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Chapter 12 : Widespread Antisense Transcription in Prokaryotes

Authors: Jens Georg1, Wolfgang R. Hess2
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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
Content Type: Monograph
Publication Year: 2019

Category: Microbial Genetics and Molecular Biology

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Abstract:

The first documented -encoded antisense RNAs (asRNAs) in bacteria were the RNA I, controlling ColE1 replication ( ), and the OOP asRNA of bacteriophage λ ( ). However, until the year 2007 a mere ∼10 bacterial asRNAs had been characterized ( ). It was only with the advent of global approaches for the analysis of bacterial transcriptomes that it was recognized that actually a substantial fraction of transcripts, in fact, constitute asRNAs. The first hints obtained with high-density microarrays pointed at antisense transcription linked to possibly as many as 3,000 to 4,000 open reading frames in ( ), more recently reinforced by the finding that asRNAs originate from 37% of all transcription start sites (TSSs) ( ), which might still be an underestimation of the initial level of antisense transcription ( ). By the hybridization of directly labeled RNA instead of cDNA to high-density microarrays, a high number of strongly expressed asRNAs were experimentally identified in the model cyanobacterium sp. PCC 6803 ( ). The direct labeling of RNA avoided the artificial second-strand synthesis in the production of cDNA, a step at which experimental artifacts might be introduced ( ). In agreement with the initial evidence, numerous transcriptome studies have demonstrated more recently that a substantial fraction of the discovered TSS in vastly different bacterial taxa is not associated with a protein-coding gene. Internal parts of coding regions in sense and antisense orientation are massively transcribed, a phenomenon often referred to as pervasive transcription ( ).

Citation: Georg J, Hess W. 2019. Widespread Antisense Transcription in Prokaryotes, p 191-210. In Storz G, Papenfort K (ed), Regulating with RNA in Bacteria and Archaea. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.RWR-0029-2018
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Widespread Antisense Transcription in Prokaryotes
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Citation: Georg J, Hess W. 2019. Widespread Antisense Transcription in Prokaryotes, p 191-210. In Storz G, Papenfort K (ed), Regulating with RNA in Bacteria and Archaea. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.RWR-0029-2018
/content/10.1128/9781683670247.chap12.fig12-1
Figure 1
Overview of the main categories of bacterial asRNAs, mechanisms of action, and selected examples.
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Figure 1

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

Citation: Georg J, Hess W. 2019. Widespread Antisense Transcription in Prokaryotes, p 191-210. In Storz G, Papenfort K (ed), Regulating with RNA in Bacteria and Archaea. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.RWR-0029-2018
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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 ( ). 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 ( ). 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 ( ). The scheme has been redrawn according to primary transcriptome information from 6803 ( ).
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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 ( ). 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 ( ). 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 ( ). The scheme has been redrawn according to primary transcriptome information from 6803 ( ).

Citation: Georg J, Hess W. 2019. Widespread Antisense Transcription in Prokaryotes, p 191-210. In Storz G, Papenfort K (ed), Regulating with RNA in Bacteria and Archaea. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.RWR-0029-2018
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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 ( ). (B) PsbAR2 and PsbAR3, two asRNAs in 6803, start 19 nt upstream from the respective start codons ( ). 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 ( ), which was recently confirmed in an independent study ( ). The ribosome binding site (RBS) was defined previously ( ). As a consequence, PsbAR2 and PsbAR3 stabilize the mRNA, together with the bound ribosomes ( ).
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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 ( ). (B) PsbAR2 and PsbAR3, two asRNAs in 6803, start 19 nt upstream from the respective start codons ( ). 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 ( ), which was recently confirmed in an independent study ( ). The ribosome binding site (RBS) was defined previously ( ). As a consequence, PsbAR2 and PsbAR3 stabilize the mRNA, together with the bound ribosomes ( ).

Citation: Georg J, Hess W. 2019. Widespread Antisense Transcription in Prokaryotes, p 191-210. In Storz G, Papenfort K (ed), Regulating with RNA in Bacteria and Archaea. ASM Press, Washington, DC. 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 ( ). This asRNA contributes to the reduction in the number of ribosomes during ethanol stress by repressing , encoding the ribosomal protein S4 ( ). (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 ( ) and the transcriptome analysis during prolonged nitrogen starvation ( ). Note the location of this asRNA linking one of the ribosomal RNA operons with , encoding the vegetative sigma factor.
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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 ( ). This asRNA contributes to the reduction in the number of ribosomes during ethanol stress by repressing , encoding the ribosomal protein S4 ( ). (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 ( ) and the transcriptome analysis during prolonged nitrogen starvation ( ). Note the location of this asRNA linking one of the ribosomal RNA operons with , encoding the vegetative sigma factor.

Citation: Georg J, Hess W. 2019. Widespread Antisense Transcription in Prokaryotes, p 191-210. In Storz G, Papenfort K (ed), Regulating with RNA in Bacteria and Archaea. ASM Press, Washington, DC. 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.
10.1128/9781683670247/fig12-5_thmb.gif
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Image of Figure 5
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.

Citation: Georg J, Hess W. 2019. Widespread Antisense Transcription in Prokaryotes, p 191-210. In Storz G, Papenfort K (ed), Regulating with RNA in Bacteria and Archaea. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.RWR-0029-2018
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Tables

Widespread Antisense Transcription in Prokaryotes
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Citation: Georg J, Hess W. 2019. Widespread Antisense Transcription in Prokaryotes, p 191-210. In Storz G, Papenfort K (ed), Regulating with RNA in Bacteria and Archaea. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.RWR-0029-2018
/content/10.1128/9781683670247.chap12.tab12-1
Table 1
Overview of selected transcriptome analyses performed in different bacteria and the reported share in asRNAs
Generic image for table
Table 1

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

Citation: Georg J, Hess W. 2019. Widespread Antisense Transcription in Prokaryotes, p 191-210. In Storz G, Papenfort K (ed), Regulating with RNA in Bacteria and Archaea. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.RWR-0029-2018
/content/10.1128/9781683670247.chap12.tab12-2
Table 2
Names and characteristic features of functionally characterized asRNAs discussed in the text
Generic image for table
Table 2

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

Citation: Georg J, Hess W. 2019. Widespread Antisense Transcription in Prokaryotes, p 191-210. In Storz G, Papenfort K (ed), Regulating with RNA in Bacteria and Archaea. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.RWR-0029-2018

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