1932

Abstract

Oxidative stress is an important and pervasive physical stress encountered by all kingdoms of life, including bacteria. In this review, we briefly describe the nature of oxidative stress, highlight well-characterized protein-based sensors (transcription factors) of reactive oxygen species that serve as standards for molecular sensors in oxidative stress, and describe molecular studies that have explored the potential of direct RNA sensitivity to oxidative stress. Finally, we describe the gaps in knowledge of RNA sensors—particularly regarding the chemical modification of RNA nucleobases. RNA sensors are poised to emerge as an essential layer of understanding and regulating dynamic biological pathways in oxidative stress responses in bacteria and, thus, also represent an important frontier of synthetic biology.

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2023-06-08
2024-12-09
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Literature Cited

  1. 1.
    Ding N, Zhou S, Deng Y. 2021.. Transcription-factor-based biosensor engineering for applications in synthetic biology. . ACS Synth. Biol. 10:(5):91122
    [Google Scholar]
  2. 2.
    Machtel P, Bąkowska-Żywicka K, Żywicki M. 2016.. Emerging applications of riboswitches—from antibacterial targets to molecular tools. . J. Appl. Genet. 57:(4):53141
    [Google Scholar]
  3. 3.
    Breaker RR. 2022.. The biochemical landscape of riboswitch ligands. . Biochemistry 61:(3):13749
    [Google Scholar]
  4. 4.
    Dykstra PB, Kaplan M, Smolke CD. 2022.. Engineering synthetic RNA devices for cell control. . Nat. Rev. Genet. 23:(4):21528
    [Google Scholar]
  5. 5.
    Townsend GE, Han W, Schwalm ND, Hong X, Bencivenga-Barry NA, et al. 2020.. A master regulator of Bacteroides thetaiotaomicron gut colonization controls carbohydrate utilization and an alternative protein synthesis factor. . mBio 11:(1):e0322119
    [Google Scholar]
  6. 6.
    Nahvi A, Sudarsan N, Ebert MS, Zou X, Brown KL, Breaker RR. 2002.. Genetic control by a metabolite binding mRNA. . Chem. Biol. 9:(9):104349
    [Google Scholar]
  7. 7.
    Zhou L-B, Zeng A-P. 2015.. Engineering a lysine-ON riboswitch for metabolic control of lysine production in Corynebacterium glutamicum. . ACS Synth. Biol. 4:(12):133540
    [Google Scholar]
  8. 8.
    Liu X, Xiong W, Qi Q, Zhang Y, Ji H, et al. 2022.. Rational guide RNA engineering for small-molecule control of CRISPR/Cas9 and gene editing. . Nucleic Acids Res. 50:(8):476983
    [Google Scholar]
  9. 9.
    Simmons TR, Ellington AD, Contreras LM. 2022.. RNP-based control systems for genetic circuits in synthetic biology beyond CRISPR. . Methods Mol. Biol. 2518::131
    [Google Scholar]
  10. 10.
    Chung HJ, Bang W, Drake MA. 2006.. Stress response of Escherichia coli. . Compr. Rev. Food Sci. Food Saf. 5:(3):5264
    [Google Scholar]
  11. 11.
    Fasnacht M, Polacek N. 2021.. Oxidative stress in bacteria and the central dogma of molecular biology. . Front. Mol. Biosci. 8::671037
    [Google Scholar]
  12. 12.
    Seixas AF, Quendera AP, Sousa JP, Silva AFQ, Arraiano CM, Andrade JM. 2021.. Bacterial response to oxidative stress and RNA oxidation. . Front. Genet. 12::821535
    [Google Scholar]
  13. 13.
    Seo SW, Kim D, Szubin R, Palsson BO. 2015.. Genome-wide reconstruction of OxyR and SoxRS transcriptional regulatory networks under oxidative stress in Escherichia coli K-12 MG1655. . Cell Rep. 12:(8):128999
    [Google Scholar]
  14. 14.
