1887
No metrics data to plot.
The attempt to load metrics for this article has failed.
The attempt to plot a graph for these metrics has failed.

RNA Localization in Bacteria

MyBook is a cheap paperback edition of the original book and will be sold at uniform, low price.
Buy this Microbiology Spectrum Article
Price Non-Member $15.00
  • Authors: Jingyi Fei1, Cynthia M. Sharma2
  • Editors: Gisela Storz3, Kai Papenfort4
  • VIEW AFFILIATIONS HIDE AFFILIATIONS
    Affiliations: 1: Department of Biochemistry and Molecular Biology, Institute for Biophysical Dynamics, The University of Chicago, Chicago, IL 60637; 2: Chair of Molecular Infection Biology II, Institute of Molecular Infection Biology (IMIB), University of Würzburg, 97080 Würzburg, Germany; 3: Division of Molecular and Cellular Biology, Eunice Kennedy Shriver National Institute of Child Health and Human Development, Bethesda, MD; 4: Department of Biology I, Microbiology, LMU Munich, Martinsried, Germany
  • Source: microbiolspec September 2018 vol. 6 no. 5 doi:10.1128/microbiolspec.RWR-0024-2018
  • Received 24 January 2018 Accepted 27 July 2018 Published 07 September 2018
  • Jingyi Fei, [email protected]; Cynthia M. Sharma, [email protected]
image of RNA Localization in Bacteria
    Preview this microbiology spectrum article:
    Zoom in
    Zoomout

    RNA Localization in Bacteria, Page 1 of 2

    | /docserver/preview/fulltext/microbiolspec/6/5/RWR-0024-2018-1.gif /docserver/preview/fulltext/microbiolspec/6/5/RWR-0024-2018-2.gif
  • Abstract:

    Diverse mechanisms and functions of posttranscriptional regulation by small regulatory RNAs and RNA-binding proteins have been described in bacteria. In contrast, little is known about the spatial organization of RNAs in bacterial cells. In eukaryotes, subcellular localization and transport of RNAs play important roles in diverse physiological processes, such as embryonic patterning, asymmetric cell division, epithelial polarity, and neuronal plasticity. It is now clear that bacterial RNAs also can accumulate at distinct sites in the cell. However, due to the small size of bacterial cells, RNA localization and localization-associated functions are more challenging to study in bacterial cells, and the underlying molecular mechanisms of transcript localization are less understood. Here, we review the emerging examples of RNAs localized to specific subcellular locations in bacteria, with indications that subcellular localization of transcripts might be important for gene expression and regulatory processes. Diverse mechanisms for bacterial RNA localization have been suggested, including close association to their genomic site of transcription, or to the localizations of their protein products in translation-dependent or -independent processes. We also provide an overview of the state of the art of technologies to visualize and track bacterial RNAs, ranging from hybridization-based approaches in fixed cells to imaging approaches using fluorescent protein reporters and/or RNA aptamers in single living bacterial cells. We conclude with a discussion of open questions in the field and ongoing technological developments regarding RNA imaging in eukaryotic systems that might likewise provide novel insights into RNA localization in bacteria.

  • Citation: Fei J, Sharma C. 2018. RNA Localization in Bacteria. Microbiol Spectrum 6(5):RWR-0024-2018. doi:10.1128/microbiolspec.RWR-0024-2018.

