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Research Paper

Architectures and complex functions of tandem riboswitches

Madeline E. Sherlocka Department of Molecular Biophysics and Biochemistry, Yale University, New Haven, CT, USA;b Department of Biochemistry and Molecular Genetics, University of Colorado, Anschutz Medical Campus, Research-1S, Aurora, CO, USAORCID Iconhttps://orcid.org/0000-0002-6471-4243View further author information
ORCID Icon,
Gadareth Higgsc Department of Molecular, Cellular and Developmental Biology, Yale University, New Haven, CT, USAView further author information
,
Diane Yuc Department of Molecular, Cellular and Developmental Biology, Yale University, New Haven, CT, USAView further author information
,
Danielle L. Widnera Department of Molecular Biophysics and Biochemistry, Yale University, New Haven, CT, USAView further author information
,
Neil A. Whitec Department of Molecular, Cellular and Developmental Biology, Yale University, New Haven, CT, USAView further author information
,
Narasimhan Sudarsand Howard Hughes Medical Institute, Yale University, New Haven, CT, USAView further author information
,
Harini Sadeeshkumarc Department of Molecular, Cellular and Developmental Biology, Yale University, New Haven, CT, USAView further author information
,
Kevin R. Perkinsc Department of Molecular, Cellular and Developmental Biology, Yale University, New Haven, CT, USAView further author information
,
Gayan Mirihana Arachchilaged Howard Hughes Medical Institute, Yale University, New Haven, CT, USA;e PTC Therapeutics, Inc, South Plainfield, NJ, USAView further author information
,
Sarah N. Malkowskif Department of Chemistry, Yale University, New Haven, CT, USAView further author information
,
Christopher G. Kinga Department of Molecular Biophysics and Biochemistry, Yale University, New Haven, CT, USAView further author information
,
Kimberly A. Harrisd Howard Hughes Medical Institute, Yale University, New Haven, CT, USAView further author information
,
Glenn Gaffieldc Department of Molecular, Cellular and Developmental Biology, Yale University, New Haven, CT, USAView further author information
,
Ruben M. Atilhoc Department of Molecular, Cellular and Developmental Biology, Yale University, New Haven, CT, USAView further author information
&
Ronald R. Breakera Department of Molecular Biophysics and Biochemistry, Yale University, New Haven, CT, USA;c Department of Molecular, Cellular and Developmental Biology, Yale University, New Haven, CT, USA;d Howard Hughes Medical Institute, Yale University, New Haven, CT, USACorrespondence[email protected]
ORCID Iconhttps://orcid.org/0000-0002-2165-536XView further author information
ORCID Icon show all
Pages 1059-1076 | Received 27 May 2022, Accepted 23 Aug 2022, Published online: 11 Sep 2022

References

  • Nahvi A, Sudarsan N, Ebert MS, et al. Genetic control by a metabolite binding mRNA. Chem Biol. 2002;9:1043–1049.
  • Winkler W, Nahvi A, Breaker RR. Thiamine derivatives bind messenger RNAs directly to regulate bacterial gene expression. Nature. 2002;419:952–956.
  • Mironov AS, Gusarov I, Rafikov R, et al. Sensing small molecules by nascent RNA: a mechanism to control transcription in bacteria. Cell. 2002;111:747–756.
  • Winkler WC, Cohen-Chalamish S, Breaker RR. An mRNA structure that controls gene expression by binding FMN. Proc Natl Acad Sci USA. 2002;99:15908–15913.
  • Sherwood AV, Henkin TM. Riboswitch-mediated gene regulation: novel RNA architectures dictate gene expression responses. Annu Rev Microbiol. 2016;70:361–374.
  • McCown PJ, Corbino KA, Stav S, et al. Riboswitch diversity and distribution. RNA. 2017;23:995–1011.
  • Vézina Bédard A-S, Hien EDM, Lafontaine DA. Riboswitch regulation mechanisms: RNA, metabolites and regulatory proteins. BBA – Gene Regul Mech. 2020;1863:194501.
  • Breaker RR. Prospects for riboswitch discovery and analysis. Mol Cell. 2011;43:867–879.
  • Mandal M, Breaker RR. Adenine riboswitches and gene activation by disruption of a transcription terminator. Nat Struct Mol Biol. 2004;11:29–35.