    Hartmann FSF, Clermont L, Tung QN, Antelmann H, Seibold GM. 2020.. The industrial organism Corynebacterium glutamicum requires mycothiol as antioxidant to resist against oxidative stress in bioreactor cultivations. . Antioxidants 9:(10):969
    [Google Scholar]
  15. 15.
    Sen A, Imlay JA. 2021.. How microbes defend themselves from incoming hydrogen peroxide. . Front. Immunol. 12::667343
    [Google Scholar]
  16. 16.
    Park J-B. 2003.. Phagocytosis induces superoxide formation and apoptosis in macrophages. . Exp. Mol. Med. 35:(5):32535
    [Google Scholar]
  17. 17.
    Krisko A, Radman M. 2013.. Biology of extreme radiation resistance: the way of Deinococcus radiodurans. . Cold Spring Harb. Perspect. Biol. 5:(7):a012765
    [Google Scholar]
  18. 18.
    Chevallier V, Andersen MR, Malphettes L. 2020.. Oxidative stress-alleviating strategies to improve recombinant protein production in CHO cells. . Biotechnol. Bioeng. 117:(4):117286
    [Google Scholar]
  19. 19.
    Moser F, Broers NJ, Hartmans S, Tamsir A, Kerkman R, et al. 2012.. Genetic circuit performance under conditions relevant for industrial bioreactors. . ACS Synth. Biol. 1:(11):55564
    [Google Scholar]
  20. 20.
    Imlay JA. 2019.. Where in the world do bacteria experience oxidative stress?. Environ. Microbiol. 21:(2):52130
    [Google Scholar]
  21. 21.
    Chen Y, Xue D, Sun W, Han J, Li J, et al. 2019.. sRNA OsiA stabilizes catalase mRNA during oxidative stress response of Deinococcus radiodurans R1. . Microorganisms 7:(10):422
    [Google Scholar]
  22. 22.
    Ezraty B, Gennaris A, Barras F, Collet J-F. 2017.. Oxidative stress, protein damage and repair in bacteria. . Nat. Rev. Microbiol. 15:(7):38596
    [Google Scholar]
  23. 23.
    Sies H, Jones DP. 2020.. Reactive oxygen species (ROS) as pleiotropic physiological signalling agents. . Nat. Rev. Mol. Cell Biol. 21:(7):36383
    [Google Scholar]
  24. 24.
    Ziegelhoffer EC, Donohue TJ. 2009.. Bacterial responses to photo-oxidative stress. . Nat. Rev. Microbiol. 7:(12):85663
    [Google Scholar]
  25. 25.
    Estevez M, Valesyan S, Jora M, Limbach PA, Addepalli B. 2021.. Oxidative damage to RNA is altered by the presence of interacting proteins or modified nucleosides. . Front. Mol. Biosci. 8::697149
    [Google Scholar]
  26. 26.
    Browning DF, Butala M, Busby SJW. 2019.. Bacterial transcription factors: regulation by pick “N” mix. . J. Mol. Biol. 431:(20):406777
    [Google Scholar]
  27. 27.
    Li Z, Malla S, Shin B, Li JM. 2014.. Battle against RNA oxidation: molecular mechanisms for reducing oxidized RNA to protect cells. . WIREs RNA 5:(3):33546
    [Google Scholar]
  28. 28.
    Imlay JA. 2015.. Diagnosing oxidative stress in bacteria: not as easy as you might think. . Curr. Opin. Microbiol. 24::12431
    [Google Scholar]
  29. 29.
    Chiang SM, Schellhorn HE. 2012.. Regulators of oxidative stress response genes in Escherichia coli and their functional conservation in bacteria. . Arch. Biochem. Biophys. 525:(2):16169
    [Google Scholar]
  30. 30.
