Large Noncoding RNAs in Bacteria

Harris, Kimberly A.; Breaker, Ronald R.

doi:10.1128/microbiolspec.rwr-0005-2017

Cited by 43 publications

(32 citation statements)

References 61 publications

(108 reference statements)

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“…5). The length of this transcript (ϳ800 bp based on the RNA-seq coverage), is comparable to that of the giant-, ornate-, lake-, and Lactobacillales-derived (GOLLD) and the rumenoriginating, ornate, large (ROOL) RNAs that have been found in many phage genomes (51). These RNAs are frequently harbored near tRNAs, although this is not the case for ICP1, since it does not possess any tRNAs.…”

Section: Resultsmentioning

confidence: 85%

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A Family of Viral Satellites Manipulates Invading Virus Gene Expression and Can Affect Cholera Toxin Mobilization

et al. 2020

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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.

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Section: Resultsmentioning

confidence: 85%

“…The role of these large ncRNAs is unknown. In one Lactobacillus brevis prophage, a GOLLD RNA was found to accumulate during lytic infection but was dispensable for phage production (51).…”

Section: Resultsmentioning

confidence: 99%

A Family of Viral Satellites Manipulates Invading Virus Gene Expression and Can Affect Cholera Toxin Mobilization

et al. 2020

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“…The most abundantly expressed ICP1 transcript is encoded in an approximately 1kb orf-less space between gp139, the start of ICP1's lysis cluster [25], and gp140 (Fig 4). The length of this transcript (~800bp based on the RNA-seq coverage), is comparable to the Giant-Ornate-Lake-and Lactobacialles-Derived (GOLLD) and the Rumen-Originating, Ornate, Large (ROOL) RNAs that have been found in many phage genomes [47]. These RNAs are frequently encoded near tRNAs, although this is not the case for ICP1 since it does not possess any tRNAs.…”

Section: Non-coding Rnas Are Abundant In Icp1 and Plesmentioning

confidence: 90%

“…The role of these large ncRNAs is unknown. In one Lactobacillus brevis prophage, a GOLLD RNA was found to accumulate during lytic infection, but was dispensable for phage production [47].…”

Section: Non-coding Rnas Are Abundant In Icp1 and Plesmentioning

confidence: 99%

A family of viral satellites manipulates invading virus gene expression and affects cholera toxin mobilization

Barth

Netter

Angermeyer

et al. 2020

Preprint

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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-seq, have dramatically enhanced resolution of expression patterns during infection. Less studied have been viral satellites, mobile genomes that parasitize viruses and have far reaching effects on host-cell fitness. 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. This transcriptional manipulation, conserved among PLEs, has also evolved independently in at least one other phage satellite, suggesting that viral satellites may be under strong selective pressure to reduce the capsid expression of their larger host viruses. 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. Our data show that PLEs exhibit conserved manipulation of their host-phage's gene expression, but divergent effects on CTXφ, revealing that PLEs can influence both their hosts' resistance to phage and the mobility of virulence encoding elements.So far, few insights have been gained into the gene expression programs of ICP1 and PLEs. PLE1 expresses its integrase in uninfected cells [22], expression of PLE1's replication initiator, RepA, is induced following infection of ICP1 [23], and the PLE's lysis modulator, LidI, is detectable by Western blot late during ICP1 infection [25]. The PLE integrase's recombination directionality factor (necessary for directing integrase excision activity) is PexA, an ICP1 protein whose native function is unknown, but whose expression can be detected by 5 minutes post infection [22]. While these limited observations have provided insight into key PLE and ICP1 genes, the gross expression patterns of ICP1 and PLEs remain unknown. Until now, we have not known the degree to which ICP1 alters cellular expression patterns, and whether PLEs alter ICP1's gene expression or reproduce and restrict ICP1 without such alterations. To address these questions, we performed RNA-seq on V. cholerae infected by ICP1 over the course of the infection cycle. We sequenced the transc...

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“…ncRNAs consist of RNA species with a variety of functions, including gene regulation (e.g., small RNA (sRNA), microRNA (miRNA), long non-coding RNA (lncRNA)), enzyme-like activities (ribozymes, e.g., ribosomal RNA (rRNA)), and transfer of amino acids to the ribosome (transfer RNA). Their size ranges from miRNAs (21–25 bp) to long rRNA strands (thousands of bp), and they act both intra- and extracellularly [42,43,44]. The mapping of these RNAs generates valuable spatio-temporal information regarding RNA dynamics and function, and the physiological state of a cell [45].…”

Section: Novel Biomarker Discovery With Transcriptomic Technologiesmentioning

confidence: 99%

Application of Transcriptomics to Enhance Early Diagnostics of Mycobacterial Infections, with an Emphasis on Mycobacterium avium ssp. paratuberculosis

Esker

Koets

2019

Veterinary Sciences

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Mycobacteria cause a wide variety of disease in human and animals. Species that infect ruminants include M. bovis and M. avium ssp. paratuberculosis (MAP). MAP is the causative agent of Johne’s disease in ruminants, which is a chronic granulomatous enteric infection that leads to severe economic losses worldwide. Characteristic of MAP infection is the long, latent phase in which intermittent shedding can take place, while diagnostic tests are unable to reliably detect an infection in this stage. This leads to unnoticed dissemination within herds and the presence of many undetected, silent carriers, which makes the eradication of Johne’s disease difficult. To improve the control of MAP infection, research is aimed at improving early diagnosis. Transcriptomic approaches can be applied to characterize host-pathogen interactions during infection, and to develop novel biomarkers using transcriptional profiles. Studies have focused on the identification of specific RNAs that are expressed in different infection stages, which will assist in the development and clinical implementation of early diagnostic tests.

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Large Noncoding RNAs in Bacteria

Cited by 43 publications

References 61 publications

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

A family of viral satellites manipulates invading virus gene expression and affects cholera toxin mobilization

Application of Transcriptomics to Enhance Early Diagnostics of Mycobacterial Infections, with an Emphasis on Mycobacterium avium ssp. paratuberculosis

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