1887

Abstract

Transcription termination factor Rho is a ring-shaped, ATP-dependent molecular motor that targets hundreds of transcription units in . Interest in Rho was renewed recently on the realization that this essential factor is involved in multiple interactions and cellular processes that protect the genome and regulate its expression on a global scale. Yet it is currently unknown if (and how) Rho-dependent mechanisms are conserved throughout the bacterial kingdom. Here, we mined public databases to assess the distribution, expression and structural conservation of Rho across bacterial phyla. We found that is present in more than 90 % of sequenced bacterial genomes, although Cyanobacteria, Mollicutes and a fraction of Firmicutes are totally devoid of . Genomes lacking tend to be small and AT-rich and often belong to species with parasitic/symbiotic lifestyles (such as Mollicutes). By contrast, large GC-rich genomes, such as those of Actinobacteria, often contain duplicates and/or encode Rho proteins that bear insertion domains of unknown function(s). Notwithstanding, most Rho sequences across taxa contain canonical RNA-binding and ATP hydrolysis signature motifs, a feature suggestive of largely conserved mechanism(s) of action. Mutations that impair binding of bicyclomycin are present in ~5 % of sequences, implying that species from diverse ecosystems have developed resistance against this natural antibiotic. Altogether, these findings assert that Rho function is widespread among bacteria and suggest that it plays a particularly relevant role in the expression of complex genomes and/or bacterial adaptation to changing environments.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.067462-0
2013-07-01
2019-12-08
Loading full text...

Full text loading...

/deliver/fulltext/micro/159/7/1423.html?itemId=/content/journal/micro/10.1099/mic.0.067462-0&mimeType=html&fmt=ahah

