Chapter 12 : Widespread Antisense Transcription in Prokaryotes

MyBook is a cheap paperback edition of the original book and will be sold at uniform, low price.

Preview this chapter:
Zoom in

Widespread Antisense Transcription in Prokaryotes, Page 1 of 2

| /docserver/preview/fulltext/10.1128/9781683670247/9781683670230_Chap12-1.gif /docserver/preview/fulltext/10.1128/9781683670247/9781683670230_Chap12-2.gif


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
Highlighted Text: Show | Hide
Loading full text...

Full text loading...


Image of Figure 1
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
Permissions and Reprints Request Permissions
Download as Powerpoint
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 ( ). 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
Permissions and Reprints Request Permissions
Download as Powerpoint
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 ( ). (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
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of Figure 4
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
Permissions and Reprints Request Permissions
Download as Powerpoint
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
Permissions and Reprints Request Permissions
Download as Powerpoint


1. Itoh T,, Tomizawa J . 1980. Formation of an RNA primer for initiation of replication of ColE1 DNA by ribonuclease H. Proc Natl Acad Sci U S A 77 : 2450 2454.[CrossRef][PubMed]
2. Krinke L,, Mahoney M,, Wulff DL . 1991. The role of the OOP antisense RNA in coliphage λ development. Mol Microbiol 5 : 1265 1272.[CrossRef][PubMed]
3. Krinke L,, Wulff DL . 1990. RNase III-dependent hydrolysis of λ cII- O gene mRNA mediated by λ OOP antisense RNA. Genes Dev 4 : 2223 2233.[CrossRef][PubMed]
4. Krinke L,, Wulff DL . 1987. OOP RNA, produced from multicopy plasmids, inhibits λ cII gene expression through an RNase III-dependent mechanism. Genes Dev 1 : 1005 1013.[CrossRef][PubMed]
5. Brantl S . 2007. Regulatory mechanisms employed by cis-encoded antisense RNAs. Curr Opin Microbiol 10 : 102 109.[CrossRef][PubMed]
6. Selinger DW,, Cheung KJ,, Mei R,, Johansson EM,, Richmond CS,, Blattner FR,, Lockhart DJ,, Church GM . 2000. RNA expression analysis using a 30 base pair resolution Escherichia coli genome array. Nat Biotechnol 18 : 1262 1268.[CrossRef][PubMed]
7. Thomason MK,, Bischler T,, Eisenbart SK,, Förstner KU,, Zhang A,, Herbig A,, Nieselt K,, Sharma CM,, Storz G . 2015. Global transcriptional start site mapping using differential RNA sequencing reveals novel antisense RNAs in Escherichia coli. J Bacteriol 197 : 18 28.[CrossRef][PubMed]
8. Raghunathan N,, Kapshikar RM,, Leela JK,, Mallikarjun J,, Bouloc P,, Gowrishankar J . 2018. Genome-wide relationship between R-loop formation and antisense transcription in Escherichia coli. Nucleic Acids Res 46 : 3400 3411.[CrossRef][PubMed]
9. Georg J,, Voss B,, Scholz I,, Mitschke J,, Wilde A,, Hess WR . 2009. Evidence for a major role of antisense RNAs in cyanobacterial gene regulation. Mol Syst Biol 5 : 305.[CrossRef][PubMed]
10. Perocchi F,, Xu Z,, Clauder-Münster S,, Steinmetz LM . 2007. Antisense artifacts in transcriptome microarray experiments are resolved by actinomycin D. Nucleic Acids Res 35 : e128.[CrossRef][PubMed]
11. Wade JT,, Grainger DC . 2014. Pervasive transcription: illuminating the dark matter of bacterial transcriptomes. Nat Rev Microbiol 12 : 647 653.[CrossRef][PubMed]
12. Raghavan R,, Sloan DB,, Ochman H . 2012. Antisense transcription is pervasive but rarely conserved in enteric bacteria. mBio 3 : e00156–e12.[CrossRef][PubMed]