References

1. Chin A, Lécuyer E. 2017. RNA localization: making its way to the center stage. Biochim Biophys Acta 1861(11 Pt B):2956–2970. http://dx.doi.org/10.1016/j.bbagen.2017.06.011. [PubMed]
2. Buxbaum AR, Haimovich G, Singer RH. 2015. In the right place at the right time: visualizing and understanding mRNA localization. Nat Rev Mol Cell Biol 16:95–109. http://dx.doi.org/10.1038/nrm3918.
3. Mofatteh M, Bullock SL. 2017. SnapShot: subcellular mRNA localization. Cell 169:178–178.e1. http://dx.doi.org/10.1016/j.cell.2017.03.004. [PubMed]
4. Jung H, Gkogkas CG, Sonenberg N, Holt CE. 2014. Remote control of gene function by local translation. Cell 157:26–40. http://dx.doi.org/10.1016/j.cell.2014.03.005. [PubMed]
5. Govindarajan S, Nevo-Dinur K, Amster-Choder O. 2012. Compartmentalization and spatiotemporal organization of macromolecules in bacteria. FEMS Microbiol Rev 36:1005–1022. http://dx.doi.org/10.1111/j.1574-6976.2012.00348.x. [PubMed]
6. Nevo-Dinur K, Govindarajan S, Amster-Choder O. 2012. Subcellular localization of RNA and proteins in prokaryotes. Trends Genet 28:314–322. http://dx.doi.org/10.1016/j.tig.2012.03.008. [PubMed]
7. Campos M, Jacobs-Wagner C. 2013. Cellular organization of the transfer of genetic information. Curr Opin Microbiol 16:171–176. http://dx.doi.org/10.1016/j.mib.2013.01.007. [PubMed]
8. Keiler KC. 2011. RNA localization in bacteria. Curr Opin Microbiol 14:155–159. http://dx.doi.org/10.1016/j.mib.2011.01.009. [PubMed]
9. Buskila AA, Kannaiah S, Amster-Choder O. 2014. RNA localization in bacteria. RNA Biol 11:1051–1060. http://dx.doi.org/10.4161/rna.36135. [PubMed]
10. Kannaiah S, Amster-Choder O. 2014. Protein targeting via mRNA in bacteria. Biochim Biophys Acta 1843:1457–1465. http://dx.doi.org/10.1016/j.bbamcr.2013.11.004. [PubMed]
11. Storz G, Vogel J, Wassarman KM. 2011. Regulation by small RNAs in bacteria: expanding frontiers. Mol Cell 43:880–891. http://dx.doi.org/10.1016/j.molcel.2011.08.022. [PubMed]
12. Vogel J, Luisi BF. 2011. Hfq and its constellation of RNA. Nat Rev Microbiol 9:578–589. http://dx.doi.org/10.1038/nrmicro2615. [PubMed]
13. McLean R, Inglis GD, Mosimann SC, Uwiera RR, Abbott DW. 2017. Determining the localization of carbohydrate active enzymes within gram-negative bacteria. Methods Mol Biol 1588:199–208. http://dx.doi.org/10.1007/978-1-4939-6899-2_15. [PubMed]
14. Fontaine F, Fuchs RT, Storz G. 2011. Membrane localization of small proteins in Escherichia coli. J Biol Chem 286:32464–32474. http://dx.doi.org/10.1074/jbc.M111.245696. [PubMed]
15. Benhalevy D, Biran I, Bochkareva ES, Sorek R, Bibi E. 2017. Evidence for a cytoplasmic pool of ribosome-free mRNAs encoding inner membrane proteins in Escherichia coli. PLoS One 12:e0183862. http://dx.doi.org/10.1371/journal.pone.0183862. [PubMed]
16. Milne JLS, Subramaniam S. 2009. Cryo-electron tomography of bacteria: progress, challenges and future prospects. Nat Rev Microbiol 7:666–675. http://dx.doi.org/10.1038/nrmicro2183. [PubMed]
17. Chakraborty K, Veetil AT, Jaffrey SR, Krishnan Y. 2016. Nucleic acid-based nanodevices in biological imaging. Annu Rev Biochem 85:349–373. http://dx.doi.org/10.1146/annurev-biochem-060815-014244. [PubMed]
18. van Gijtenbeek LA, Kok J. 2017. Illuminating messengers: an update and outlook on RNA visualization in bacteria. Front Microbiol 8:1161. http://dx.doi.org/10.3389/fmicb.2017.01161. [PubMed]
19. Femino AM, Fay FS, Fogarty K, Singer RH. 1998. Visualization of single RNA transcripts in situ. Science 280:585–590. http://dx.doi.org/10.1126/science.280.5363.585. [PubMed]
20. So LH, Ghosh A, Zong C, Sepúlveda LA, Segev R, Golding I. 2011. General properties of transcriptional time series in Escherichia coli. Nat Genet 43:554–560. http://dx.doi.org/10.1038/ng.821. [PubMed]
21. Raj A, van den Bogaard P, Rifkin SA, van Oudenaarden A, Tyagi S. 2008. Imaging individual mRNA molecules using multiple singly labeled probes. Nat Methods 5:877–879. http://dx.doi.org/10.1038/nmeth.1253. [PubMed]
22. Raj A, Peskin CS, Tranchina D, Vargas DY, Tyagi S. 2006. Stochastic mRNA synthesis in mammalian cells. PLoS Biol 4:e309. http://dx.doi.org/10.1371/journal.pbio.0040309. [PubMed]
23. Neuert G, Munsky B, Tan RZ, Teytelman L, Khammash M, van Oudenaarden A. 2013. Systematic identification of signal-activated stochastic gene regulation. Science 339:584–587. http://dx.doi.org/10.1126/science.1231456. [PubMed]
24. Jones DL, Brewster RC, Phillips R. 2014. Promoter architecture dictates cell-to-cell variability in gene expression. Science 346:1533–1536. http://dx.doi.org/10.1126/science.1255301. [PubMed]
25. Schnell U, Dijk F, Sjollema KA, Giepmans BN. 2012. Immunolabeling artifacts and the need for live-cell imaging. Nat Methods 9:152–158. http://dx.doi.org/10.1038/nmeth.1855. [PubMed]
26. Bertrand E, Chartrand P, Schaefer M, Shenoy SM, Singer RH, Long RM. 1998. Localization of ASH1 mRNA particles in living yeast. Mol Cell 2:437–445. http://dx.doi.org/10.1016/S1097-2765(00)80143-4.
27. Lange S, Katayama Y, Schmid M, Burkacky O, Bräuchle C, Lamb DC, Jansen RP. 2008. Simultaneous transport of different localized mRNA species revealed by live-cell imaging. Traffic 9:1256–1267. http://dx.doi.org/10.1111/j.1600-0854.2008.00763.x. [PubMed]
28. Hocine S, Raymond P, Zenklusen D, Chao JA, Singer RH. 2013. Single-molecule analysis of gene expression using two-color RNA labeling in live yeast. Nat Methods 10:119–121. http://dx.doi.org/10.1038/nmeth.2305. [PubMed]