  • Regulski EE, Moy RH, Weinberg Z, et al. A widespread riboswitch candidate that controls bacterial genes involved in molybdenum cofactor and tungsten cofactor metabolism. Mol Microbiol. 2008;68:918–932.
  • Kellenberger CA, Wilson SC, Hickey SF, et al. GEMM-I riboswitches from geobacter sense the bacterial second messenger cyclic AMP-GMP. Proc Natl Acad Sci USA. 2015;112:5383–5388.
  • Nelson JW, Sudarsan N, Phillips GE, et al. Control of bacterial exoelectrogenesis by c-AMP-GMP. Proc Natl Acad Sci USA. 2015;112:5389–5394.
  • Sherlock ME, Sadeeshkumar H, Breaker RR. Variant bacterial riboswitches associated with nucleotide hydrolase genes sense nucleoside diphosphates. Biochemistry. 2019;58:401–410.
  • Ames TD, Breaker RR. Bacterial riboswitch discovery and analysis. In: Mayer G, editor. The chemical biology of nucleic acids. Chichester (UK): Wiley; 2010. pp. 433–454.
  • Breaker RR. Riboswitches and the RNA world. Cold Spring Harb Perspect Biol. 2012;4:a003566.
  • Serganov A, Patel DJ. Metabolite recognition principles and molecular mechanisms underlying riboswitch function. Annu Rev Biophys. 2012;41:343–370.
  • Peselis A, Serganov A. Themes and variations in riboswitch structure and function. Biochim Biophys Acta. 2014;1839:908–918.
  • Savinov A, Perez CF, Block SM. Single-molecule studies of riboswitch folding. Biochim Biophys Acta. 2014;1839:1030–1045.
  • Boudreault J, Perez-Gonzalez DC, Penedo JC, et al. Single-molecule approaches for the characterization of riboswitch folding mechanisms. Methods Mol Biol. 2015;1334:101–107.
  • Hua B, Jones CP, Mitra J, et al. Real-time monitoring of single ZTP riboswitches reveals a complex and kinetically controlled decision landscape. Nat Commun. 2020;11:4531.
  • Helmling C, Wacker A, Wolfinger MT, et al. NMR structural profiling of transcriptional intermediates reveals riboswitch regulation by metastable RNA conformations. J Am Chem Soc. 2017;139:2647–2656.
  • de Jesus V, Qureshi NS, Warhaut S, et al. Switching at the ribosome: riboswitches need rProteins as modulators to regulate translation. Nat Commun. 2021;12:4723.
  • Benner SA, Ellington AD, Tauer A. Modern metabolism as a palimpsest of the RNA world. Proc Natl Acad Sci USA. 1989;86(18):7054–7058.
  • Chen X, Li N, Ellington AD. Ribozyme catalysis of metabolism in the RNA world. Chem Biodivers. 2007;4:633–655.
  • Sudarsan N, Hammond MC, Block KF, et al. Tandem riboswitch architectures exhibit complex gene control functions. Science. 2006;314:300–304.
  • Stoddard CD, Batey RT. Mix-and-match riboswitches. ACS Chem Biol. 2006;12:751–754.
  • Mandal M, Lee M, Barrick JE, et al. A glycine-dependent riboswitch that uses cooperative binding to control gene expression. Science. 2004;306:275–279.
  • Lehman E, Leighton FT, Meyer AR. In: Mathematics for computer science, 12th media services, 2017; Ch. 1.
  • Nawrocki EP, Eddy SR. Infernal 1.1: 100-fold faster RNA homology searches. Bioinformatics. 2013;29:2933–2935.
  • Pruitt K, Tatusova T, Maglott D. NCBI reference sequence (RefSeq): a curated non-redundant sequence database of genomes, transcripts and proteins. Nucleic Acids Res. 2005;33:D501–D504.
  • O’Leary NA, Wright MW, Brister JR, et al. Reference sequence (RefSeq) database at NCBI: current status, taxonomic expansion, and functional annotation. Nucleic Acids Res. 2016;44:D733–D745.
  • Roth A, Weinberg Z, Chen AG, et al. A widespread self-cleaving ribozyme class is revealed by bioinformatics. Nat Chem Biol. 2014;10:56–60.
  • Weinberg Z, Wang JX, Bogue J, et al. Comparative genomics reveals 104 candidate structured RNAs from bacteria, archaea, and their metagenomes. Genome Biol. 2010;11:R31.