13. Wagner EG,, Romby P . 2015. Small RNAs in bacteria and archaea: who they are, what they do, and how they do it. Adv Genet 90 : 133 208.[CrossRef][PubMed]
14. Storz G,, Wolf YI,, Ramamurthi KS . 2014. Small proteins can no longer be ignored. Annu Rev Biochem 83 : 753 777.[CrossRef][PubMed]
15. Meydan S,, Vázquez-Laslop N,, Mankin AS . 2018. Genes within genes in bacterial genomes. Microbiol Spectr 6 : RWR-0020-2018.[CrossRef]
16. Lloréns-Rico V,, Cano J,, Kamminga T,, Gil R,, Latorre A,, Chen WH,, Bork P,, Glass JI,, Serrano L,, Lluch-Senar M . 2016. Bacterial antisense RNAs are mainly the product of transcriptional noise. Sci Adv 2 : e1501363.[CrossRef][PubMed]
17. Adebali O,, Chiou YY,, Hu J,, Sancar A,, Selby CP . 2017. Genome-wide transcription-coupled repair in Escherichia coli is mediated by the Mfd translocase. Proc Natl Acad Sci U S A 114 : E2116 E2125.[CrossRef][PubMed]
18. Brophy JA,, Voigt CA . 2016. Antisense transcription as a tool to tune gene expression. Mol Syst Biol 12 : 854.[CrossRef][PubMed]
19. Bordoy AE,, Varanasi US,, Courtney CM,, Chatterjee A . 2016. Transcriptional interference in convergent promoters as a means for tunable gene expression. ACS Synth Biol 5 : 1331 1341.[CrossRef][PubMed]
20. Hao N,, Palmer AC,, Ahlgren-Berg A,, Shearwin KE,, Dodd IB . 2016. The role of repressor kinetics in relief of transcriptional interference between convergent promoters. Nucleic Acids Res 44 : 6625 6638.[CrossRef][PubMed]
21. Bordoy AE,, Chatterjee A . 2015. cis-antisense transcription gives rise to tunable genetic switch behavior: a mathematical modeling approach. PLoS One 10 : e0133873.[CrossRef][PubMed]
22. Sneppen K,, Dodd IB,, Shearwin KE,, Palmer AC,, Schubert RA,, Callen BP,, Egan JB . 2005. A mathematical model for transcriptional interference by RNA polymerase traffic in Escherichia coli. J Mol Biol 346 : 399 409.[CrossRef][PubMed]
23. Gowrishankar J,, Leela JK,, Anupama K . 2013. R-loops in bacterial transcription: their causes and consequences. Transcription 4 : 153 157.[CrossRef][PubMed]
24. Cahoon LA,, Seifert HS . 2013. Transcription of a cis-acting, noncoding, small RNA is required for pilin antigenic variation in Neisseria gonorrhoeae. PLoS Pathog 9 : e1003074.[CrossRef][PubMed]
25. Kawano M,, Aravind L,, Storz G . 2007. An antisense RNA controls synthesis of an SOS-induced toxin evolved from an antitoxin. Mol Microbiol 64 : 738 754.[CrossRef][PubMed]
26. Opdyke JA,, Kang JG,, Storz G . 2004. GadY, a small-RNA regulator of acid response genes in Escherichia coli. J Bacteriol 186 : 6698 6705.[CrossRef][PubMed]
27. Dühring U,, Axmann IM,, Hess WR,, Wilde A . 2006. An internal antisense RNA regulates expression of the photosynthesis gene isiA. Proc Natl Acad Sci U S A 103 : 7054 7058.[CrossRef][PubMed]
28. Toledo-Arana A,, Dussurget O,, Nikitas G,, Sesto N,, Guet-Revillet H,, Balestrino D,, Loh E,, Gripenland J,, Tiensuu T,, Vaitkevicius K,, Barthelemy M,, Vergassola M,, Nahori MA,, Soubigou G,, Régnault B,, Coppée JY,, Lecuit M,, Johansson J,, Cossart P . 2009. The Listeria transcriptional landscape from saprophytism to virulence. Nature 459 : 950 956.[CrossRef][PubMed]
29. Stazic D,, Lindell D,, Steglich C . 2011. Antisense RNA protects mRNA from RNase E degradation by RNA-RNA duplex formation during phage infection. Nucleic Acids Res 39 : 4890 4899.[CrossRef][PubMed]
30. Stazic D,, Pekarski I,, Kopf M,, Lindell D,, Steglich C . 2016. A novel strategy for exploitation of host RNase E activity by a marine cyanophage. Genetics 203 : 1149 1159.[CrossRef][PubMed]