References

  1. Adelman J. L., Jeong Y. J., Liao J. C., Patel G., Kim D. E., Oster G., Patel S. S.. ( 2006;). Mechanochemistry of transcription termination factor Rho. . Mol Cell 22:, 611–621. [CrossRef][PubMed]
    [Google Scholar]
  2. Banerjee S., Chalissery J., Bandey I., Sen R.. ( 2006;). Rho-dependent transcription termination: more questions than answers. . J Microbiol 44:, 11–22.[PubMed]
    [Google Scholar]
  3. Bentley S. D., Parkhill J.. ( 2004;). Comparative genomic structure of prokaryotes. . Annu Rev Genet 38:, 771–792. [CrossRef][PubMed]
    [Google Scholar]
  4. Bentley J., Hyatt L. S., Ainley K., Parish J. H., Herbert R. B., White G. R.. ( 1993;). Cloning and sequence analysis of an Escherichia coli gene conferring bicyclomycin resistance. . Gene 127:, 117–120. [CrossRef][PubMed]
    [Google Scholar]
  5. Bordenstein S. R., Reznikoff W. S.. ( 2005;). Mobile DNA in obligate intracellular bacteria. . Nat Rev Microbiol 3:, 688–699. [CrossRef][PubMed]
    [Google Scholar]
  6. Bossi L., Schwartz A., Guillemardet B., Boudvillain M., Figueroa-Bossi N.. ( 2012;). A role for Rho-dependent polarity in gene regulation by a noncoding small RNA. . Genes Dev 26:, 1864–1873. [CrossRef][PubMed]
    [Google Scholar]
  7. Boudvillain M., Nollmann M., Margeat E.. ( 2010;). Keeping up to speed with the transcription termination factor Rho motor. . Transcription 1:, 70–75. [CrossRef][PubMed]
    [Google Scholar]
  8. Boudvillain M., Figueroa-Bossi N., Bossi L.. ( 2013;). Terminator still moving forward: expanding roles for Rho factor. . Curr Opin Microbiol 16:, 118–124. [CrossRef][PubMed]
    [Google Scholar]
  9. Butland G., Peregrín-Alvarez J. M., Li J., Yang W., Yang X., Canadien V., Starostine A., Richards D., Beattie B. et al. ( 2005;). Interaction network containing conserved and essential protein complexes in Escherichia coli. . Nature 433:, 531–537. [CrossRef][PubMed]
    [Google Scholar]
  10. Canals A., Usón I., Coll M.. ( 2010;). The structure of RNA-free Rho termination factor indicates a dynamic mechanism of transcript capture. . J Mol Biol 400:, 16–23. [CrossRef][PubMed]
    [Google Scholar]
  11. Cardinale C. J., Washburn R. S., Tadigotla V. R., Brown L. M., Gottesman M. E., Nudler E.. ( 2008;). Termination factor Rho and its cofactors NusA and NusG silence foreign DNA in E. coli. . Science 320:, 935–938. [CrossRef][PubMed]
    [Google Scholar]
  12. Ciampi M. S.. ( 2006;). Rho-dependent terminators and transcription termination. . Microbiology 152:, 2515–2528. [CrossRef][PubMed]
    [Google Scholar]
  13. de Hoon M. J., Makita Y., Nakai K., Miyano S.. ( 2005;). Prediction of transcriptional terminators in Bacillus subtilis and related species. . PLOS Comput Biol 1:, e25. [CrossRef][PubMed]
    [Google Scholar]
  14. Dunning Hotopp J. C., Lin M., Madupu R., Crabtree J., Angiuoli S. V., Eisen J. A., Seshadri R., Ren Q., Wu M. et al. ( 2006;). Comparative genomics of emerging human ehrlichiosis agents. . PLoS Genet 2:, e21. [CrossRef][PubMed]
    [Google Scholar]
  15. Dunning Hotopp J. C., Clark M. E., Oliveira D. C., Foster J. M., Fischer P., Muñoz Torres M. C., Giebel J. D., Kumar N., Ishmael N. et al. ( 2007;). Widespread lateral gene transfer from intracellular bacteria to multicellular eukaryotes. . Science 317:, 1753–1756. [CrossRef][PubMed]
    [Google Scholar]
  16. Dutta D., Shatalin K., Epshtein V., Gottesman M. E., Nudler E.. ( 2011;). Linking RNA polymerase backtracking to genome instability in E. coli. . Cell 146:, 533–543. [CrossRef][PubMed]
    [Google Scholar]
  17. Erie D. A.. ( 2002;). The many conformational states of RNA polymerase elongation complexes and their roles in the regulation of transcription. . Biochim Biophys Acta 1577:, 224–239. [CrossRef][PubMed]
    [Google Scholar]
  18. Garcia-Boronat M., Diez-Rivero C. M., Reinherz E. L., Reche P. A.. ( 2008;). PVS: a web server for protein sequence variability analysis tuned to facilitate conserved epitope discovery. . Nucleic Acids Res 36: (Web Server issue), W35–W41. [CrossRef][PubMed]
    [Google Scholar]
  19. Gouy M., Guindon S., Gascuel O.. ( 2010;). SeaView version 4: a multiplatform graphical user interface for sequence alignment and phylogenetic tree building. . Mol Biol Evol 27:, 221–224. [CrossRef][PubMed]
    [Google Scholar]
  20. Griffin J. E., Gawronski J. D., Dejesus M. A., Ioerger T. R., Akerley B. J., Sassetti C. M.. ( 2011;). High-resolution phenotypic profiling defines genes essential for mycobacterial growth and cholesterol catabolism. . PLoS Pathog 7:, e1002251. [CrossRef][PubMed]
    [Google Scholar]
  21. Hildebrand F., Meyer A., Eyre-Walker A.. ( 2010;). Evidence of selection upon genomic GC-content in bacteria. . PLoS Genet 6:, e1001107. [CrossRef][PubMed]
    [Google Scholar]
  22. Hollands K., Proshkin S., Sklyarova S., Epshtein V., Mironov A., Nudler E., Groisman E. A.. ( 2012;). Riboswitch control of Rho-dependent transcription termination. . Proc Natl Acad Sci U S A 109:, 5376–5381. [CrossRef][PubMed]
    [Google Scholar]