  • Marchler-Bauer A, Derbyshire MK, Gonzales NR, et al. CDD: NCBI’s conserved domain database. Nucleic Acids Res. 2015;43:D222–D226.
  • Weinberg Z, Lunse CE, Corbino KA, et al. Detection of 224 candidate structured RNAs by comparative analysis of specific subsets of intergenic regions. Nucleic Acid Res. 2017;45:10811–10823.
  • Nawrocki EP, Burge SW, Bateman A, et al. Rfam 12.0: updates to the RNA families database. Nucleic Acids Res. 2015;43(D1):D130–D137.
  • Yao Z, Barrick J, Weinberg Z, et al. A computational pipeline for high-throughput discovery of cis-regulatory noncoding RNA in prokaryotes. PLoS Comput Biol. 2007;3:e126.
  • Weinberg Z, Ruzzo WL. Sequence-based heuristics for faster annotation of non-coding RNA families. Bioinformatics. 2006;22:35–39.
  • Mirihana Arachchilage G, Sherlock ME, Weinberg Z, et al. SAM-VI RNAs selectively bind S-adenosylmethionine and exhibit similarities to SAM-III riboswitches. RNA Biol. 2018;15:371–378.
  • Soukup GA, Breaker RR. Relationship between internucleotide linkage geometry and the stability of RNA. RNA. 1999;5:1308–1325.
  • Regulski EE, Breaker RR. In-line probing analysis of riboswitches. Methods Mol Biol. 2008;419:53–67.
  • Sudarsan N, Lee ER, Weinberg Z, et al. Riboswitches in eubacteria sense the second messenger cyclic di-GMP. Science. 2008;321:5887.
  • Smith KD, Lipchock SV, Ames TD, et al. Structural basis of ligand binding by a c-di-GMP riboswitch. Nat Struct Mol Biol. 2009;16:1218–1223.
  • Trausch JJ, Ceres P, Reyes FE, et al. The structure of a Tetrahydrofolate-sensing riboswitch reveals two ligand binding sites in a single aptamer. Structure. 2011;19(10):1413–1423.
  • Gao A, Serganov A. Structural insights into recognition of c-di-AMP by the ydaO riboswitch. Nat Chem Biol. 2014;10:787–792.
  • Ren A, Patel DJ. c-di-AMP binds the ydaO riboswitch in two pseudo-symmetry-related pockets. Nat Chem Biol. 2014;10:780–786.
  • Jones CP, Ferré-D’Amaré AR. Crystal structure of a c-di-AMP riboswitch reveals an internally pseudo-dimeric RNA. EMBO J. 2014;33:2692–2703.
  • Schroeder GM, Cavender CE, Blau ME, et al. A small RNA that cooperatively senses two stacked metabolites in one pocket for gene control. Nat Commun. 2022;13:199.
  • Dann IIICE, Wakeman CA, Sieling CL, et al. Structure and mechanism of a metal-sensing regulatory RNA. Cell. 2007;130:878–892.
  • Furukawa K, Ramesh A, Zhou Z, et al. Bacterial riboswitches cooperatively bind Ni2+ or Co2+ ions and control expression of heavy metal transporters. Mol Cell. 2015;57:1088–1098.
  • Kwon M, Strobel SA. Chemical basis of glycine riboswitch cooperativity. RNA. 2008;14:25–34.
  • Erion TV, Strobel SA. Identification of a tertiary interaction important for cooperative ligand binding by the glycine riboswitch. RNA. 2011;17:74–84.
  • Butler EB, Xiong Y, Wang J, et al. Structural basis of cooperative ligand binding by the glycine riboswitch. Chem Biol. 2011;18:293–298.
  • Welz R, Breaker RR. Ligand binding and gene control characteristics of tandem riboswitches in Bacillus anthracis. RNA. 2007;13:573–582.
  • Poiata E, Meyer MM, Ames TD, et al. A variant riboswitch aptamer class for S-adenosylmethionine common in marine bacteria. RNA. 2009;15:2046–2056.
  • Sherlock ME, Sudarsan N, Stav S, et al. Tandem riboswitches form a natural Boolean logic gate to control purine metabolism in bacteria. eLife. 2018;7:e33908.
  • Wilson KS, von Hippel PH. Transcription termination at intrinsic terminators: the role of the RNA hairpin. Proc Natl Acad Sci USA. 1995;92:8793–8797.