31. Wurtzel O,, Sesto N,, Mellin JR,, Karunker I,, Edelheit S,, Bécavin C,, Archambaud C,, Cossart P,, Sorek R . 2012. Comparative transcriptomics of pathogenic and non-pathogenic Listeria species. Mol Syst Biol 8 : 583.[CrossRef][PubMed]
32. Sesto N,, Wurtzel O,, Archambaud C,, Sorek R,, Cossart P . 2013. The excludon: a new concept in bacterial antisense RNA-mediated gene regulation. Nat Rev Microbiol 11 : 75 82.[CrossRef][PubMed]
33. Ning D,, Liu S,, Xu W,, Zhuang Q,, Wen C,, Tang X . 2013. Transcriptional and proteolytic regulation of the toxin-antitoxin locus vapBC10 ( ssr2962/slr1767) on the chromosome of Synechocystis sp. PCC 6803. PLoS One 8 : e80716.[CrossRef][PubMed]
34. Kopfmann S,, Roesch SK,, Hess WR . 2016. Type II toxin-antitoxin systems in the unicellular cyanobacterium Synechocystis sp. PCC 6803. Toxins (Basel) 8 : E228.[CrossRef][PubMed]
35. Masachis Gelo S,, Darfeuille F . 2018. Type I toxin-antitoxin systems: regulating toxin expression via Shine-Dalgarno sequestration and small RNA binding. Microbiol Spectr 6 : RWR-0030-2018.[CrossRef]
36. Silby MW,, Levy SB . 2008. Overlapping protein-encoding genes in Pseudomonas fluorescens Pf0-1. PLoS Genet 4 : e1000094.[CrossRef][PubMed]
37. Haycocks JRJ,, Grainger DC . 2016. Unusually situated binding sites for bacterial transcription factors can have hidden functionality. PLoS One 11 : e0157016.[CrossRef][PubMed]
38. Voigt K,, Sharma CM,, Mitschke J,, Lambrecht SJ,, Voß B,, Hess WR,, Steglich C . 2014. Comparative transcriptomics of two environmentally relevant cyanobacteria reveals unexpected transcriptome diversity. ISME J 8 : 2056 2068.[CrossRef][PubMed]
39. Schlüter JP,, Reinkensmeier J,, Daschkey S,, Evguenieva-Hackenberg E,, Janssen S,, Jänicke S,, Becker JD,, Giegerich R,, Becker A . 2010. A genome-wide survey of sRNAs in the symbiotic nitrogen-fixing alpha-proteobacterium Sinorhizobium meliloti. BMC Genomics 11 : 245.[CrossRef][PubMed]
40. Cohen O,, Doron S,, Wurtzel O,, Dar D,, Edelheit S,, Karunker I,, Mick E,, Sorek R . 2016. Comparative transcriptomics across the prokaryotic tree of life. Nucleic Acids Res 44 : W46 W53.[CrossRef][PubMed]
41. Lybecker M,, Zimmermann B,, Bilusic I,, Tukhtubaeva N,, Schroeder R . 2014. The double-stranded transcriptome of Escherichia coli. Proc Natl Acad Sci U S A 111 : 3134 3139.[CrossRef][PubMed]
42. Gatewood ML,, Bralley P,, Weil MR,, Jones GH . 2012. RNA-Seq and RNA immunoprecipitation analyses of the transcriptome of Streptomyces coelicolor identify substrates for RNase III. J Bacteriol 194 : 2228 2237.[CrossRef][PubMed]
43. Šetinová D,, Šmídová K,, Pohl P,, Musić I,, Bobek J . 2018. RNase III-binding-mRNAs revealed novel complementary transcripts in Streptomyces. Front Microbiol 8 : 2693.[CrossRef][PubMed]
44. Lioliou E,, Sharma CM,, Caldelari I,, Helfer A-C,, Fechter P,, Vandenesch F,, Vogel J,, Romby P . 2012. Global regulatory functions of the Staphylococcus aureus endoribonuclease III in gene expression. PLoS Genet 8 : e1002782.[CrossRef][PubMed]
45. Durand S,, Gilet L,, Condon C . 2012. The essential function of B. subtilis RNase III is to silence foreign toxin genes. PLoS Genet 8 : e1003181.[CrossRef][PubMed]
46. Fozo EM,, Hemm MR,, Storz G . 2008. Small toxic proteins and the antisense RNAs that repress them. Microbiol Mol Biol Rev 72 : 579 589.[CrossRef][PubMed]
47. Kawano M . 2012. Divergently overlapping cis-encoded antisense RNA regulating toxin-antitoxin systems from E. coli: hok/sok, ldr/rdl, symE/symR. RNA Biol 9 : 1520 1527.[CrossRef][PubMed]