29. Miller LW, Cai Y, Sheetz MP, Cornish VW. 2005. In vivo protein labeling with trimethoprim conjugates: a flexible chemical tag. Nat Methods 2:255–257. http://dx.doi.org/10.1038/nmeth749. [PubMed]
30. Keppler A, Gendreizig S, Gronemeyer T, Pick H, Vogel H, Johnsson K. 2003. A general method for the covalent labeling of fusion proteins with small molecules in vivo. Nat Biotechnol 21:86–89. http://dx.doi.org/10.1038/nbt765. [PubMed]
31. Sun X, Zhang A, Baker B, Sun L, Howard A, Buswell J, Maurel D, Masharina A, Johnsson K, Noren CJ, Xu MQ, Corrêa IR Jr. 2011. Development of SNAP-tag fluorogenic probes for wash-free fluorescence imaging. Chembiochem 12:2217–2226. http://dx.doi.org/10.1002/cbic.201100173. [PubMed]
32. Carrocci TJ, Hoskins AA. 2014. Imaging of RNAs in live cells with spectrally diverse small molecule fluorophores. Analyst (Lond) 139:44–47. http://dx.doi.org/10.1039/C3AN01550E. [PubMed]
33. Valencia-Burton M, McCullough RM, Cantor CR, Broude NE. 2007. RNA visualization in live bacterial cells using fluorescent protein complementation. Nat Methods 4:421–427.
34. Valencia-Burton M, Shah A, Sutin J, Borogovac A, McCullough RM, Cantor CR, Meller A, Broude NE. 2009. Spatiotemporal patterns and transcription kinetics of induced RNA in single bacterial cells. Proc Natl Acad Sci U S A 106:16399–16404. http://dx.doi.org/10.1073/pnas.0907495106. [PubMed]
35. Ozawa T, Natori Y, Sato M, Umezawa Y. 2007. Imaging dynamics of endogenous mitochondrial RNA in single living cells. Nat Methods 4:413–419.
36. Wu B, Chen J, Singer RH. 2014. Background free imaging of single mRNAs in live cells using split fluorescent proteins. Sci Rep 4:3615. http://dx.doi.org/10.1038/srep03615. [PubMed]
37. Wang S, Moffitt JR, Dempsey GT, Xie XS, Zhuang X. 2014. Characterization and development of photoactivatable fluorescent proteins for single-molecule-based superresolution imaging. Proc Natl Acad Sci U S A 111:8452–8457. http://dx.doi.org/10.1073/pnas.1406593111. [PubMed]
38. Landgraf D, Okumus B, Chien P, Baker TA, Paulsson J. 2012. Segregation of molecules at cell division reveals native protein localization. Nat Methods 9:480–482. http://dx.doi.org/10.1038/nmeth.1955. [PubMed]
39. LeCuyer KA, Behlen LS, Uhlenbeck OC. 1995. Mutants of the bacteriophage MS2 coat protein that alter its cooperative binding to RNA. Biochemistry 34:10600–10606. http://dx.doi.org/10.1021/bi00033a035. [PubMed]
40. Golding I, Paulsson J, Zawilski SM, Cox EC. 2005. Real-time kinetics of gene activity in individual bacteria. Cell 123:1025–1036. http://dx.doi.org/10.1016/j.cell.2005.09.031. [PubMed]
41. Haimovich G, Zabezhinsky D, Haas B, Slobodin B, Purushothaman P, Fan L, Levin JZ, Nusbaum C, Gerst JE. 2016. Use of the MS2 aptamer and coat protein for RNA localization in yeast: a response to “MS2 coat proteins bound to yeast mRNAs block 5′ to 3′ degradation and trap mRNA decay products: implications for the localization of mRNAs by MS2-MCP system.” RNA 22:660–666. http://dx.doi.org/10.1261/rna.055095.115. [PubMed]
42. Garcia JF, Parker R. 2015. MS2 coat proteins bound to yeast mRNAs block 5′ to 3′ degradation and trap mRNA decay products: implications for the localization of mRNAs by MS2-MCP system. RNA 21:1393–1395. http://dx.doi.org/10.1261/rna.051797.115. [PubMed]
43. Heinrich S, Sidler CL, Azzalin CM, Weis K. 2017. Stem-loop RNA labeling can affect nuclear and cytoplasmic mRNA processing. RNA 23:134–141. http://dx.doi.org/10.1261/rna.057786.116. [PubMed]
44. Garcia JF, Parker R. 2016. Ubiquitous accumulation of 3′ mRNA decay fragments in Saccharomyces cerevisiae mRNAs with chromosomally integrated MS2 arrays. RNA 22:657–659. http://dx.doi.org/10.1261/rna.056325.116. [PubMed]
45. Tutucci E, Vera M, Biswas J, Garcia J, Parker R, Singer RH. 2018. An improved MS2 system for accurate reporting of the mRNA life cycle. Nat Methods 15:81–89. http://dx.doi.org/10.1038/nmeth.4502. [PubMed]
46. You M, Jaffrey SR. 2015. Structure and mechanism of RNA mimics of green fluorescent protein. Annu Rev Biophys 44:187–206. http://dx.doi.org/10.1146/annurev-biophys-060414-033954. [PubMed]
47. Ouellet J. 2016. RNA fluorescence with light-up aptamers. Front Chem 4:29. http://dx.doi.org/10.3389/fchem.2016.00029. [PubMed]
48. Dolgosheina EV, Unrau PJ. 2016. Fluorophore-binding RNA aptamers and their applications. Wiley Interdiscip Rev RNA 7:843–851. http://dx.doi.org/10.1002/wrna.1383. [PubMed]
49. Babendure JR, Adams SR, Tsien RY. 2003. Aptamers switch on fluorescence of triphenylmethane dyes. J Am Chem Soc 125:14716–14717. http://dx.doi.org/10.1021/ja037994o. [PubMed]
50. Constantin TP, Silva GL, Robertson KL, Hamilton TP, Fague K, Waggoner AS, Armitage BA. 2008. Synthesis of new fluorogenic cyanine dyes and incorporation into RNA fluoromodules. Org Lett 10:1561–1564. http://dx.doi.org/10.1021/ol702920e. [PubMed]
51. Sando S, Narita A, Hayami M, Aoyama Y. 2008. Transcription monitoring using fused RNA with a dye-binding light-up aptamer as a tag: a blue fluorescent RNA. Chem Commun (Camb) (33):3858–3860. http://dx.doi.org/10.1039/b808449a. [PubMed]
52. Paige JS, Wu KY, Jaffrey SR. 2011. RNA mimics of green fluorescent protein. Science 333:642–646. http://dx.doi.org/10.1126/science.1207339. [PubMed]
53. Strack RL, Disney MD, Jaffrey SR. 2013. A superfolding Spinach2 reveals the dynamic nature of trinucleotide repeat-containing RNA. Nat Methods 10:1219–1224. http://dx.doi.org/10.1038/nmeth.2701. [PubMed]