  • Yarnell WS, Roberts JW. Mechanism of intrinsic transcription termination and antitermination. Science. 1999;284:611–615.
  • Lee ER, Baker JL, Weinberg Z, et al. An allosteric self-splicing ribozyme triggered by a bacterial second messenger. Science. 2010;329:845–848.
  • Hougland JL, Piccirilli JA, Forconi M, et al. How the group I intron works: a case study of RNA structure and function. Gesteland, RF, Cech, TR, Atkins, JF. eds. In: The RNA World, 3rd ed., Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press. 2006;pp. 133–205.
  • Chen AGY, Sudarsan N, Breaker RR. Mechanism for gene control by a natural allosteric group I ribozyme. RNA. 2011;17:1967–1972.
  • Bengert P, Dandekar T. Riboswitch finder – a tool for identification of riboswitch RNAs. Nucleic Acids Res. 2004;32:W154–W159.
  • Singh P, Bandyopadhyay P, Bhattacharya S, et al. Riboswitch detection using profile hidden Markov models. BMC Bioinformatics. 2009;10:325.
  • Ruff KM, Muhammad A, McCown PJ, et al. Singlet glycine riboswitches bind ligand as well as tandem riboswitches. RNA. 2016;22:1728–1738.
  • Torgerson CD, Hiller DA, Stav S, et al. Gene regulation by a glycine riboswitch singlet uses a finely tuned energetic landscape for helical switching. RNA. 2018;24:1813–1827.
  • Sherman EM, Esquiaqui J, Elsayed G, et al. An energetically beneficial leader-linker interaction abolishes ligand-binding cooperativity in glycine riboswitches. RNA. 2012;18:496–507.
  • Baird NJ, Ferré-D’Amaré AR. Modulation of quaternary structure and enhancement of ligand binding by the K-turn of tandem glycine riboswitches. RNA. 2013;19:167–176.
  • Torgerson CD, Hiller DA, Strobel SA. The asymmetry and cooperativity of tandem glycine riboswitch aptamers. RNA. 2020;26:564–580.
  • Weinberg Z, Nelson JW, Lünse CE, et al. Bioinformatic analysis of riboswitch structures uncovers variant classes with altered ligand specificity. Proc Natl Acad Sci USA. 2017;114:E2077–E2085.
  • Sherlock ME, Malkowski SN, Breaker RR. Biochemical validation of a second guanidine riboswitch class in bacteria. Biochemistry. 2017;56:352–358.
  • Reiss CW, Strobel SA. Structural basis for ligand binding to the guanidine-II riboswitch. RNA. 2017;23:1338–1343.
  • Huang L, Wang J, Lilley DMJ. The structure of the guanidine-II riboswitch. Cell Chem Biol. 2017;24:695–702.
  • Nelson JW, Atilho RM, Sherlock ME, et al. Metabolism of free guanidine in bacteria is regulated by a widespread riboswitch class. Mol Cell. 2017;65:220–230.
  • Sherlock ME, Breaker RR. Biochemical validation of a third guanidine riboswitch class in bacteria. Biochemistry. 2017;56:359–363.
  • Lenkeit F, Eckert I, Hartig JS. Discovery and characterization of a fourth class of guanidine riboswitches. Nucleic Acids Res. 2020;48:12889–12899.
  • Salvail H, Balaji A, Yu D, et al. Biochemical validation of a fourth guanidine riboswitch class in bacteria. Biochemistry. 2020;59:4654–4662.
  • Malkowski SN, Spencer TCJ, Breaker RR. Evidence that the nadA motif is a bacterial riboswitch for the ubiquitous enzyme cofactor NAD. RNA. 2019;25:1616–1627.
  • Huang L, Wang J, Lilley DMJ. Structure and ligand binding of the ADP-binding domain of the NAD+ riboswitch. RNA. 2020;26:878–887.
  • Chen H, Egger M, Xu X, et al. Structural distinctions between NAD+ riboswitch domains 1 and 2 determine differential folding and ligand binding. Nucleic Acids Res. 2020;48:12394–12406.
  • Watson PY, Fedor MJ. The ydaO motif is an ATP-sensing riboswitch in Bacillus subtilis. Nat Chem Biol. 2012;8:963–965.