48. Coray DS,, Wheeler NE,, Heinemann JA,, Gardner PP . 2017. Why so narrow: distribution of anti-sense regulated, type I toxin-antitoxin systems compared with type II and type III systems. RNA Biol 14 : 275 280.[CrossRef][PubMed]
49. Georg J,, Hess WR . 2011. cis-antisense RNA, another level of gene regulation in bacteria. Microbiol Mol Biol Rev 75 : 286 300.[CrossRef][PubMed]
50. Vogel J,, Luisi BF . 2011. Hfq and its constellation of RNA. Nat Rev Microbiol 9 : 578 589.[CrossRef][PubMed]
51. Heidrich N,, Bauriedl S,, Barquist L,, Li L,, Schoen C,, Vogel J . 2017. The primary transcriptome of Neisseria meningitidis and its interaction with the RNA chaperone Hfq. Nucleic Acids Res 45 : 6147 6167.[CrossRef][PubMed]
52. Chao Y,, Papenfort K,, Reinhardt R,, Sharma CM,, Vogel J . 2012. An atlas of Hfq-bound transcripts reveals 3′ UTRs as a genomic reservoir of regulatory small RNAs. EMBO J 31 : 4005 4019.[CrossRef][PubMed]
53. Sittka A,, Lucchini S,, Papenfort K,, Sharma CM,, Rolle K,, Binnewies TT,, Hinton JC,, Vogel J . 2008. Deep sequencing analysis of small noncoding RNA and mRNA targets of the global post-transcriptional regulator, Hfq. PLoS Genet 4 : e1000163.[CrossRef][PubMed]
54. Melamed S,, Peer A,, Faigenbaum-Romm R,, Gatt YE,, Reiss N,, Bar A,, Altuvia Y,, Argaman L,, Margalit H . 2016. Global mapping of small RNA-target interactions in bacteria. Mol Cell 63 : 884 897.[CrossRef][PubMed]
55. Bilusic I,, Popitsch N,, Rescheneder P,, Schroeder R,, Lybecker M . 2014. Revisiting the coding potential of the E. coli genome through Hfq co-immunoprecipitation. RNA Biol 11 : 641 654.[CrossRef][PubMed]
56. Rasmussen AA,, Eriksen M,, Gilany K,, Udesen C,, Franch T,, Petersen C,, Valentin-Hansen P . 2005. Regulation of ompA mRNA stability: the role of a small regulatory RNA in growth phase-dependent control. Mol Microbiol 58 : 1421 1429.[CrossRef][PubMed]
57. Udekwu KI,, Darfeuille F,, Vogel J,, Reimegård J,, Holmqvist E,, Wagner EG . 2005. Hfq-dependent regulation of OmpA synthesis is mediated by an antisense RNA. Genes Dev 19 : 2355 2366.[CrossRef][PubMed]
58. Udekwu KI . 2010. Transcriptional and post-transcriptional regulation of the Escherichia coli luxS mRNA; involvement of the sRNA MicA. PLoS One 5 : e13449.[CrossRef][PubMed]
59. Aiso T,, Kamiya S,, Yonezawa H,, Gamou S . 2014. Overexpression of an antisense RNA, ArrS, increases the acid resistance of Escherichia coli. Microbiology 160 : 954 961.[CrossRef][PubMed]
60. Takada A,, Umitsuki G,, Nagai K,, Wachi M . 2007. RNase E is required for induction of the glutamate-dependent acid resistance system in Escherichia coli. Biosci Biotechnol Biochem 71 : 158 164.[CrossRef][PubMed]
61. Tramonti A,, De Canio M,, De Biase D . 2008. GadX/GadW-dependent regulation of the Escherichia coli acid fitness island: transcriptional control at the gadY-gadW divergent promoters and identification of four novel 42 bp GadX/GadW-specific binding sites. Mol Microbiol 70 : 965 982.[PubMed]
62. Sayed N,, Jousselin A,, Felden B . 2011. A cis-antisense RNA acts in trans in Staphylococcus aureus to control translation of a human cytolytic peptide. Nat Struct Mol Biol 19 : 105 112.[CrossRef][PubMed]
63. Eisenhut M,, Georg J,, Klähn S,, Sakurai I,, Mustila H,, Zhang P,, Hess WR,, Aro EM . 2012. The antisense RNA As1_flv4 in the cyanobacterium Synechocystis sp. PCC 6803 prevents premature expression of the flv4-2 operon upon shift in inorganic carbon supply. J Biol Chem 287 : 33153 33162.[CrossRef][PubMed]
64. Shimakawa G,, Shaku K,, Nishi A,, Hayashi R,, Yamamoto H,, Sakamoto K,, Makino A,, Miyake C . 2015. FLAVODIIRON2 and FLAVODIIRON4 proteins mediate an oxygen-dependent alternative electron flow in Synechocystis sp. PCC 6803 under CO 2-limited conditions. Plant Physiol 167 : 472 480.[CrossRef][PubMed]
