Chapter 8 : Processive Antitermination

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An extraordinarily diverse range of genetic regulatory mechanisms has been discovered in the half century since Francois Jacob and Jacques Monod first proposed the operon model of gene regulation ( ). Studies based on this model identified a soluble regulator, located distally from the targeted operon, that acts to repress transcription initiation of the operon. This discovery led to the identification and characterization of many more repressor proteins, each acting in modestly different ways to reduce the efficiency of transcription initiation. Soon followed discoveries of other types of transcriptional regulators, including those that activate gene expression by enhancing transcription initiation. And now, in an era in which bacterial genome sequences can be acquired and draft-annotated in mere days and at low cost, it is clear that all bacteria encode dozens or hundreds of proteins that regulate transcription initiation and that this “layer” of genetic regulation is both ubiquitous and profoundly important. However, perhaps because transcription initiation is so universally recognized as a key point of regulatory influence ( ), later stages of transcription elongation have not yet been sufficiently analyzed for genetic regulation. While the molecular mechanisms of transcription have been, and continue to be, intensively investigated, the biological extent of postinitiation regulatory mechanisms has been incompletely analyzed. Transcription initiation is only the first stage of gene expression. The stages that follow include transcription elongation, transcription termination, translation, and mRNA degradation; each of these stages can be subjected to genetic regulatory control ( ).

Citation: Goodson J, Winkler W. 2019. Processive Antitermination, p 117-131. In Storz G, Papenfort K (ed), Regulating with RNA in Bacteria and Archaea. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.RWR-0031-2018
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Figure 1

Genomic context of PA systems. This figure schematically illustrates the transcripts regulated by the λN, , rRNA, and EAR RNA-based antitermination systems. (A) Phage λ early transcripts are initiated from two divergently facing promoters with elements found early in the transcripts. The λN protein is encoded by the first gene in the left early transcript. RNAP complexes associated with λN bypass multiple terminators in both transcripts. Using a different mechanism, the λQ protein promotes antitermination of the late transcript by binding to DNA near the late promoter and promoting a terminator-resistant configuration of RNAP. (B) Phage HK022 early transcripts are similar to phage λ, although they include elements early in each transcript, which trigger λN-independent antitermination. Additional Rho-dependent terminators are likely present in these transcripts, although they have not been specifically characterized and are therefore not indicated here. (C) A representative rRNA operon is shown, containing elements immediately downstream of the P promoter. These elements promote read-through of Rho-dependent termination in the noncoding rRNA genes. (D) Several intrinsic terminators have been demonstrated in the operon, which codes for biosynthesis of biofilm exopolysaccharides. The -associated RNA (EAR) is found within the intergenic region and promotes read-through of the terminators within the operon. Intrinsic terminators are shown as sticks with empty circles, and Rho termination regions are shown as sticks with wavy lines, both in red. RNA elements involved in antitermination are shown in blue, and proteins and protein-coding genes involved in antitermination are shown in green. Elements are not shown to scale.

Citation: Goodson J, Winkler W. 2019. Processive Antitermination, p 117-131. In Storz G, Papenfort K (ed), Regulating with RNA in Bacteria and Archaea. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.RWR-0031-2018
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Figure 2

Cryo-EM reveals details of the antitermination mechanism. This figure contains structural models generated from cryo-EM data on TECs (PDB IDs: 5MS0 and 6FLQ). (A) The λN antitermination complex (PDB ID: 5MS0) comprising λN (black), NusA (magenta), NusB (red), S10 (orange), NusG (green), and RNA (blue), in addition to RNAP (gray). (B) A zoom-in on the and λN complex shows extended binding of the RNA sequence with multiple protein components, with bound to the NusB-S10 dimer and the hairpin bound to λN and NusA. (C) Formation of the λN antitermination complex shifts the position of NusA (magenta) by 40° away from the RNA exit channel, as compared to NusA (purple) in a TEC constructed with the hairpin-mediated pause sequence (PDB ID: 6FLQ). Nascent RNA is shown in green.

Citation: Goodson J, Winkler W. 2019. Processive Antitermination, p 117-131. In Storz G, Papenfort K (ed), Regulating with RNA in Bacteria and Archaea. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.RWR-0031-2018
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Figure 3

RNA elements involved in PA. This figure shows the sequence and secondary structure of RNA elements known or predicted to be utilized in PA mechanisms. Shown are the and elements forming the λN sequence as well as rRNA antitermination signal, the RNA element from phage HK022, EAR from the exopolysaccharide pathway, and a UNCG-type hairpin implicated in LoaP antitermination.

Citation: Goodson J, Winkler W. 2019. Processive Antitermination, p 117-131. In Storz G, Papenfort K (ed), Regulating with RNA in Bacteria and Archaea. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.RWR-0031-2018
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Figure 4

Genomic context of NusG paralog antitermination systems. This figure illustrates the transcripts regulated by the RfaH, LoaP, and UpxY antitermination systems. (A) RfaH regulates multiple pathways in , including the hemolysin, F pilus, and lipo- and exopolysaccharide operons. Each regulated transcript includes the DNA element for RfaH recruitment. RfaH promotes antitermination of Rho-dependent promoters. (B) LoaP regulates two polyketide antibiotic operons in : the difficidin operon and the macrolactin operon. LoaP is found divergently oriented upstream of the operon. Each transcript includes a required sequence region in the 5′ leader region, which might include a functionally important hairpin followed by an intrinsic terminator. Additional intrinsic terminator sites have been implicated within the and operons, although they are not shown in this figure. (C) UpxY proteins regulate multiple capsular polysaccharide pathways in . Each polysaccharide operon includes both a UpxY and UpxZ protein involved in targeted regulation, with the 5′ leader sequence required for antitermination. has eight distinct polysaccharide operons containing UpxY proteins. Gray rectangles represent multigene operons. RNA elements potentially involved in antitermination are shown in blue, and proteins and protein-coding genes involved in antitermination are shown in green.

Citation: Goodson J, Winkler W. 2019. Processive Antitermination, p 117-131. In Storz G, Papenfort K (ed), Regulating with RNA in Bacteria and Archaea. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.RWR-0031-2018
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Figure 5

The RfaH CTD undergoes a large conformational shift from an α-helix to a β-barrel. Full-length RfaH (left) exists as an autoinhibited structure with the CTD (blue) in an α-helix conformation bound to the NTD (red) (PDB ID: 2OUG). Upon binding to RNAP and the DNA, the CTD (right) is released and forms the β-barrel conformation characteristic of NusG KOW domains (PDB ID: 2LCL).

Citation: Goodson J, Winkler W. 2019. Processive Antitermination, p 117-131. In Storz G, Papenfort K (ed), Regulating with RNA in Bacteria and Archaea. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.RWR-0031-2018
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Figure 6

Phylogenetic tree of NusG, Spt5, and specialized NusG paralog groups. Represented NusG sequences selected from the subgroups discussed in this review form the NusG family. Bacterial sequences from core NusG proteins are found in all bacteria, while a variety of paralogs are found in diverse bacteria phyla. Some groups of NusG paralogs are commonly found in or adjacent to large gene clusters coding for production of polysaccharides (PS) or polyketides (PK).

Citation: Goodson J, Winkler W. 2019. Processive Antitermination, p 117-131. In Storz G, Papenfort K (ed), Regulating with RNA in Bacteria and Archaea. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.RWR-0031-2018
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