    Kobayashi K, Fujikawa M, Kozawa T. 2014.. Oxidative stress sensing by the iron-sulfur cluster in the transcription factor, SoxR. . J. Inorg. Biochem. 133::8791
    [Google Scholar]
  31. 31.
    Imlay JA. 2013.. The molecular mechanisms and physiological consequences of oxidative stress: lessons from a model bacterium. . Nat. Rev. Microbiol. 11:(7):44354
    [Google Scholar]
  32. 32.
    Fillat MF. 2014.. The FUR (ferric uptake regulator) superfamily: diversity and versatility of key transcriptional regulators. . Arch. Biochem. Biophys. 546::4152
    [Google Scholar]
  33. 33.
    Imlay JA. 2015.. Transcription factors that defend bacteria against reactive oxygen species. . Annu. Rev. Microbiol. 69::93108
    [Google Scholar]
  34. 34.
    Seaver LC, Imlay JA. 2001.. Alkyl hydroperoxide reductase is the primary scavenger of endogenous hydrogen peroxide in Escherichia coli. . J. Bacteriol. 183:(24):717381
    [Google Scholar]
  35. 35.
    Storz G, Tartaglia LA. 1992.. OxyR: a regulator of antioxidant genes. . J. Nutr. 122:(3 Suppl.):62730
    [Google Scholar]
  36. 36.
    Wu H-J, Seib KL, Srikhanta YN, Edwards J, Kidd SP, et al. 2010.. Manganese regulation of virulence factors and oxidative stress resistance in Neisseria gonorrhoeae. . J. Proteom. 73:(5):899916
    [Google Scholar]
  37. 37.
    Schellhorn HE. 2020.. Function, evolution, and composition of the RpoS regulon in Escherichia coli. . Front. Microbiol. 11::560099
    [Google Scholar]
  38. 38.
    Fernández de Henestrosa AR, Ogi T, Aoyagi S, Chafin D, Hayes JJ, et al. 2000.. Identification of additional genes belonging to the LexA regulon in Escherichia coli. . Mol. Microbiol. 35:(6):156072
    [Google Scholar]
  39. 39.
    Kim SO, Merchant K, Nudelman R, Beyer WF, Keng T, et al. 2002.. OxyR: a molecular code for redox-related signaling. . Cell 109:(3):38396
    [Google Scholar]
  40. 40.
    Jo I, Chung I-Y, Bae H-W, Kim J-S, Song S, et al. 2015.. Structural details of the OxyR peroxide-sensing mechanism. . PNAS 112:(20):644348
    [Google Scholar]
  41. 41.
    McKernan LN. 2015.. Using a simple Escherichia coli growth curve model to teach the scientific method. . Am. Biol. Teach. 77:(5):35762
    [Google Scholar]
  42. 42.
    Zhang A, Wassarman KM, Ortega J, Steven AC, Storz G. 2002.. The Sm-like Hfq protein increases OxyS RNA interaction with target mRNAs. . Mol. Cell 9:(1):1122
    [Google Scholar]
  43. 43.
    Kavita K, de Mets F, Gottesman S. 2018.. New aspects of RNA-based regulation by Hfq and its partner sRNAs. . Curr. Opin. Microbiol. 42::5361
    [Google Scholar]
  44. 44.
    Duarte V, Latour J-M. 2010.. PerR versus OhrR: selective peroxide sensing in Bacillus subtilis. . Mol. Biosyst. 6:(2):31623
    [Google Scholar]
  45. 45.
    Lee J-W, Helmann JD. 2006.. The PerR transcription factor senses H2O2 by metal-catalysed histidine oxidation. . Nature 440:(7082):36367
    [Google Scholar]
  46. 46.
    Yin L, Wang L, Lu H, Xu G, Chen H, et al. 2010.. DRA0336, another OxyR homolog, involved in the antioxidation mechanisms in Deinococcus radiodurans. . J. Microbiol. 48:(4):47379
    [Google Scholar]
  47. 47.