54. Dolgosheina EV, Jeng SC, Panchapakesan SS, Cojocaru R, Chen PS, Wilson PD, Hawkins N, Wiggins PA, Unrau PJ. 2014. RNA Mango aptamer-fluorophore: a bright, high-affinity complex for RNA labeling and tracking. ACS Chem Biol 9:2412–2420. http://dx.doi.org/10.1021/cb500499x. [PubMed]
55. Filonov GS, Moon JD, Svensen N, Jaffrey SR. 2014. Broccoli: rapid selection of an RNA mimic of green fluorescent protein by fluorescence-based selection and directed evolution. J Am Chem Soc 136:16299–16308. http://dx.doi.org/10.1021/ja508478x. [PubMed]
56. Filonov GS, Jaffrey SR. 2016. RNA imaging with dimeric Broccoli in live bacterial and mammalian cells. Curr Protoc Chem Biol 8:1–28.
57. Warner KD, Sjekloća L, Song W, Filonov GS, Jaffrey SR, Ferré-D’Amaré AR. 2017. A homodimer interface without base pairs in an RNA mimic of red fluorescent protein. Nat Chem Biol 13:1195–1201. http://dx.doi.org/10.1038/nchembio.2475. [PubMed]
58. Zhang J, Fei J, Leslie BJ, Han KY, Kuhlman TE, Ha T. 2015. Tandem Spinach array for mRNA imaging in living bacterial cells. Sci Rep 5:17295. http://dx.doi.org/10.1038/srep17295. [PubMed]
59. Sunbul M, Jäschke A. 2013. Contact-mediated quenching for RNA imaging in bacteria with a fluorophore-binding aptamer. Angew Chem Int Ed Engl 52:13401–13404. http://dx.doi.org/10.1002/anie.201306622. [PubMed]
60. Arora A, Sunbul M, Jäschke A. 2015. Dual-colour imaging of RNAs using quencher- and fluorophore-binding aptamers. Nucleic Acids Res 43:e144.
61. Betzig E, Patterson GH, Sougrat R, Lindwasser OW, Olenych S, Bonifacino JS, Davidson MW, Lippincott-Schwartz J, Hess HF. 2006. Imaging intracellular fluorescent proteins at nanometer resolution. Science 313:1642–1645. http://dx.doi.org/10.1126/science.1127344. [PubMed]
62. Rust MJ, Bates M, Zhuang X. 2006. Sub-diffraction-limit imaging by stochastic optical reconstruction microscopy (STORM). Nat Methods 3:793–795. http://dx.doi.org/10.1038/nmeth929. [PubMed]
63. Huang B, Wang W, Bates M, Zhuang X. 2008. Three-dimensional super-resolution imaging by stochastic optical reconstruction microscopy. Science 319:810–813. http://dx.doi.org/10.1126/science.1153529. [PubMed]
64. Montero Llopis P, Jackson AF, Sliusarenko O, Surovtsev I, Heinritz J, Emonet T, Jacobs-Wagner C. 2010. Spatial organization of the flow of genetic information in bacteria. Nature 466:77–81. http://dx.doi.org/10.1038/nature09152. [PubMed]
65. Nevo-Dinur K, Nussbaum-Shochat A, Ben-Yehuda S, Amster-Choder O. 2011. Translation-independent localization of mRNA in E. coli. Science 331:1081–1084. http://dx.doi.org/10.1126/science.1195691.
66. dos Santos VT, Bisson-Filho AW, Gueiros-Filho FJ. 2012. DivIVA-mediated polar localization of ComN, a posttranscriptional regulator of Bacillus subtilis. J Bacteriol 194:3661–3669. http://dx.doi.org/10.1128/JB.05879-11. [PubMed]
67. Golding I, Cox EC. 2004. RNA dynamics in live Escherichia coli cells. Proc Natl Acad Sci U S A 101:11310–11315. http://dx.doi.org/10.1073/pnas.0404443101. [PubMed]
68. Toran P, Smolina I, Driscoll H, Ding F, Sun Y, Cantor CR, Broude NE. 2014. Labeling native bacterial RNA in live cells. Cell Res 24:894–897. http://dx.doi.org/10.1038/cr.2014.47. [PubMed]
69. Pilhofer M, Pavlekovic M, Lee NM, Ludwig W, Schleifer KH. 2009. Fluorescence in situ hybridization for intracellular localization of nifH mRNA. Syst Appl Microbiol 32:186–192. http://dx.doi.org/10.1016/j.syapm.2008.12.007. [PubMed]
70. Moffitt JR, Pandey S, Boettiger AN, Wang S, Zhuang X. 2016. Spatial organization shapes the turnover of a bacterial transcriptome. Elife 5:313065. http://dx.doi.org/10.7554/eLife.13065. [PubMed]
71. Dugar G, Svensson SL, Bischler T, Wäldchen S, Reinhardt R, Sauer M, Sharma CM. 2016. The CsrA-FliW network controls polar localization of the dual-function flagellin mRNA in Campylobacter jejuni. Nat Commun 7:11667. http://dx.doi.org/10.1038/ncomms11667. [PubMed]
72. Sorg JA, Miller NC, Schneewind O. 2005. Substrate recognition of type III secretion machines—testing the RNA signal hypothesis. Cell Microbiol 7:1217–1225. http://dx.doi.org/10.1111/j.1462-5822.2005.00563.x. [PubMed]
73. Anderson DM, Schneewind O. 1997. A mRNA signal for the type III secretion of Yop proteins by Yersinia enterocolitica. Science 278:1140–1143. http://dx.doi.org/10.1126/science.278.5340.1140.
74. Singer HM, Erhardt M, Hughes KT. 2014. Comparative analysis of the secretion capability of early and late flagellar type III secretion substrates. Mol Microbiol 93:505–520. http://dx.doi.org/10.1111/mmi.12675. [PubMed]
75. Majander K, Anton L, Antikainen J, Lång H, Brummer M, Korhonen TK, Westerlund-Wikström B. 2005. Extracellular secretion of polypeptides using a modified Escherichia coli flagellar secretion apparatus. Nat Biotechnol 23:475–481. http://dx.doi.org/10.1038/nbt1077. [PubMed]
76. Driessen AJ, Nouwen N. 2008. Protein translocation across the bacterial cytoplasmic membrane. Annu Rev Biochem 77:643–667. http://dx.doi.org/10.1146/annurev.biochem.77.061606.160747. [PubMed]
77. Korkmazhan E, Teimouri H, Peterman N, Levine E. 2017. Dynamics of translation can determine the spatial organization of membrane-bound proteins and their mRNA. Proc Natl Acad Sci U S A 114:13424–13429. http://dx.doi.org/10.1073/pnas.1700941114. [PubMed]
78. Anderson DM, Schneewind O. 1999. Yersinia enterocolitica type III secretion: an mRNA signal that couples translation and secretion of YopQ. Mol Microbiol 31:1139–1148. http://dx.doi.org/10.1046/j.1365-2958.1999.01254.x.