  • Nelson JW, Sudarsan N, Furukawa K, et al. Riboswitches in eubacteria sense the second messenger c-di-AMP. Nat Chem Biol. 2013;9:834–839.
  • Breaker laboratory, unpublished findings.
  • McDaniel BA M, Grundy FJ, Artsimovitch I, et al. Transcription termination control of the S box system: direct measurement of S-adenosylmethionine by the leader RNA. Proc Natl Acad Sci USA. 2003;100:3083–3088.
  • Winkler WC, Nahvi A, Sudarsan N, et al. An mRNA structure that controls gene expression by binding S-adenosylmethionine. Nat Struct Mol Biol. 2003;10:701–707.
  • Epshtein V, Mironov AS, Nudler E. The riboswitch-mediated control of sulfur metabolism in bacteria. Proc Natl Acad Sci USA. 2003;100:5052–5056.
  • Corbino KA, Barrick JE, Lim J, et al. Evidence for a second class of S-adenosylmethionine riboswitches and other regulatory RNA motifs in alpha-proteobacteria. Genome Biol. 2005;6:R70.
  • Barrick JE, Breaker RR. The distributions, mechanisms, and structures of metabolite-binding riboswitches. Genome Biol. 2007;8:R239.
  • Breaker RR. Riboswitches and translation control. Cold Spring Harb Perspect Biol. 2018;10:a032797.
  • Kim PB, Nelson JW, Breaker RR. An ancient riboswitch class in bacteria regulates purine biosynthesis and one-carbon metabolism. Mol Cell. 2015;57:317–328.
  • Bochner BR, Ames BN. ZTP (5-amino 4-imidazole carboxamide riboside 5′-triphosphate): a proposed alarmone for 10-formyl-tetrahydrofolate deficiency. Cell. 1982;29:929–937.
  • Nichols J, Rajagopalan KV. Escherichia coli MoeA and Moga function in metal incorporation step of molybdenum cofactor biosynthesis. J Biol Chem. 2002;277:24995–25000.
  • Jenal U, Reinders A, Lori C. Cyclic di-GMP: second messenger extraordinaire. Nat Rev Microbiol. 2017;15:271–284.
  • Zhou H, Zheng C, Su J, et al. Characterization of a natural triple-tandem c-di-GMP riboswitch and application of the riboswitch-based dual-fluorescence reporter. Sci Rep. 2016;6:20871.
  • Nelson JW, Sudarsan N, Kurukawa K, et al. Riboswitches in eubacteria sense the second messenger c-di-AMP. Nat Chem Biol. 2013;9:834–839.
  • Mandal M, Boese B, Barrick JE, et al. Riboswitches control fundamental biochemical pathways in Bacillus subtilis and other bacteria. Cell. 2003;113:577–586.
  • Grundy FJ, Lehman SC, Henkin TM. The L box regulon: lysine sensing by leader RNAs of bacterial lysine biosynthesis genes. Proc Natl Acad Sci USA. 2003;100:12057–12062.
  • Sudarsan N, Wickiser JK, Nakamura S, et al. An mRNA structure in bacteria that controls gene expression by binding lysine. Genes Dev. 2003;17:2688–2697.
  • Barrick JE, Corbino KA, Winkler WC, et al. New RNA motifs suggest an expanded scope for riboswitches in bacterial genetic control. Proc Natl Acad Sci USA. 2004;101:6421–6426.
  • Ames TD, Breaker RR. Bacterial aptamers that selectively bind glutamine. RNA Biol. 2011;8:82–89.
  • White N, Sadeeshkumar H, Sun A, et al. Lithium-sensing riboswitch classes regulate expression of bacterial cation transporter genes. ( submitted).
  • Wang JX, Breaker RR. Riboswitches that sense S-adenosylmethionine and S-adenosylhomocysteine. Biochem Cell Biol. 2008;86:157–168.
  • Gilbert SD, Rambo RP, VanTyne D, et al. Structure of the SAM-II riboswitch bound to S-adenosylmethionine. Nat Struct Mol Biol. 2008;15:177–182.
  • Huang L, Lilley DMJ. Structure and ligand binding of the SAM-V riboswitch. Nucleic Acids Res. 2018;46:6869–6879.
  • Weinberg Z, Regulski EE, Hammond MC, et al. The aptamer core of SAM-IV riboswitches mimics the ligand-binding site of SAM-I riboswitches. RNA. 2008;14:822–828.