    Jiang Y, Dong Y, Luo Q, Li N, Wu G, Gao H. 2014.. Protection from oxidative stress relies mainly on derepression of OxyR-dependent KatB and Dps in Shewanella oneidensis. . J. Bacteriol. 196:(2):44558
    [Google Scholar]
  48. 48.
    Xu L, Chen H, Hu X, Zhang R, Zhang Z, Luo ZW. 2006.. Average gene length is highly conserved in prokaryotes and eukaryotes and diverges only between the two kingdoms. . Mol. Biol. Evol. 23:(6):11078
    [Google Scholar]
  49. 49.
    Shepherd J, Ibba M. 2015.. Bacterial transfer RNAs. . FEMS Microbiol. Rev. 39:(3):280300
    [Google Scholar]
  50. 50.
    Melnikov S, Ben-Shem A, Garreau de Loubresse N, Jenner L, Yusupova G, Yusupov M. 2012.. One core, two shells: bacterial and eukaryotic ribosomes. . Nat. Struct. Mol. Biol. 19:(6):56067
    [Google Scholar]
  51. 51.
    Cao Y, Wu J, Liu Q, Zhao Y, Ying X, et al. 2010.. sRNATarBase: a comprehensive database of bacterial sRNA targets verified by experiments. . RNA 16:(11):205157
    [Google Scholar]
  52. 52.
    Radak Z, Boldogh I. 2010.. 8-Oxo-7,8-dihydroguanine: links to gene expression, aging, and defense against oxidative stress. . Free Radic. Biol. Med. 49:(4):58796
    [Google Scholar]
  53. 53.
    Shcherbik N, Pestov DG. 2019.. The impact of oxidative stress on ribosomes: from injury to regulation. . Cells 8:(11):1379
    [Google Scholar]
  54. 54.
    Tsai C-H, Liao R, Chou B, Contreras LM. 2015.. Transcriptional analysis of Deinococcus radiodurans reveals novel small RNAs that are differentially expressed under ionizing radiation. . Appl. Environ. Microbiol. 81:(5):175464
    [Google Scholar]
  55. 55.
    Villa JK, Amador P, Janovsky J, Bhuyan A, Saldanha R, et al. 2017.. A genome-wide search for ionizing-radiation-responsive elements in Deinococcus radiodurans reveals a regulatory role for the DNA gyrase subunit A gene's 5′ untranslated region in the radiation and desiccation response. . Appl. Environ. Microbiol. 83:(12):e0003917
    [Google Scholar]
  56. 56.
    Simms CL, Zaher HS. 2016.. Quality control of chemically damaged RNA. . Cell. Mol. Life Sci. 73:(19):363953
    [Google Scholar]
  57. 57.
    Yan LL, Zaher HS. 2019.. How do cells cope with RNA damage and its consequences?. J. Biol. Chem. 294:(41):1515871
    [Google Scholar]
  58. 58.
    da Cruz Nizer WS, Inkovskiy V, Versey Z, Strempel N, Cassol E, Overhage J. 2021.. Oxidative stress response in Pseudomonas aeruginosa. . Pathogens 10:(9):1187
    [Google Scholar]
  59. 59.
    Zhong J, Xiao C, Gu W, Du G, Sun X, et al. 2015.. Transfer RNAs mediate the rapid adaptation of Escherichia coli to oxidative stress. . PLOS Genet. 11:(6):e1005302
    [Google Scholar]
  60. 60.
    Leiva LE, Pincheira A, Elgamal S, Kienast SD, Bravo V, et al. 2020.. Modulation of Escherichia coli translation by the specific inactivation of tRNAGly under oxidative stress. . Front. Genet. 11::856
    [Google Scholar]
  61. 61.