79. Azam TA, Hiraga S, Ishihama A. 2000. Two types of localization of the DNA-binding proteins within the Escherichia coli nucleoid. Genes Cells 5:613–626. http://dx.doi.org/10.1046/j.1365-2443.2000.00350.x. [PubMed]
80. Müller A, Beeby M, McDowall AW, Chow J, Jensen GJ, Clemons WM Jr. 2014. Ultrastructure and complex polar architecture of the human pathogen Campylobacter jejuni. MicrobiologyOpen 3:702–710. http://dx.doi.org/10.1002/mbo3.200. [PubMed]
81. Sanamrad A, Persson F, Lundius EG, Fange D, Gynnå AH, Elf J. 2014. Single-particle tracking reveals that free ribosomal subunits are not excluded from the Escherichia coli nucleoid. Proc Natl Acad Sci U S A 111:11413–11418. http://dx.doi.org/10.1073/pnas.1411558111. [PubMed]
82. Lewis PJ, Thaker SD, Errington J. 2000. Compartmentalization of transcription and translation in Bacillus subtilis. EMBO J 19:710–718. http://dx.doi.org/10.1093/emboj/19.4.710. [PubMed]
83. Ortiz JO, Förster F, Kürner J, Linaroudis AA, Baumeister W. 2006. Mapping 70S ribosomes in intact cells by cryoelectron tomography and pattern recognition. J Struct Biol 156:334–341. http://dx.doi.org/10.1016/j.jsb.2006.04.014. [PubMed]
84. Bakshi S, Choi H, Weisshaar JC. 2015. The spatial biology of transcription and translation in rapidly growing Escherichia coli. Front Microbiol 6:636. http://dx.doi.org/10.3389/fmicb.2015.00636. [PubMed]
85. Mascarenhas J, Weber MH, Graumann PL. 2001. Specific polar localization of ribosomes in Bacillus subtilis depends on active transcription. EMBO Rep 2:685–689. http://dx.doi.org/10.1093/embo-reports/kve160. [PubMed]
86. Keiler KC. 2011. Localization of the bacterial RNA infrastructure. Adv Exp Med Biol 722:231–238. http://dx.doi.org/10.1007/978-1-4614-0332-6_15. [PubMed]
87. Stracy M, Lesterlin C, Garza de Leon F, Uphoff S, Zawadzki P, Kapanidis AN. 2015. Live-cell superresolution microscopy reveals the organization of RNA polymerase in the bacterial nucleoid. Proc Natl Acad Sci U S A 112:E4390–E4399. http://dx.doi.org/10.1073/pnas.1507592112. [PubMed]
88. Chai Q, Singh B, Peisker K, Metzendorf N, Ge X, Dasgupta S, Sanyal S. 2014. Organization of ribosomes and nucleoids in Escherichia coli cells during growth and in quiescence. J Biol Chem 289:11342–11352. http://dx.doi.org/10.1074/jbc.M114.557348. [PubMed]
89. Herskovits AA, Bibi E. 2000. Association of Escherichia coli ribosomes with the inner membrane requires the signal recognition particle receptor but is independent of the signal recognition particle. Proc Natl Acad Sci U S A 97:4621–4626. http://dx.doi.org/10.1073/pnas.080077197. [PubMed]
90. Bayas CA, Wang J, Lee MK, Schrader JM, Shapiro L, Moerner WE. 2018. Spatial organization and dynamics of RNase E and ribosomes in Caulobacter crescentus. Proc Natl Acad Sci U S A 115:E3712–E3721. http://dx.doi.org/10.1073/pnas.1721648115. [PubMed]
91. Montero Llopis P, Sliusarenko O, Heinritz J, Jacobs-Wagner C. 2012. In vivo biochemistry in bacterial cells using FRAP: insight into the translation cycle. Biophys J 103:1848–1859. http://dx.doi.org/10.1016/j.bpj.2012.09.035. [PubMed]
92. Evguenieva-Hackenberg E, Roppelt V, Lassek C, Klug G. 2011. Subcellular localization of RNA degrading proteins and protein complexes in prokaryotes. RNA Biol 8:49–54. http://dx.doi.org/10.4161/rna.8.1.14066. [PubMed]
93. Redder P. 2016. How does sub-cellular localization affect the fate of bacterial mRNA? Curr Genet 62:687–690. http://dx.doi.org/10.1007/s00294-016-0587-1. [PubMed]
94. Mackie GA. 2013. RNase E: at the interface of bacterial RNA processing and decay. Nat Rev Microbiol 11:45–57. http://dx.doi.org/10.1038/nrmicro2930. [PubMed]
95. Carpousis AJ. 2007. The RNA degradosome of Escherichia coli: an mRNA-degrading machine assembled on RNase E. Annu Rev Microbiol 61:71–87. http://dx.doi.org/10.1146/annurev.micro.61.080706.093440. [PubMed]
96. Lehnik-Habrink M, Lewis RJ, Mäder U, Stülke J. 2012. RNA degradation in Bacillus subtilis: an interplay of essential endo- and exoribonucleases. Mol Microbiol 84:1005–1017. http://dx.doi.org/10.1111/j.1365-2958.2012.08072.x. [PubMed]
97. Taghbalout A, Rothfield L. 2007. RNaseE and the other constituents of the RNA degradosome are components of the bacterial cytoskeleton. Proc Natl Acad Sci U S A 104:1667–1672. http://dx.doi.org/10.1073/pnas.0610491104. [PubMed]
98. Khemici V, Poljak L, Luisi BF, Carpousis AJ. 2008. The RNase E of Escherichia coli is a membrane-binding protein. Mol Microbiol 70:799–813. [PubMed]
99. Taghbalout A, Yang Q, Arluison V. 2014. The Escherichia coli RNA processing and degradation machinery is compartmentalized within an organized cellular network. Biochem J 458:11–22. http://dx.doi.org/10.1042/BJ20131287. [PubMed]
100. Strahl H, Turlan C, Khalid S, Bond PJ, Kebalo JM, Peyron P, Poljak L, Bouvier M, Hamoen L, Luisi BF, Carpousis AJ. 2015. Membrane recognition and dynamics of the RNA degradosome. PLoS Genet 11:e1004961. http://dx.doi.org/10.1371/journal.pgen.1004961. [PubMed]
101. Murashko ON, Lin-Chao S. 2017. Escherichia coli responds to environmental changes using enolasic degradosomes and stabilized DicF sRNA to alter cellular morphology. Proc Natl Acad Sci U S A 114:E8025–E8034. http://dx.doi.org/10.1073/pnas.1703731114. [PubMed]
102. Cascante-Estepa N, Gunka K, Stülke J. 2016. Localization of components of the RNA-degrading machine in Bacillus subtilis. Front Microbiol 7:1492. http://dx.doi.org/10.3389/fmicb.2016.01492. [PubMed]