65. Horie Y,, Ito Y,, Ono M,, Moriwaki N,, Kato H,, Hamakubo Y,, Amano T,, Wachi M,, Shirai M,, Asayama M . 2007. Dark-induced mRNA instability involves RNase E/G-type endoribonuclease cleavage at the AU-box and SD sequences in cyanobacteria. Mol Genet Genomics 278 : 331 346.[CrossRef][PubMed]
66. Sakurai I,, Stazic D,, Eisenhut M,, Vuorio E,, Steglich C,, Hess WR,, Aro EM . 2012. Positive regulation of psbA gene expression by cis-encoded antisense RNAs in Synechocystis sp. PCC 6803. Plant Physiol 160 : 1000 1010.[CrossRef][PubMed]
67. Hu J,, Li T,, Xu W,, Zhan J,, Chen H,, He C,, Wang Q . 2017. Small antisense RNA RblR positively regulates RuBisCo in Synechocystis sp. PCC 6803. Front Microbiol 8 : 231.[CrossRef][PubMed]
68. Mustachio LM,, Aksit S,, Mistry RH,, Scheffler R,, Yamada A,, Liu JM . 2012. The Vibrio cholerae mannitol transporter is regulated posttranscriptionally by the MtlS small regulatory RNA. J Bacteriol 194 : 598 606.[CrossRef][PubMed]
69. Chang H,, Replogle JM,, Vather N,, Tsao-Wu M,, Mistry R,, Liu JM . 2015. A cis-regulatory antisense RNA represses translation in Vibrio cholerae through extensive complementarity and proximity to the target locus. RNA Biol 12 : 136 148.[CrossRef][PubMed]
70. Chen Q,, Crosa JH . 1996. Antisense RNA, Fur, iron, and the regulation of iron transport genes in Vibrio anguillarum. J Biol Chem 271 : 18885 18891.[CrossRef][PubMed]
71. Waldbeser LS,, Chen Q,, Crosa JH . 1995. Antisense RNA regulation of the fatB iron transport protein gene in Vibrio anguillarum. Mol Microbiol 17 : 747 756.[CrossRef][PubMed]
72. Stork M,, Di Lorenzo M,, Welch TJ,, Crosa JH . 2007. Transcription termination within the iron transport-biosynthesis operon of Vibrio anguillarum requires an antisense RNA. J Bacteriol 189 : 3479 3488.[CrossRef][PubMed]
73. Giangrossi M,, Prosseda G,, Tran CN,, Brandi A,, Colonna B,, Falconi M . 2010. A novel antisense RNA regulates at transcriptional level the virulence gene icsA of Shigella flexneri. Nucleic Acids Res 38 : 3362 3375.[CrossRef][PubMed]
74. Giangrossi M,, Giuliodori AM,, Tran CN,, Amici A,, Marchini C,, Falconi M . 2017. VirF relieves the transcriptional attenuation of the virulence gene icsA of Shigella flexneri affecting the icsA mRNA-RnaG complex formation. Front Microbiol 8 : 650.[CrossRef][PubMed]
75. Shao W,, Price MN,, Deutschbauer AM,, Romine MF,, Arkin AP . 2014. Conservation of transcription start sites within genes across a bacterial genus. mBio 5 : e01398–e14.[CrossRef][PubMed]
76. Kopf M,, Klähn S,, Scholz I,, Hess WR,, Voß B . 2015. Variations in the non-coding transcriptome as a driver of inter-strain divergence and physiological adaptation in bacteria. Sci Rep 5 : 9560.[CrossRef][PubMed]
77. Lasa I,, Villanueva M . 2014. Overlapping transcription and bacterial RNA removal. Proc Natl Acad Sci U S A 111 : 2868 2869.[CrossRef][PubMed]
78. Lasa I,, Toledo-Arana A,, Dobin A,, Villanueva M,, de los Mozos IR,, Vergara-Irigaray M,, Segura V,, Fagegaltier D,, Penadés JR,, Valle J,, Solano C,, Gingeras TR . 2011. Genome-wide antisense transcription drives mRNA processing in bacteria. Proc Natl Acad Sci U S A 108 : 20172 20177.[CrossRef][PubMed]
79. Lasa I,, Toledo-Arana A,, Gingeras TR . 2012. An effort to make sense of antisense transcription in bacteria. RNA Biol 9 : 1039 1044.[CrossRef][PubMed]
80. Lybecker M,, Bilusic I,, Raghavan R . 2014. Pervasive transcription: detecting functional RNAs in bacteria. Transcription 5 : e944039.[CrossRef][PubMed]