    Svenningsen SL, Kongstad M, Stenum TS, Muñoz-Gómez AJ, Sørensen MA. 2017.. Transfer RNA is highly unstable during early amino acid starvation in Escherichia coli. . Nucleic Acids Res. 45:(2):793804
    [Google Scholar]
  62. 62.
    Zhu M, Dai X. 2019.. Maintenance of translational elongation rate underlies the survival of Escherichia coli during oxidative stress. . Nucleic Acids Res. 47:(14):7592604
    [Google Scholar]
  63. 63.
    Czech A, Wende S, Mörl M, Pan T, Ignatova Z. 2013.. Reversible and rapid transfer-RNA deactivation as a mechanism of translational repression in stress. . PLOS Genet. 9:(8):e1003767
    [Google Scholar]
  64. 64.
    Megel C, Morelle G, Lalande S, Duchêne A-M, Small I, Maréchal-Drouard L. 2015.. Surveillance and cleavage of eukaryotic tRNAs. . Int. J. Mol. Sci. 16:(1):187393
    [Google Scholar]
  65. 65.
    Li Z, Stanton BA. 2021.. Transfer RNA-derived fragments, the underappreciated regulatory small RNAs in microbial pathogenesis. . Front. Microbiol. 12::687632
    [Google Scholar]
  66. 66.
    Kaczanowska M, Rydén-Aulin M. 2007.. Ribosome biogenesis and the translation process in Escherichia coli. . Microbiol. Mol. Biol. Rev. 71:(3):47794
    [Google Scholar]
  67. 67.
    Willi J, Küpfer P, Evéquoz D, Fernandez G, Katz A, et al. 2018.. Oxidative stress damages rRNA inside the ribosome and differentially affects the catalytic center. . Nucleic Acids Res. 46:(4):194557
    [Google Scholar]
  68. 68.
    Simms CL, Hudson BH, Mosior JW, Rangwala AS, Zaher HS. 2014.. An active role for the ribosome in determining the fate of oxidized mRNA. . Cell Rep. 9:(4):125664
    [Google Scholar]
  69. 69.
    Liu M, Gong X, Alluri RK, Wu J, Sablo T, Li Z. 2012.. Characterization of RNA damage under oxidative stress in Escherichia coli. . Biol. Chem. 393:(3):12332
    [Google Scholar]
  70. 70.
    Wang J-X, Gao J, Ding S-L, Wang K, Jiao J-Q, et al. 2015.. Oxidative modification of miR-184 enables it to target Bcl-xL and Bcl-w. . Mol. Cell 59:(1):5061
    [Google Scholar]
  71. 71.
    Shan X, Tashiro H, Lin CG. 2003.. The identification and characterization of oxidized RNAs in Alzheimer's disease. . J. Neurosci. 23:(12):491321
    [Google Scholar]
  72. 72.
    Gonzalez-Rivera JC, Sherman MW, Wang DS, Chuvalo-Abraham JCL, Hildebrandt Ruiz L, Contreras LM. 2020.. RNA oxidation in chromatin modification and DNA-damage response following exposure to formaldehyde. . Sci. Rep. 10::16545
    [Google Scholar]
  73. 73.
    Thomas EN, Simms CL, Keedy HE, Zaher HS. 2019.. Insights into the base-pairing preferences of 8-oxoguanosine on the ribosome. . Nucleic Acids Res. 47:(18):985770
    [Google Scholar]
  74. 74.
    Wu J, Jiang Z, Liu M, Gong X, Wu S, et al. 2009.. Polynucleotide phosphorylase protects Escherichia coli against oxidative stress. . Biochemistry 48:(9):201220
    [Google Scholar]
  75. 75.
    Becket E, Tse L, Yung M, Cosico A, Miller JH. 2012.. Polynucleotide phosphorylase plays an important role in the generation of spontaneous mutations in Escherichia coli. . J. Bacteriol. 194:(20):561320
    [Google Scholar]
  76. 76.