  • Atilho RM, Mirihana Arachicilage G, Greenlee EB, et al. A bacterial riboswitch class for the thiamin precursor HMP-PP employs a terminator-embedded aptamer. eLife. 2019;8:e45210.
  • Sherlock ME, Sudarsan N, Breaker RR. Riboswitches for the alarmone ppGpp expand the collection of RNA-based signaling systems. Proc Natl Acad Sci USA. 2018;115:6052–6057.
  • Kreuzer KD, Henkin TM, Storz G. The T-box riboswitch: tRNA as an effector to modulate gene regulation. Microbiol Spectr. 2018;6(4):6–4.
  • Irving SE, Choudhury NR, Corrigan RM. The stringent response and physiological roles of (pp)pGpp in bacteria. Nat Rev Microbiol. 2021;19:256–271.
  • Barnhart MM, Chapman MR. Curli biogenesis and function. Annu Rev Microbiol. 2006;60:131–147.
  • Goyal P, Krasteva PV, Van Gerven N, et al. Structural and mechanistic insights into the bacterial amyloid secretion channel CsgG. Nature. 2014;516:250–253.
  • Simm R, Morr M, Kader A, et al. GGDEF and EAL domains inversely regulate cyclic di-GMP levels and transition from sessility to motility. Mol Microbiol. 2004;53:1123–1134.
  • Chirwa NT, Herrington MB. CsgD, a regulator of curli and cellulose synthesis, also regulates serine hydroxymethyltransferase synthesis in Escherichia coli K-12. Microbiology. 2003;149:525–535.
  • Ferla MP, Patrick WM. Bacterial methionine biosynthesis. Microbiology. 2014;160:1571–1584.
  • Gonzalez JC, Peariso K, Penner-Hahn JE, et al. Cobalamin-independent methionine synthase from Escherichia coli: a zinc metalloenzyme. Biochemistry. 1996;35:12228–12234.
  • McCown PJ, Liang JJ, Weinberg Z, et al. Structural, functional, and taxonomic diversity of three preQ1 riboswitch classes. Chem Biol. 2014;21:880–889.
  • Ames TD, Rodionov DA, Weinberg Z, et al. A eubacterial riboswitch class that senses the coenzyme tetrahydrofolate. Chem Biol. 2010;17:681–685.
  • Stolz M, Peters-Wendisch P, Etterich H, et al. Reduced folate supply as a key to enhanced L-serine production by Corynebacterium glutamicum. Appl Environ Microbiol. 2007;7(3):750–755.
  • White N, Sadeeshkumar H, Sun A, et al. A bacterial riboswitch class for Na+ regulates genes for ion transport, osmoregulation, and ATP production. Nat Chem Biol. 2022;18(8):878–885. (in press).
  • Commichau FM, Gibhardt J, Halbedel S, et al. A delicate connection: c-di-AMP affects cell integrity by controlling osmolyte transport. Trends Microbiol. 2018;26:175–185.
  • Stülke J, Krüger L. Cyclic-di-AMP signaling in bacteria. Annu Rev Microbiol. 2020;8:159–179.
  • Begley TP, Ealick SE, McLafferty FW. Thiamin biosynthesis: still yielding fascinating biological chemistry. Biochem Soc Trans. 2012;40:555–560.
  • Santos CNS, Xiao W, Stephanopoulos G. Rational, combinatorial, and genomic approaches for engineering L-tyrosine production in Escherichia coli. Proc Natl Acad Sci USA. 2012;109:13538–13543.
  • Kazanov MD, Vitreschak AG, Gelfand MS. Abundance and functional diversity of riboswitches in microbial communities. BMC Genomics. 2007;8:347.
  • Gutiérrez-Preciado A, Henkin TM, Grundy FJ, et al. Biochemical features and functional implications of the RNA-based T-box regulatory mechanism. Microbiol Mol Biol Rev. 2009;73:36–61.
  • Krásný L, Tišerová H, Jonák J, et al. The identity of the transcription +1 position is crucial for changes in gene expression in response to amino acid starvation in Bacillus subtilis. Mol Microbiol. 2008;69:42–54.
  • Johnson JEsJr, Reyes RE, Polaski JT, et al. B12 cofactors directly stabilize an mRNA regulatory switch. Nature. 2012;492:133–137.
