mRNA with phage transcripts. The expressed genes of JD032 were clustered into early, middle, and late temporal categories that were functionally similar. Specifically, a gene (JD032_orf016) involved in the lysis-lysogeny decision was identified as an early expression gene. Only 17.7% (668/3,781) of the host genes were differentially expressed, and more genes were downregulated than upregulated. The expression of genes involved in host macromolecular synthesis (DNA/RNA/proteins) was altered by JD032 at the level of transcription. In particular, the expression of the ropA operon was downregulated. Most noteworthy is that the gene expression of some antiphage systems, including CRISPR-Cas, restriction-modification, and toxin-antitoxin systems, was suppressed by JD032 during infection. In addition, bacterial sporulation, adhesion, and virulence factor genes were significantly downregulated. This study provides the first description of the interaction between anaerobic spore-forming bacteria and phages during lytic infection and highlights new aspects of C. difficile phage-host interactions. IMPORTANCE C. difficile is one of the most clinically significant intestinal pathogens. Although phages have been shown to effectively control C. difficile infection, the host responses to phage predation have not been fully studied. In this study, we reported the isolation and characterization of a new phage, JD032, and analyzed the global transcriptomic changes in the hypervirulent RT078 C. difficile strain, TW11, during phage JD032 infection. We found that bacterial host mRNA was progressively replaced with phage transcripts, three temporal categories of JD032 gene expression, the extensive interplay between phage-bacterium, antiphage-like responses of the host and phage evasion, and decreased expression of sporulation- and virulence-related genes of the host after phage infection. These findings confirmed the complexity of interactions between C. difficile and phages and suggest that phages undergoing a lytic cycle may also cause different phenotypes in hosts, similar to prophages, which may inspire phage therapy for the control of C. difficile.

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Section: Resultsmentioning

confidence: 99%

“…(B) Graphs displayed below the subclasses show expression profiles of the individual genes in that subclass as a function of time after infection. (30) and NCTC 12673 (22), respectively, but similar to P. aeruginosa after infection with the lysogenic phage PaP3 (31).…”

Section: Figmentioning

confidence: 99%

Isolation and Characterization of the Novel Phage JD032 and Global Transcriptomic Response during JD032 Infection of Clostridioides difficile Ribotype 078

Zhang

Dong

et al. 2020

mSystems

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“…This inactivation would be accompanied by the adsorption of the phage to the superficial phage-specific receptors on the surface of mycobacteria [ 34 , 35 , 36 , 37 ]. L1 [ 38 , 39 ] and L5 [ 40 , 41 , 42 ] are mycobacteriophages that can induce the formation of superinfection-stable lysogens [ 38 , 39 ] and, meanwhile, have toxicity against M. smegmatis . Both mycobacteriophages could infect fast- and slow-growing mycobacterial species with the difference that the calcium concentration is critical in L5 infectivity [ 43 , 44 ].…”

Section: An Explanation Of Discovered Mycobacteriophages Infective To...mentioning

confidence: 99%

A Review on Mycobacteriophages: From Classification to Applications

Hosseiniporgham

Sechi

2022

Pathogens

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Mycobacterial infections are a group of life-threatening conditions triggered by fast- or slow-growing mycobacteria. Some mycobacteria, such as Mycobacterium tuberculosis, promote the deaths of millions of lives throughout the world annually. The control of mycobacterial infections is influenced by the challenges faced in the diagnosis of these bacteria and the capability of these pathogens to develop resistance against common antibiotics. Detection of mycobacterial infections is always demanding due to the intracellular nature of these pathogens that, along with the lipid-enriched structure of the cell wall, complicates the access to the internal contents of mycobacterial cells. Moreover, recent studies depicted that more than 20% of M. tuberculosis (Mtb) infections are multi-drug resistant (MDR), and only 50% of positive MDR-Mtb cases are responsive to standard treatments. Similarly, the susceptibility of nontuberculosis mycobacteria (NTM) to first-line tuberculosis antibiotics has also declined in recent years. Exploiting mycobacteriophages as viruses that infect mycobacteria has significantly accelerated the diagnosis and treatment of mycobacterial infections. This is because mycobacteriophages, regardless of their cycle type (temperate/lytic), can tackle barriers in the mycobacterial cell wall and make the infected bacteria replicate phage DNA along with their DNA. Although the infectivity of the majority of discovered mycobacteriophages has been evaluated in non-pathogenic M. smegmatis, more research is still ongoing to find mycobacteriophages specific to pathogenic mycobacteria, such as phage DS6A, which has been shown to be able to infect members of the M. tuberculosis complex. Accordingly, this review aimed to introduce some potential mycobacteriophages in the research, specifically those that are infective to the three troublesome mycobacteria, M. tuberculosis, M. avium subsp. paratuberculosis (MAP), and M. abscessus, highlighting their theranostic applications in medicine.

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“…Lytic gene expression has been described for several Cluster A phages including L5, D29, StarStuff, Kampy, and SWU1 (54, 60, 61), for Giles (Cluster Q) (59), and Fruitloop (Cluster F) (62), and several Cluster N phages (63). In general, there appears to be two major types of transcription that occur, in early and late periods.…”

Section: Mycobacteriophage Genome Organization and Expressionmentioning

confidence: 99%

“…Curiously, in the Cluster A phages that have been transcriptionally characterized (L5, D29, StarStuff, RedRock, Kampe, SWU1), a non-coding region near the right genome end is transcribed extremely high very early in lytic growth (54, 58, 60, 61). There may be several small transcripts made, but their functions are not known.…”

Section: Mycobacteriophage Genome Organization and Expressionmentioning

confidence: 99%

Mycobacteriophages

Hatfull

2018

Microbiol Spectr

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Mycobacteriophages are viruses that infect mycobacterial hosts. A large number of mycobacteriophages have been isolated and genomically characterized, providing insights into viral diversity and evolution, as well as fueling development of tools for mycobacterial genetics. Mycobacteriophages have intimate relationships with their hosts, and provide insights into the genetics and physiology of the mycobacteria, and tools for potential clinical applications such as drug development, diagnosis, vaccines, and potentially therapy.

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The Global Reciprocal Reprogramming between Mycobacteriophage SWU1 and Mycobacterium Reveals the Molecular Strategy of Subversion and Promotion of Phage Infection

Cited by 9 publications

References 64 publications

Isolation and Characterization of the Novel Phage JD032 and Global Transcriptomic Response during JD032 Infection of Clostridioides difficile Ribotype 078

Isolation and Characterization of the Novel Phage JD032 and Global Transcriptomic Response during JD032 Infection of Clostridioides difficile Ribotype 078

A Review on Mycobacteriophages: From Classification to Applications

Mycobacteriophages

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