    Jones GH. 2018.. Novel aspects of polynucleotide phosphorylase function in Streptomyces. . Antibiotics 7:(1):E25
    [Google Scholar]
  77. 77.
    Briani F, Carzaniga T, Dehò G. 2016.. Regulation and functions of bacterial PNPase. . WIREs RNA 7:(2):24158
    [Google Scholar]
  78. 78.
    Han R, Jiang J, Fang J, Contreras LM. 2022.. PNPase and RhlB interact and reduce the cellular availability of oxidized RNA in Deinococcus radiodurans. . Microbiol. Spectr. 10:(4):e0214022
    [Google Scholar]
  79. 79.
    Hayakawa H, Uchiumi T, Fukuda T, Ashizuka M, Kohno K, et al. 2002.. Binding capacity of human YB-1 protein for RNA containing 8-oxoguanine. . Biochemistry 41:(42):1273944
    [Google Scholar]
  80. 80.
    Taddei F, Hayakawa H, Bouton M, Cirinesi A, Matic I, et al. 1997.. Counteraction by MutT protein of transcriptional errors caused by oxidative damage. . Science 278:(5335):12830
    [Google Scholar]
  81. 81.
    Setoyama D, Ito R, Takagi Y, Sekiguchi M. 2011.. Molecular actions of Escherichia coli MutT for control of spontaneous mutagenesis. . Mutat. Res. 707:(1–2):914
    [Google Scholar]
  82. 82.
    Sekiguchi T, Ito R, Hayakawa H, Sekiguchi M. 2013.. Elimination and utilization of oxidized guanine nucleotides in the synthesis of RNA and its precursors. . J. Biol. Chem. 288:(12):812835
    [Google Scholar]
  83. 83.
    Hamal Dhakal S, Panchapakesan SSS, Slattery P, Roth A, Breaker RR. 2022.. Variants of the guanine riboswitch class exhibit altered ligand specificities for xanthine, guanine, or 2′-deoxyguanosine. . PNAS 119:(22):e2120246119
    [Google Scholar]
  84. 84.
    Villa JK, Su Y, Contreras LM, Hammond MC. 2018.. Synthetic biology of small RNAs and riboswitches. . Microbiol. Spectr. 6:(3):7
    [Google Scholar]
  85. 85.
    Sharma A, Alajangi HK, Pisignano G, Sood V, Singh G, Barnwal RP. 2022.. RNA thermometers and other regulatory elements: diversity and importance in bacterial pathogenesis. . WIREs RNA 13:(5):e1711
    [Google Scholar]
  86. 86.
    Kiggins C, Skinner A, Resendiz MJE. 2020.. 7:, 8-Dihydro-8-oxoguanosine lesions inhibit the theophylline aptamer or change its selectivity. . ChemBioChem 21:(9):134755
    [Google Scholar]
  87. 87.
    Samuelian JS, Gremminger TJ, Song Z, Poudyal RR, Li J, et al. 2022.. An RNA aptamer that shifts the reduction potential of metabolic cofactors. . Nat. Chem. Biol. 18::126369
    [Google Scholar]
  88. 88.
    Ariza-Mateos A, Prieto-Vega S, Díaz-Toledano R, Birk A, Szeto H, et al. 2012.. RNA self-cleavage activated by ultraviolet light-induced oxidation. . Nucleic Acids Res. 40:(4):174866
    [Google Scholar]
  89. 89.
    Schmidt CM, Smolke CD. 2019.. RNA switches for synthetic biology. . Cold Spring Harb. Perspect. Biol. 11:(1):a032532
    [Google Scholar]
  90. 90.
    Zinskie JA, Ghosh A, Trainor BM, Shedlovskiy D, Pestov DG, Shcherbik N. 2018.. Iron-dependent cleavage of ribosomal RNA during oxidative stress in the yeast Saccharomyces cerevisiae. . J. Biol. Chem. 293:(37):1423748
    [Google Scholar]
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