  • Wang F, Gu Y, O’Brien JP, et al. Structure of microbial nanowires reveals stacked hemes that transport electrons over micrometers. Cell. 2019;177:361–369.
  • Winkler WC, Nahvi A, Roth A, et al. Control of gene expression by a natural metabolite-responsive ribozyme. Nature. 2004;428:281–286.
  • Klein DJ, Ferré-D’Amaré AR. Structural basis of glmS ribozyme activation by glucosamine-6-phosphate. Science. 2006;313:1752–1756.
  • Cochrane JC, Lipchock SV, Strobel SA. Structural investigation of the GlmS ribozyme bound to its catalytic cofactor. Chem Biol. 2007;14:97–105.
  • de la Peña M, García-Robles I, Cervera A, et al. The hammerhead ribozyme: a long history for a short RNA. Molecules. 2017;22:78.
  • Wu HN, Lin YJ, Lin FP, et al. Human hepatitis delta virus RNA subfragments contain an autocleavage activity. Proc Natl Acad Sci USA. 1989;86:1831–1835.
  • Weinberg Z, Kim PB, Chen TH, et al. New classes of self-cleaving ribozymes revealed by comparative genomics analysis. Nat Chem Biol. 2015;11:606–610.
  • Harris KA, Lünse CE, Li S, et al. Biochemical analysis of pistol self-cleaving ribozymes. RNA. 2015;21:1852–1858.
  • Li S, Lünse CE, Harris KA, et al. Biochemical analysis of hatchet self-cleaving ribozymes. RNA. 2015;21:1845–1851.
  • Panchapakesan SSS, Breaker RR. The case of the missing allosteric ribozymes. Nat Chem Biol. 2021;17:375–382.
  • Candales MA, Duong A, Hood KS, et al. Database for bacterial group II introns. Nucleic Acids Res. 2012;40:D187–190.
  • Moretz SE, Lampson BC. A group IIC-type intron interrupts the rRNA methylase gene of Geobacillus stearothermophilus strain 10. J Bacteriol. 2010;192:5245–5248.
  • Xu J, Cotruvo JAsJr. The czcD (NiCo) riboswitch responds to Iron(II). Biochemistry. 2020;59:1508–1516.
  • Dambach M, Sandoval M, Updegrove TB, et al. The ubiquitous yybP-ykoY riboswitch is a manganese-responsive regulatory element. Mol Cell. 2015;57:1099–1109.
  • Price IR, Gaballa A, Ding F, et al. Mn2+-sensing mechanisms of yybP-ykoY orphan riboswitches. Mol Cell. 2015;57(6):1110–1123.
  • Vitreschak AG, Rodionov DA, Mironov AA, et al. Regulation of the vitamin B12 metabolism and transport in bacteria by a conserved RNA structural element. RNA. 2003;9:1084–1097.
  • Choudhary PK, Duret A, Rohrbach-Brandt E, et al. Diversity of cobalamin riboswitches in the corrinoid-producing organohalide respire Desulfitobacterium hafniense. J Bacteriol. 2013;195:5186–5195.
  • Breaker RR. Complex riboswitches. Science. 2008;319:1795–1797.
  • Greenlee EB, Stav S, Atilho RM, et al. Challenges of ligand identification for the second wave of orphan riboswitch candidates. RNA Biol. 2018;15:377–390.
  • Stav S, Atilho RM, Mirihana Arachchilage G, et al. Genome-wide discovery of structured noncoding RNAs in bacteria. BMC Microbiol. 2019;19:66.
  • Brewer KI, Greenlee EB, Higgs G, et al. Comprehensive discovery of novel structured noncoding RNAs in 26 bacterial genomes. RNA Biol. 2021;18:2417–2432.
  • Tang J, Breaker RR. Rational design of allosteric ribozymes. Chem Biol. 1997;4:453–459.
  • Tang J, Breaker RR. Examination of the catalytic fitness of the hammerhead ribozyme by in vitro selection. RNA. 1997;3:914–925.
  • Araki M, Okuno Y, Hara Y, et al. Allosteric regulation of a ribozyme activity through ligand-induced conformational change. Nucleic Acids Res. 1998;26:3379–3384.
  • Robertson MP, Ellington AD. In vitro selection of an allosteric ribozyme that transduces analytes to amplicons. Nat Biotechnol. 1999;17:62–66.

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