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Widespread Antisense Transcription in Prokaryotes

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  • Authors: Jens Georg1, Wolfgang R. Hess2
  • Editors: Gisela Storz3, Kai Papenfort4
  • VIEW AFFILIATIONS HIDE AFFILIATIONS
    Affiliations: 1: University of Freiburg, Faculty of Biology, Institute of Biology III, Genetics and Experimental Bioinformatics, D-79104 Freiburg, Germany; 2: University of Freiburg, Faculty of Biology, Institute of Biology III, Genetics and Experimental Bioinformatics, D-79104 Freiburg, Germany; 3: Division of Molecular and Cellular Biology, Eunice Kennedy Shriver National Institute of Child Health and Human Development, Bethesda, MD; 4: Department of Biology I, Microbiology, LMU Munich, Martinsried, Germany
  • Source: microbiolspec July 2018 vol. 6 no. 4 doi:10.1128/microbiolspec.RWR-0029-2018
  • Received 05 March 2018 Accepted 24 April 2018 Published 13 July 2018
  • Wolfgang R. Hess, wolfgang.hess@biologie.uni-freiburg.de
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  • Abstract:

    Although bacterial genomes are usually densely protein-coding, genome-wide mapping approaches of transcriptional start sites revealed that a significant fraction of the identified promoters drive the transcription of noncoding RNAs. These can be -acting RNAs, mainly originating from intergenic regions and, in many studied examples, possessing regulatory functions. However, a significant fraction of these noncoding RNAs consist of natural antisense transcripts (asRNAs), which overlap other transcriptional units. Naturally occurring asRNAs were first observed to play a role in bacterial plasmid replication and in bacteriophage λ more than 30 years ago. Today’s view is that asRNAs abound in all three domains of life. There are several examples of asRNAs in bacteria with clearly defined functions. Nevertheless, many asRNAs appear to result from pervasive initiation of transcription, and some data point toward global functions of such widespread transcriptional activity, explaining why the search for a specific regulatory role is sometimes futile. In this review, we give an overview about the occurrence of antisense transcription in bacteria, highlight particular examples of functionally characterized asRNAs, and discuss recent evidence pointing at global relevance in RNA processing and transcription-coupled DNA repair.

  • Citation: Georg J, Hess W. 2018. Widespread Antisense Transcription in Prokaryotes. Microbiol Spectrum 6(4):RWR-0029-2018. doi:10.1128/microbiolspec.RWR-0029-2018.

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/content/journal/microbiolspec/10.1128/microbiolspec.RWR-0029-2018
2018-07-13
2018-07-18

Abstract:

Although bacterial genomes are usually densely protein-coding, genome-wide mapping approaches of transcriptional start sites revealed that a significant fraction of the identified promoters drive the transcription of noncoding RNAs. These can be -acting RNAs, mainly originating from intergenic regions and, in many studied examples, possessing regulatory functions. However, a significant fraction of these noncoding RNAs consist of natural antisense transcripts (asRNAs), which overlap other transcriptional units. Naturally occurring asRNAs were first observed to play a role in bacterial plasmid replication and in bacteriophage λ more than 30 years ago. Today’s view is that asRNAs abound in all three domains of life. There are several examples of asRNAs in bacteria with clearly defined functions. Nevertheless, many asRNAs appear to result from pervasive initiation of transcription, and some data point toward global functions of such widespread transcriptional activity, explaining why the search for a specific regulatory role is sometimes futile. In this review, we give an overview about the occurrence of antisense transcription in bacteria, highlight particular examples of functionally characterized asRNAs, and discuss recent evidence pointing at global relevance in RNA processing and transcription-coupled DNA repair.

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Figures

Image of FIGURE 1
FIGURE 1

Overview of the main categories of bacterial asRNAs, mechanisms of action, and selected examples.

Source: microbiolspec July 2018 vol. 6 no. 4 doi:10.1128/microbiolspec.RWR-0029-2018
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Image of FIGURE 2
FIGURE 2

Excludons, instances of long overlapping mRNAs that inhibit the expression of one set of genes by the expression of a second overlapping set of genes. (A) Excludon in formed by the overlap between the motility operon transcript and the transcript, with its long 5′ UTR originating from the distal σ-dependent promoter ( 32 ). MogR is a repressor of flagellum and motility gene transcription. Therefore, the arrangement of these two transcriptional units in an excludon ensures the exclusive expression of only one of both coding regions, which is of direct relevance for the motile or nonmotile lifestyle. Note that there is also a proximal σ-independent promoter. (B) Arrangement of the VapBC10-type toxin-antitoxin system genes and in 6803 in an excludon with the to genes encoding urease accessory protein UreD, nitrilase (), and glutamate decarboxylase ( 34 ). The genes to are transcribed in the form of a long mRNA that is transcribed from TSSs upstream from . The resulting transcriptional unit overlaps and just between the final and the penultimate genes. This arrangement contributes to silence expression of this toxin-antitoxin system under most conditions in addition to the autoregulatory transcriptional and the proteolytic regulation ( 33 ). The scheme has been redrawn according to primary transcriptome information from 6803 ( 106 ).