103. Koch G, Wermser C, Acosta IC, Kricks L, Stengel ST, Yepes A, Lopez D. 2017. Attenuating Staphylococcus aureus virulence by targeting flotillin protein scaffold activity. Cell Chem Biol 24:845–857.e6. http://dx.doi.org/10.1016/j.chembiol.2017.05.027. [PubMed]
104. Russell JH, Keiler KC. 2009. Subcellular localization of a bacterial regulatory RNA. Proc Natl Acad Sci U S A 106:16405–16409. http://dx.doi.org/10.1073/pnas.0904904106. [PubMed]
105. Fei J, Singh D, Zhang Q, Park S, Balasubramanian D, Golding I, Vanderpool CK, Ha T. 2015. RNA biochemistry. Determination of in vivo target search kinetics of regulatory noncoding RNA. Science 347:1371–1374. http://dx.doi.org/10.1126/science.1258849. [PubMed]
106. Sheng H, Stauffer WT, Hussein R, Lin C, Lim HN. 2017. Nucleoid and cytoplasmic localization of small RNAs in Escherichia coli. Nucleic Acids Res 45:2919–2934. [PubMed]
107. Wadler CS, Vanderpool CK. 2007. A dual function for a bacterial small RNA: SgrS performs base pairing-dependent regulation and encodes a functional polypeptide. Proc Natl Acad Sci U S A 104:20454–20459. http://dx.doi.org/10.1073/pnas.0708102104. [PubMed]
108. Wadler CS, Vanderpool CK. 2009. Characterization of homologs of the small RNA SgrS reveals diversity in function. Nucleic Acids Res 37:5477–5485. http://dx.doi.org/10.1093/nar/gkp591. [PubMed]
109. 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. http://dx.doi.org/10.1016/bs.adgen.2015.05.001. [PubMed]
110. Teimouri H, Korkmazhan E, Stavans J, Levine E. 2017. Sub-cellular mRNA localization modulates the regulation of gene expression by small RNAs in bacteria. Phys Biol 14:056001. http://dx.doi.org/10.1088/1478-3975/aa69ac. [PubMed]
111. Kawamoto H, Morita T, Shimizu A, Inada T, Aiba H. 2005. Implication of membrane localization of target mRNA in the action of a small RNA: mechanism of post-transcriptional regulation of glucose transporter in Escherichia coli. Genes Dev 19:328–338. http://dx.doi.org/10.1101/gad.1270605. [PubMed]
112. Updegrove TB, Zhang A, Storz G. 2016. Hfq: the flexible RNA matchmaker. Curr Opin Microbiol 30:133–138. http://dx.doi.org/10.1016/j.mib.2016.02.003. [PubMed]
113. Diestra E, Cayrol B, Arluison V, Risco C. 2009. Cellular electron microscopy imaging reveals the localization of the Hfq protein close to the bacterial membrane. PLoS One 4:e8301. http://dx.doi.org/10.1371/journal.pone.0008301. [PubMed]
114. Malabirade A, Jiang K, Kubiak K, Diaz-Mendoza A, Liu F, van Kan JA, Berret JF, Arluison V, van der Maarel JR. 2017. Compaction and condensation of DNA mediated by the C-terminal domain of Hfq. Nucleic Acids Res 45:7299–7308. http://dx.doi.org/10.1093/nar/gkx431. [PubMed]
115. Malabirade A, Morgado-Brajones J, Trépout S, Wien F, Marquez I, Seguin J, Marco S, Velez M, Arluison V. 2017. Membrane association of the bacterial riboregulator Hfq and functional perspectives. Sci Rep 7:10724. http://dx.doi.org/10.1038/s41598-017-11157-5. [PubMed]
116. Persson F, Lindén M, Unoson C, Elf J. 2013. Extracting intracellular diffusive states and transition rates from single-molecule tracking data. Nat Methods 10:265–269. http://dx.doi.org/10.1038/nmeth.2367. [PubMed]
117. Choi HM, Beck VA, Pierce NA. 2014. Next-generation in situ hybridization chain reaction: higher gain, lower cost, greater durability. ACS Nano 8:4284–4294. http://dx.doi.org/10.1021/nn405717p. [PubMed]
118. Shah S, Lubeck E, Zhou W, Cai L. 2017. Editorial note to: In situ transcription profiling of single cells reveals spatial organization of cells in the mouse hippocampus. Neuron 94:745–746. http://dx.doi.org/10.1016/j.neuron.2017.05.009. [PubMed]
119. Qian X, Lloyd RV. 2003. Recent developments in signal amplification methods for in situ hybridization. Diagn Mol Pathol 12:1–13. http://dx.doi.org/10.1097/00019606-200303000-00001. [PubMed]
120. Bagasra O. 2007. Protocols for the in situ PCR-amplification and detection of mRNA and DNA sequences. Nat Protoc 2:2782–2795. http://dx.doi.org/10.1038/nprot.2007.395. [PubMed]
121. Larsson C, Koch J, Nygren A, Janssen G, Raap AK, Landegren U, Nilsson M. 2004. In situ genotyping individual DNA molecules by target-primed rolling-circle amplification of padlock probes. Nat Methods 1:227–232. http://dx.doi.org/10.1038/nmeth723. [PubMed]
122. Larsson C, Grundberg I, Söderberg O, Nilsson M. 2010. In situ detection and genotyping of individual mRNA molecules. Nat Methods 7:395–397. http://dx.doi.org/10.1038/nmeth.1448. [PubMed]
123. Lubeck E, Cai L. 2012. Single-cell systems biology by super-resolution imaging and combinatorial labeling. Nat Methods 9:743–748. http://dx.doi.org/10.1038/nmeth.2069. [PubMed]
124. Lubeck E, Coskun AF, Zhiyentayev T, Ahmad M, Cai L. 2014. Single-cell in situ RNA profiling by sequential hybridization. Nat Methods 11:360–361. http://dx.doi.org/10.1038/nmeth.2892. [PubMed]
125. Jungmann R, Avendaño MS, Woehrstein JB, Dai M, Shih WM, Yin P. 2014. Multiplexed 3D cellular super-resolution imaging with DNA-PAINT and Exchange-PAINT. Nat Methods 11:313–318. http://dx.doi.org/10.1038/nmeth.2835. [PubMed]
126. Chen KH, Boettiger AN, Moffitt JR, Wang S, Zhuang X. 2015. RNA imaging. Spatially resolved, highly multiplexed RNA profiling in single cells. Science 348:aaa6090. http://dx.doi.org/10.1126/science.aaa6090. [PubMed]
127. Moffitt JR, Hao J, Wang G, Chen KH, Babcock HP, Zhuang X. 2016. High-throughput single-cell gene-expression profiling with multiplexed error-robust fluorescence in situ hybridization. Proc Natl Acad Sci U S A 113:11046–11051. http://dx.doi.org/10.1073/pnas.1612826113. [PubMed]