81. Steglich C,, Lindell D,, Futschik M,, Rector T,, Steen R,, Chisholm SW . 2010. Short RNA half-lives in the slow-growing marine cyanobacterium Prochlorococcus. Genome Biol 11 : R54.[CrossRef][PubMed]
82. Bidnenko V,, Nicolas P,, Grylak-Mielnicka A,, Delumeau O,, Auger S,, Aucouturier A,, Guerin C,, Repoila F,, Bardowski J,, Aymerich S,, Bidnenko E . 2017. Termination factor Rho: from the control of pervasive transcription to cell fate determination in Bacillus subtilis. PLoS Genet 13 : e1006909.[CrossRef][PubMed]
83. Peters JM,, Mooney RA,, Grass JA,, Jessen ED,, Tran F,, Landick R . 2012. Rho and NusG suppress pervasive antisense transcription in Escherichia coli. Genes Dev 26 : 2621 2633.[CrossRef][PubMed]
84. Sedlyarova N,, Rescheneder P,, Magán A,, Popitsch N,, Rziha N,, Bilusic I,, Epshtein V,, Zimmermann B,, Lybecker M,, Sedlyarov V,, Schroeder R,, Nudler E . 2017. Natural RNA polymerase aptamers regulate transcription in E. coli. Mol Cell 67 : 30 43.e6.[CrossRef][PubMed]
85. Duquette ML,, Handa P,, Vincent JA,, Taylor AF,, Maizels N . 2004. Intracellular transcription of G-rich DNAs induces formation of G-loops, novel structures containing G4 DNA. Genes Dev 18 : 1618 1629.[CrossRef][PubMed]
86. Leela JK,, Syeda AH,, Anupama K,, Gowrishankar J . 2013. Rho-dependent transcription termination is essential to prevent excessive genome-wide R-loops in Escherichia coli. Proc Natl Acad Sci U S A 110 : 258 263.[CrossRef][PubMed]
87. Boque-Sastre R,, Soler M,, Oliveira-Mateos C,, Portela A,, Moutinho C,, Sayols S,, Villanueva A,, Esteller M,, Guil S . 2015. Head-to-head antisense transcription and R-loop formation promotes transcriptional activation. Proc Natl Acad Sci U S A 112 : 5785 5790.[CrossRef][PubMed]
88. Aguilera A,, Gaillard H . 2014. Transcription and recombination: when RNA meets DNA. Cold Spring Harb Perspect Biol 6 : a016543.[CrossRef][PubMed]
89. Tan FY,, Wörmann ME,, Loh E,, Tang CM,, Exley RM . 2015. Characterization of a novel antisense RNA in the major pilin locus of Neisseria meningitidis influencing antigenic variation. J Bacteriol 197 : 1757 1768.[CrossRef][PubMed]
90. Chatterjee A,, Johnson CM,, Shu CC,, Kaznessis YN,, Ramkrishna D,, Dunny GM,, Hu WS . 2011. Convergent transcription confers a bistable switch in Enterococcus faecalis conjugation. Proc Natl Acad Sci U S A 108 : 9721 9726.[CrossRef][PubMed]
91. Chatterjee A,, Drews L,, Mehra S,, Takano E,, Kaznessis YN,, Hu WS . 2011. Convergent transcription in the butyrolactone regulon in Streptomyces coelicolor confers a bistable genetic switch for antibiotic biosynthesis. PLoS One 6 : e21974.[CrossRef][PubMed]
92. André G,, Even S,, Putzer H,, Burguière P,, Croux C,, Danchin A,, Martin-Verstraete I,, Soutourina O . 2008. S-box and T-box riboswitches and antisense RNA control a sulfur metabolic operon of Clostridium acetobutylicum. Nucleic Acids Res 36 : 5955 5969.[CrossRef][PubMed]
93. Palmer AC,, Ahlgren-Berg A,, Egan JB,, Dodd IB,, Shearwin KE . 2009. Potent transcriptional interference by pausing of RNA polymerases over a downstream promoter. Mol Cell 34 : 545 555.[CrossRef][PubMed]
94. Callen BP,, Shearwin KE,, Egan JB . 2004. Transcriptional interference between convergent promoters caused by elongation over the promoter. Mol Cell 14 : 647 656.[CrossRef][PubMed]