Source: microbiolspec July 2018 vol. 6 no. 4 doi:10.1128/microbiolspec.RWR-0029-2018
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Image of FIGURE 3
FIGURE 3

Distance does matter. The divergent effects of two asRNAs (colored red) initiated within the 5′ UTR of a gene (black) are compared. (A) MtlS, an asRNA in , starts 5 nt upstream from the start codon in inverse orientation and is repressive ( 68 ). (B) PsbAR2 and PsbAR3, two asRNAs in 6803, start 19 nt upstream from the respective start codons ( 66 ). The target genes, and , are in the shown region identical to each other. The 5′ UTR of the and mRNAs is a substrate for the RNase E endoribonuclease. The cleavage occurs in an AU-rich element, preferably at the sites indicated by the dashed arrows ( 65 ), which was recently confirmed in an independent study ( 107 ). The ribosome binding site (RBS) was defined previously ( 65 ). As a consequence, PsbAR2 and PsbAR3 stabilize the mRNA, together with the bound ribosomes ( 66 ).

Source: microbiolspec July 2018 vol. 6 no. 4 doi:10.1128/microbiolspec.RWR-0029-2018
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FIGURE 4

Stress-induced asRNAs functioning in global transcriptome remodeling. (A) Ethanol addition triggers the SigB-dependent transcription of the S1136-S1134 asRNA in ( 96 ). This asRNA contributes to the reduction in the number of ribosomes during ethanol stress by repressing , encoding the ribosomal protein S4 ( 96 ). (B) Expression of asRNAs overlapping the gene in 6803, which become strongly induced upon long-term nitrogen depletion. The figure has been redrawn according to information about the 6803 primary transcriptome ( 106 ) and the transcriptome analysis during prolonged nitrogen starvation ( 97 ). Note the location of this asRNA linking one of the ribosomal RNA operons with , encoding the vegetative sigma factor.

Source: microbiolspec July 2018 vol. 6 no. 4 doi:10.1128/microbiolspec.RWR-0029-2018
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FIGURE 5

Scenario of the evolutionary processes in bacteria leading from pervasive transcription to global functions of asRNAs and to highly specific roles and mechanisms. (A) Global mechanisms. TSSs (arrows) originate relatively easily due to the simplicity of bacterial promoters. They give rise to various transcript types, including mRNAs (black) and asRNAs (red). These transcripts are not automatically functional. The TSSs with detrimental effects will rapidly be selected out by evolution or the pervasive transcription is counteracted by diverse safety mechanisms involving e.g., Rho, NusG and RNAse H (cross). However, in many instances transcription is beneficial. Thus, global functions of antisense transcription can be exerted at the DNA level as well as the RNA level. Examples at the DNA level include transcription-coupled repair; at the RNA level, asRNAs contribute to transcriptome remodeling and possibly mRNA decay after translation. (B) Specific roles. The rich pool of existing asRNAs is a resource from which some become associated with a specific role (only selected examples are shown). These specific roles may interfere with the transcription of specific genes, here exemplified by the RnaG asRNA, which upon base-pairing to the mRNA inhibits the formation of an antiterminator, leading to termination of transcription. Multiple examples exist for the involvement of asRNAs in hampering the translation of specific mRNAs, in codegradation by recruiting RNase III, or in providing protection from cleavage by masking RNase E cleavage sites.

Source: microbiolspec July 2018 vol. 6 no. 4 doi:10.1128/microbiolspec.RWR-0029-2018
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Tables

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TABLE 1

Overview of selected transcriptome analyses performed in different bacteria and the reported share in asRNAs

Source: microbiolspec July 2018 vol. 6 no. 4 doi:10.1128/microbiolspec.RWR-0029-2018
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TABLE 2

Names and characteristic features of functionally characterized asRNAs discussed in the text

Source: microbiolspec July 2018 vol. 6 no. 4 doi:10.1128/microbiolspec.RWR-0029-2018

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