128. Takei Y, Shah S, Harvey S, Qi LS, Cai L. 2017. Multiplexed dynamic imaging of genomic loci by combined CRISPR imaging and DNA sequential FISH. Biophys J 112:1773–1776. http://dx.doi.org/10.1016/j.bpj.2017.03.024. [PubMed]
129. Guan J, Liu H, Shi X, Feng S, Huang B. 2017. Tracking multiple genomic elements using correlative CRISPR imaging and sequential DNA FISH. Biophys J 112:1077–1084. http://dx.doi.org/10.1016/j.bpj.2017.01.032. [PubMed]
130. Chen B, Gilbert LA, Cimini BA, Schnitzbauer J, Zhang W, Li GW, Park J, Blackburn EH, Weissman JS, Qi LS, Huang B. 2013. Dynamic imaging of genomic loci in living human cells by an optimized CRISPR/Cas system. Cell 155:1479–1491. http://dx.doi.org/10.1016/j.cell.2013.12.001. [PubMed]
131. Nelles DA, Fang MY, O’Connell MR, Xu JL, Markmiller SJ, Doudna JA, Yeo GW. 2016. Programmable RNA tracking in live cells with CRISPR/Cas9. Cell 165:488–496. http://dx.doi.org/10.1016/j.cell.2016.02.054. [PubMed]
132. Abudayyeh OO, Gootenberg JS, Essletzbichler P, Han S, Joung J, Belanto JJ, Verdine V, Cox DB, Kellner MJ, Regev A, Lander ES, Voytas DF, Ting AY, Zhang F. 2017. RNA targeting with CRISPR-Cas13. Nature 550:280–284. http://dx.doi.org/10.1038/nature24049. [PubMed]
133. O’Connell MR, Oakes BL, Sternberg SH, East-Seletsky A, Kaplan M, Doudna JA. 2014. Programmable RNA recognition and cleavage by CRISPR/Cas9. Nature 516:263–266. http://dx.doi.org/10.1038/nature13769. [PubMed]
134. Gross GG, Junge JA, Mora RJ, Kwon HB, Olson CA, Takahashi TT, Liman ER, Ellis-Davies GC, McGee AW, Sabatini BL, Roberts RW, Arnold DB. 2013. Recombinant probes for visualizing endogenous synaptic proteins in living neurons. Neuron 78:971–985. http://dx.doi.org/10.1016/j.neuron.2013.04.017. [PubMed]
135. Halstead JM, Lionnet T, Wilbertz JH, Wippich F, Ephrussi A, Singer RH, Chao JA. 2015. Translation. An RNA biosensor for imaging the first round of translation from single cells to living animals. Science 347:1367–1671. http://dx.doi.org/10.1126/science.aaa3380. [PubMed]
136. Tanenbaum ME, Gilbert LA, Qi LS, Weissman JS, Vale RD. 2014. A protein-tagging system for signal amplification in gene expression and fluorescence imaging. Cell 159:635–646. http://dx.doi.org/10.1016/j.cell.2014.09.039. [PubMed]
137. Yan X, Hoek TA, Vale RD, Tanenbaum ME. 2016. Dynamics of translation of single mRNA molecules in vivo. Cell 165:976–989. http://dx.doi.org/10.1016/j.cell.2016.04.034. [PubMed]
138. Wu B, Eliscovich C, Yoon YJ, Singer RH. 2016. Translation dynamics of single mRNAs in live cells and neurons. Science 352:1430–1435. http://dx.doi.org/10.1126/science.aaf1084. [PubMed]
139. Wang C, Han B, Zhou R, Zhuang X. 2016. Real-time imaging of translation on single mRNA transcripts in live cells. Cell 165:990–1001. http://dx.doi.org/10.1016/j.cell.2016.04.040. [PubMed]
140. Morisaki T, Lyon K, DeLuca KF, DeLuca JG, English BP, Zhang Z, Lavis LD, Grimm JB, Viswanathan S, Looger LL, Lionnet T, Stasevich TJ. 2016. Real-time quantification of single RNA translation dynamics in living cells. Science 352:1425–1429. http://dx.doi.org/10.1126/science.aaf0899. [PubMed]
141. Horvathova I, Voigt F, Kotrys AV, Zhan Y, Artus-Revel CG, Eglinger J, Stadler MB, Giorgetti L, Chao JA. 2017. The dynamics of mRNA turnover revealed by single-molecule imaging in single cells. Mol Cell 68:615–625.e9. http://dx.doi.org/10.1016/j.molcel.2017.09.030. [PubMed]
142. Kieft JS, Rabe JL, Chapman EG. 2015. New hypotheses derived from the structure of a flaviviral Xrn1-resistant RNA: conservation, folding, and host adaptation. RNA Biol 12:1169–1177. http://dx.doi.org/10.1080/15476286.2015.1094599. [PubMed]
143. Huang K, Doyle F, Wurz ZE, Tenenbaum SA, Hammond RK, Caplan JL, Meyers BC. 2017. FASTmiR: an RNA-based sensor for in vitro quantification and live-cell localization of small RNAs. Nucleic Acids Res 45:e130. http://dx.doi.org/10.1093/nar/gkx504. [PubMed]
144. Chen F, Wassie AT, Cote AJ, Sinha A, Alon S, Asano S, Daugharthy ER, Chang JB, Marblestone A, Church GM, Raj A, Boyden ES. 2016. Nanoscale imaging of RNA with expansion microscopy. Nat Methods 13:679–684. http://dx.doi.org/10.1038/nmeth.3899. [PubMed]
145. Chang JB, Chen F, Yoon YG, Jung EE, Babcock H, Kang JS, Asano S, Suk HJ, Pak N, Tillberg PW, Wassie AT, Cai D, Boyden ES. 2017. Iterative expansion microscopy. Nat Methods 14:593–599. http://dx.doi.org/10.1038/nmeth.4261. [PubMed]
146. Zhang YS, Chang JB, Alvarez MM, Trujillo-de Santiago G, Aleman J, Batzaya B, Krishnadoss V, Ramanujam AA, Kazemzadeh-Narbat M, Chen F, Tillberg PW, Dokmeci MR, Boyden ES, Khademhosseini A. 2016. Hybrid microscopy: enabling inexpensive high-performance imaging through combined physical and optical magnifications. Sci Rep 6:22691. http://dx.doi.org/10.1038/srep22691. [PubMed]
147. Ramamurthi KS, Schneewind O. 2005. A synonymous mutation in Yersinia enterocolitica yopE affects the function of the YopE type III secretion signal. J Bacteriol 187:707–715. http://dx.doi.org/10.1128/JB.187.2.707-715.2005. [PubMed]
148. Prilusky J, Bibi E. 2009. Studying membrane proteins through the eyes of the genetic code revealed a strong uracil bias in their coding mRNAs. Proc Natl Acad Sci U S A 106:6662–6666. http://dx.doi.org/10.1073/pnas.0902029106. [PubMed]
149. Storz G, Wolf YI, Ramamurthi KS. 2014. Small proteins can no longer be ignored. Annu Rev Biochem 83:753–777. http://dx.doi.org/10.1146/annurev-biochem-070611-102400. [PubMed]
Loading