95. Nicolas P,, Mäder U,, Dervyn E,, Rochat T,, Leduc A,, Pigeonneau N,, Bidnenko E,, Marchadier E,, Hoebeke M,, Aymerich S,, Becher D,, Bisicchia P,, Botella E,, Delumeau O,, Doherty G,, Denham EL,, Fogg MJ,, Fromion V,, Goelzer A,, Hansen A,, Härtig E,, Harwood CR,, Homuth G,, Jarmer H,, Jules M,, Klipp E,, Le Chat L,, Lecointe F,, Lewis P,, Liebermeister W,, March A,, Mars RA,, Nannapaneni P,, Noone D,, Pohl S,, Rinn B,, Rügheimer F,, Sappa PK,, Samson F,, Schaffer M,, Schwikowski B,, Steil L,, Stülke J,, Wiegert T,, Devine KM,, Wilkinson AJ,, van Dijl JM,, Hecker M,, Völker U,, Bessières P,, Noirot P . 2012. Condition-dependent transcriptome reveals high-level regulatory architecture in Bacillus subtilis. Science 335 : 1103 1106.[CrossRef][PubMed]
96. Mars RA,, Mendonça K,, Denham EL,, van Dijl JM . 2015. The reduction in small ribosomal subunit abundance in ethanol-stressed cells of Bacillus subtilis is mediated by a SigB-dependent antisense RNA. Biochim Biophys Acta 1853 : 2553 2559.[CrossRef][PubMed]
97. Klotz A,, Georg J,, Bučinská L,, Watanabe S,, Reimann V,, Januszewski W,, Sobotka R,, Jendrossek D,, Hess WR,, Forchhammer K . 2016. Awakening of a dormant cyanobacterium from nitrogen chlorosis reveals a genetically determined program. Curr Biol 26 : 2862 2872.[CrossRef][PubMed]
98. Heilmann B,, Hakkila K,, Georg J,, Tyystjärvi T,, Hess WR,, Axmann IM,, Dienst D . 2017. 6S RNA plays a role in recovery from nitrogen depletion in Synechocystis sp. PCC 6803. BMC Microbiol 17 : 229.[CrossRef][PubMed]
99. Bidnenko E,, Bidnenko V . 2017. Transcription termination factor Rho and microbial phenotypic heterogeneity. Curr Genet 64 : 541 546.[PubMed]
100. Selby CP,, Sancar A . 1993. Molecular mechanism of transcription-repair coupling. Science 260 : 53 58.[CrossRef]
101. Fan J,, Leroux-Coyau M,, Savery NJ,, Strick TR . 2016. Reconstruction of bacterial transcription-coupled repair at single-molecule resolution. Nature 536 : 234 237.[CrossRef][PubMed]
102. Legewie S,, Dienst D,, Wilde A,, Herzel H,, Axmann IM . 2008. Small RNAs establish delays and temporal thresholds in gene expression. Biophys J 95 : 3232 3238.[CrossRef][PubMed]
103. Mitschke J,, Vioque A,, Haas F,, Hess WR,, Muro-Pastor AM . 2011. Dynamics of transcriptional start site selection during nitrogen stress-induced cell differentiation in Anabaena sp. PCC7120. Proc Natl Acad Sci U S A 108 : 20130 20135.[CrossRef][PubMed]
104. Voss B,, Bolhuis H,, Fewer DP,, Kopf M,, Möke F,, Haas F,, El-Shehawy R,, Hayes P,, Bergman B,, Sivonen K,, Dittmann E,, Scanlan DJ,, Hagemann M,, Stal LJ,, Hess WR . 2013. Insights into the physiology and ecology of the brackish-water-adapted cyanobacterium Nodularia spumigena CCY9414 based on a genome-transcriptome analysis. PLoS One 8 : e60224.[CrossRef][PubMed]
105. Dutcher HA,, Raghavan R . 2018. Origin, evolution, and loss of bacterial small RNAs. Microbiol Spectr 6 : RWR-0004-2017.[CrossRef][PubMed]
106. Kopf M,, Klähn S,, Scholz I,, Matthiessen JK,, Hess WR,, Voß B . 2014. Comparative analysis of the primary transcriptome of Synechocystis sp. PCC 6803. DNA Res 21 : 527 539.[CrossRef][PubMed]
107. Behler J,, Sharma K,, Reimann V,, Wilde A,, Urlaub H,, Hess WR . 2018. The host-encoded RNase E endonuclease as the crRNA maturation enzyme in a CRISPR-Cas subtype III-Bv system. Nat Microbiol 3 : 367 377.[CrossRef][PubMed]
108. Schlüter JP,, Reinkensmeier J,, Barnett MJ,, Lang C,, Krol E,, Giegerich R,, Long SR,, Becker A . 2013. Global mapping of transcription start sites and promoter motifs in the symbiotic α-proteobacterium Sinorhizobium meliloti 1021. BMC Genomics 14 : 156.[CrossRef][PubMed]
109. Hou S,, López-Pérez M,, Pfreundt U,, Belkin N,, Stüber K,, Huettel B,, Reinhardt R,, Berman-Frank I,, Rodriguez-Valera F,, Hess WR . 2018. Benefit from decline: the primary transcriptome of Alteromonas macleodii str. Te101 during Trichodesmium demise. ISME J 12 : 981 996.
