Abstract
Timely and accurate RNA synthesis depends on accessory proteins that instruct RNA polymerase (RNAP) where and when to start and stop transcription. Among thousands of transcription factors, NusG/Spt5 stand out as the only universally conserved family of regulators. These proteins interact with RNAP to promote uninterrupted RNA synthesis and with diverse cellular partners to couple transcription to RNA processing, modification or translation, or to trigger premature termination of aberrant transcription. NusG homologs are present in all cells that utilize bacterial-type RNAP, from endosymbionts to plants, underscoring their ancient and essential function. Yet, in stark contrast to other core RNAP components, NusG family is actively evolving: horizontal gene transfer and sub-functionalization drive emergence of NusG paralogs, such as bacterial LoaP, RfaH, and UpxY. These specialized regulators activate a few (or just one) operons required for expression of antibiotics, capsules, secretion systems, toxins, and other niche-specific macromolecules. Despite their common origin and binding site on the RNAP, NusG homologs differ in their target selection, interacting partners and effects on RNA synthesis. Even among housekeeping NusGs from diverse bacteria, some factors promote pause-free transcription while others slow the RNAP down. Here, we discuss structure, function, and evolution of NusG proteins, focusing on unique mechanisms that determine their effects on gene expression and enable bacterial adaptation to diverse ecological niches.
Highlights
Specialty section: This article was submitted to Microbial Physiology and Metabolism, a section of the journal Frontiers in MicrobiologyReceived: 20 October 2020 Accepted: December 2020Published: January 2021Citation: Wang B and Artsimovitch I (2021) NusG, an Ancient Yet Rapidly EvolvingTranscription Factor
In contrast to E. coli, where NusG aids Rho in termination of rut-less RNAs (Lawson and Berger, 2019), Rho-dependent termination in B. subtilis is strongly linked to cis-encoded C-rich RNA elements (Johnson et al, 2020). These results suggest that NusG is not involved in gene expression control by Rho in B. subtilis and raise a possibility that an alternative mechanism of transcription noise silencing operates in these species
Sequence-specific pausing through non-template DNA contacts has been first shown for RfaH (Artsimovitch and Landick, 2002), which recognizes 12-nt ops elements in the E. coli genome (Belogurov et al, 2009); RfaH-induced RNA polymerase (RNAP) delay is thought to facilitate the ribosome recruitment to the nascent RNA in a handful of leader regions
Summary
Specialty section: This article was submitted to Microbial Physiology and Metabolism, a section of the journal Frontiers in Microbiology. These results suggest that NusG is not involved in gene expression control by Rho in B. subtilis (and perhaps other related bacteria) and raise a possibility that an alternative mechanism of transcription noise silencing operates in these species Another key function of E. coli NusG is bridging the RNAP and the ribosome (Figure 7) to mediate transcriptiontranslation coupling, which is thought to occur in all singlecompartment cells (see above). Sequence-specific pausing through non-template DNA contacts has been first shown for RfaH (Artsimovitch and Landick, 2002), which recognizes 12-nt ops elements in the E. coli genome (Belogurov et al, 2009); RfaH-induced RNAP delay is thought to facilitate the ribosome recruitment to the nascent RNA (see below) in a handful of leader regions. Given that the principal role of the E. coli rrn-TACs appears to be in chaperoning of the nascent RNA (Huang et al, 2020), an analogous complex, with or without NusG, may be required to ensure the correct rRNA folding and processing in B. subtilis
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