Article metrics loading...

/content/journal/microbiolspec/10.1128/microbiolspec.RWR-0024-2018
2018-09-07
2018-11-19

Abstract:

Diverse mechanisms and functions of posttranscriptional regulation by small regulatory RNAs and RNA-binding proteins have been described in bacteria. In contrast, little is known about the spatial organization of RNAs in bacterial cells. In eukaryotes, subcellular localization and transport of RNAs play important roles in diverse physiological processes, such as embryonic patterning, asymmetric cell division, epithelial polarity, and neuronal plasticity. It is now clear that bacterial RNAs also can accumulate at distinct sites in the cell. However, due to the small size of bacterial cells, RNA localization and localization-associated functions are more challenging to study in bacterial cells, and the underlying molecular mechanisms of transcript localization are less understood. Here, we review the emerging examples of RNAs localized to specific subcellular locations in bacteria, with indications that subcellular localization of transcripts might be important for gene expression and regulatory processes. Diverse mechanisms for bacterial RNA localization have been suggested, including close association to their genomic site of transcription, or to the localizations of their protein products in translation-dependent or -independent processes. We also provide an overview of the state of the art of technologies to visualize and track bacterial RNAs, ranging from hybridization-based approaches in fixed cells to imaging approaches using fluorescent protein reporters and/or RNA aptamers in single living bacterial cells. We conclude with a discussion of open questions in the field and ongoing technological developments regarding RNA imaging in eukaryotic systems that might likewise provide novel insights into RNA localization in bacteria.

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

Full text loading...

Figures

Image of FIGURE 1
FIGURE 1

Methods to visualize bacterial RNAs. (A) smFISH and its application to imaging SgrS sRNA and its target mRNA . Images from diffraction-limited and super-resolution microscopes are shown for comparison. Adapted from reference 105 . (B) Illustration of the FP reporter approaches with a FP-RBP and a corresponding RNA motif, using the MS2 system as an example, and its application to track mRNAs at the single-molecule level in live cells. Image adapted from reference 67 . The scale bar in the image represents 1 μm. (C) The Spinach aptamer and its application to image mRNAs in live cells, in which a Spinach aptamer is fused to the RNA and with fluorescence detection upon addition of the organic ligand 3,5-difluoro-4-hydroxybenzylidene imidazolinone (DFHBI). Image adapted from reference 58 (licensed under a Creative Commons Attribution 4.0 International License [http://creativecommons.org/licenses/by/4.0/]).

Source: microbiolspec September 2018 vol. 6 no. 5 doi:10.1128/microbiolspec.RWR-0024-2018
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of FIGURE 2
FIGURE 2

Diverse patterns of subcellular mRNA localization in bacteria. Schematic drawings of diverse mRNA localization patterns commonly reported in different bacteria. RNA molecules are shown in green, and the nucleoid in gray. (A) Distribution throughout the cytoplasm. (B) Localization at the site of transcription in the nucleoid. (C) Helical localization. (D) Enrichment at the inner membrane. (E) Localization at the cell poles and (F) septum.

Source: microbiolspec September 2018 vol. 6 no. 5 doi:10.1128/microbiolspec.RWR-0024-2018
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of FIGURE 3
FIGURE 3

Emerging mRNA imaging methods in eukaryotic systems. (A) In the HCR, binding of the primary probe initiates the alternating binding of two HCR probes, thereby amplifying the signal. (B) In the PCR, a cDNA is first generated from the RNA of interest. Padlock probes are hybridized to the cDNA and ligated to be circular DNAs. Fluorophore-labeled secondary probes are then hybridized to the products generated from rolling circle amplification of these circular DNA templates. (C) Schematic representation of the TRICK reporter construct. (D) Schematic representation of the SunTag construct. (E) Schematic representation of the TREAT reporter construct.

Source: microbiolspec September 2018 vol. 6 no. 5 doi:10.1128/microbiolspec.RWR-0024-2018
Permissions and Reprints Request Permissions
Download as Powerpoint

Supplemental Material

No supplementary material available for this content.

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