110. Kröger C,, Dillon SC,, Cameron AD,, Papenfort K,, Sivasankaran SK,, Hokamp K,, Chao Y,, Sittka A,, Hébrard M,, Händler K,, Colgan A,, Leekitcharoenphon P,, Langridge GC,, Lohan AJ,, Loftus B,, Lucchini S,, Ussery DW,, Dorman CJ,, Thomson NR,, Vogel J,, Hinton JC . 2012. The transcriptional landscape and small RNAs of Salmonella enterica serovar Typhimurium. Proc Natl Acad Sci U S A 109 : E1277 E1286.[CrossRef][PubMed]
111. Papenfort K,, Förstner KU,, Cong JP,, Sharma CM,, Bassler BL . 2015. Differential RNA-seq of Vibrio cholerae identifies the VqmR small RNA as a regulator of biofilm formation. Proc Natl Acad Sci U S A 112 : E766 E775.[CrossRef][PubMed]
112. Alkhateeb RS,, Vorhölter FJ,, Rückert C,, Mentz A,, Wibberg D,, Hublik G,, Niehaus K,, Pühler A . 2016. Genome wide transcription start sites analysis of Xanthomonas campestris pv. campestris B100 with insights into the gum gene cluster directing the biosynthesis of the exopolysaccharide xanthan. J Biotechnol 225 : 18 28.[CrossRef][PubMed]
113. Qiu Y,, Cho BK,, Park YS,, Lovley D,, Palsson ,, Zengler K . 2010. Structural and operational complexity of the Geobacter sulfurreducens genome. Genome Res 20 : 1304 1311.[CrossRef][PubMed]
114. Dugar G,, Herbig A,, Förstner KU,, Heidrich N,, Reinhardt R,, Nieselt K,, Sharma CM . 2013. High-resolution transcriptome maps reveal strain-specific regulatory features of multiple Campylobacter jejuni isolates. PLoS Genet 9 : e1003495.[CrossRef][PubMed]
115. Sharma CM,, Hoffmann S,, Darfeuille F,, Reignier J,, Findeiss S,, Sittka A,, Chabas S,, Reiche K,, Hackermüller J,, Reinhardt R,, Stadler PF,, Vogel J . 2010. The primary transcriptome of the major human pathogen Helicobacter pylori. Nature 464 : 250 255.[CrossRef][PubMed]
116. Mitschke J,, Georg J,, Scholz I,, Sharma CM,, Dienst D,, Bantscheff J,, Voss B,, Steglich C,, Wilde A,, Vogel J,, Hess WR . 2011. An experimentally anchored map of transcriptional start sites in the model cyanobacterium Synechocystis sp. PCC6803. Proc Natl Acad Sci U S A 108 : 2124 2129.[CrossRef][PubMed]
117. Pfreundt U,, Kopf M,, Belkin N,, Berman-Frank I,, Hess WR . 2014. The primary transcriptome of the marine diazotroph Trichodesmium erythraeum IMS101. Sci Rep 4 : 6187.[CrossRef][PubMed]
118. Güell M,, van Noort V,, Yus E,, Chen WH,, Leigh-Bell J,, Michalodimitrakis K,, Yamada T,, Arumugam M,, Doerks T,, Kühner S,, Rode M,, Suyama M,, Schmidt S,, Gavin AC,, Bork P,, Serrano L . 2009. Transcriptome complexity in a genome-reduced bacterium. Science 326 : 1268 1271.[CrossRef][PubMed]
119. Orell A,, Tripp V,, Aliaga-Tobar V,, Albers SV,, Maracaja-Coutinho V,, Randau L . 2018. A regulatory RNA is involved in RNA duplex formation and biofilm regulation in Sulfolobus acidocaldarius. Nucleic Acids Res 46 : 4794 4806.[CrossRef][PubMed]


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
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

This is a required field
Please enter a valid email address
Please check the format of the address you have entered.
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error