  23. Hu P., Janga S. C., Babu M., Díaz-Mejía J. J., Butland G., Yang W., Pogoutse O., Guo X., Phanse S. et al. ( 2009;). Global functional atlas of Escherichia coli encompassing previously uncharacterized proteins. . PLoS Biol 7:, e96. [CrossRef][PubMed]
    [Google Scholar]
  24. Ingham C. J., Hunter I. S., Smith M. C.. ( 1996;). Isolation and sequencing of the rho gene from Streptomyces lividans ZX7 and characterization of the RNA-dependent NTPase activity of the overexpressed protein. . J Biol Chem 271:, 21803–21807. [CrossRef][PubMed]
    [Google Scholar]
  25. Ivanova N., Daum C., Lang E., Abt B., Kopitz M., Saunders E., Lapidus A., Lucas S., Glavina Del Rio T. et al. ( 2010;). Complete genome sequence of Haliangium ochraceum type strain (SMP-2). . Stand Genomic Sci 2:, 96–106. [CrossRef][PubMed]
    [Google Scholar]
  26. Kalarickal N. C., Ranjan A., Kalyani B. S., Wal M., Sen R.. ( 2010;). A bacterial transcription terminator with inefficient molecular motor action but with a robust transcription termination function. . J Mol Biol 395:, 966–982. [CrossRef][PubMed]
    [Google Scholar]
  27. Kingsford C. L., Ayanbule K., Salzberg S. L.. ( 2007;). Rapid, accurate, computational discovery of Rho-independent transcription terminators illuminates their relationship to DNA uptake. . Genome Biol 8:, R22. [CrossRef][PubMed]
    [Google Scholar]
  28. Leela J. K., Syeda A. H., Anupama K., Gowrishankar J.. ( 2013;). Rho-dependent transcription termination is essential to prevent excessive genome-wide R-loops in Escherichia coli.. Proc Natl Acad Sci U S A 110:, 258–263. [CrossRef][PubMed]
    [Google Scholar]
  29. Li J., Mason S. W., Greenblatt J.. ( 1993;). Elongation factor NusG interacts with termination factor rho to regulate termination and antitermination of transcription. . Genes Dev 7:, 161–172. [CrossRef][PubMed]
    [Google Scholar]
  30. Magyar A., Zhang X., Abdi F., Kohn H., Widger W. R.. ( 1999;). Identifying the bicyclomycin binding domain through biochemical analysis of antibiotic-resistant rho proteins. . J Biol Chem 274:, 7316–7324. [CrossRef][PubMed]
    [Google Scholar]
  31. Massé E., Drolet M.. ( 1999;). R-loop-dependent hypernegative supercoiling in Escherichia coli topA mutants preferentially occurs at low temperatures and correlates with growth inhibition. . J Mol Biol 294:, 321–332. [CrossRef][PubMed]
    [Google Scholar]
  32. McCutcheon J. P., McDonald B. R., Moran N. A.. ( 2009;). Origin of an alternative genetic code in the extremely small and GC-rich genome of a bacterial symbiont. . PLoS Genet 5:, e1000565. [CrossRef][PubMed]
    [Google Scholar]
  33. Mischo H. E., Gómez-González B., Grzechnik P., Rondón A. G., Wei W., Steinmetz L., Aguilera A., Proudfoot N. J.. ( 2011;). Yeast Sen1 helicase protects the genome from transcription-associated instability. . Mol Cell 41:, 21–32. [CrossRef][PubMed]
    [Google Scholar]
  34. Mitra A., Nagaraja V.. ( 2012;). Under-representation of intrinsic terminators across bacterial genomic islands: Rho as a principal regulator of xenogenic DNA expression. . Gene 508:, 221–228. [CrossRef][PubMed]
    [Google Scholar]
  35. Miyamura S., Ogasawara N., Otsuka H., Niwayama S., Tanaka H., Take T., Uchiyama T., Ochiai H.. ( 1973;). Antibiotic 5879 produced by Streptomyces aizunensis, identical with bicyclomycin. . J Antibiot (Tokyo) 26:, 479–484. [CrossRef][PubMed]
    [Google Scholar]
  36. Miyoshi T., Miyairi N., Aoki H., Kosaka M., Sakai H.. ( 1972;). Bicyclomycin, a new antibiotic. I. Taxonomy, isolation and characterization. . J Antibiot (Tokyo) 25:, 569–575. [CrossRef][PubMed]
    [Google Scholar]
  37. Mooney R. A., Artsimovitch I., Landick R.. ( 1998;). Information processing by RNA polymerase: recognition of regulatory signals during RNA chain elongation. . J Bacteriol 180:, 3265–3275.[PubMed]
    [Google Scholar]
  38. Mykytczuk N. C., Trevors J. T., Foote S. J., Leduc L. G., Ferroni G. D., Twine S. M.. ( 2011;). Proteomic insights into cold adaptation of psychrotrophic and mesophilic Acidithiobacillus ferrooxidans strains. . Antonie van Leeuwenhoek 100:, 259–277. [CrossRef][PubMed]
    [Google Scholar]
  39. Näsvall J., Sun L., Roth J. R., Andersson D. I.. ( 2012;). Real-time evolution of new genes by innovation, amplification, and divergence. . Science 338:, 384–387. [CrossRef][PubMed]
    [Google Scholar]
  40. Nicolas P., Mäder U., Dervyn E., Rochat T., Leduc A., Pigeonneau N., Bidnenko E., Marchadier E., Hoebeke M. et al. ( 2012;). Condition-dependent transcriptome reveals high-level regulatory architecture in Bacillus subtilis. . Science 335:, 1103–1106. [CrossRef][PubMed]
    [Google Scholar]
  41. Nikoh N., Tanaka K., Shibata F., Kondo N., Hizume M., Shimada M., Fukatsu T.. ( 2008;). Wolbachia genome integrated in an insect chromosome: evolution and fate of laterally transferred endosymbiont genes. . Genome Res 18:, 272–280. [CrossRef][PubMed]
    [Google Scholar]
  42. Nishida M., Mine Y., Matsubara T., Goto S., Kuwahara S.. ( 1972;). Bicyclomycin, a new antibiotic. 3. In vitro and in vivo antimicrobial activity. . J Antibiot (Tokyo) 25:, 582–593. [CrossRef][PubMed]
    [Google Scholar]
  43. Nowatzke W. L., Burns C. M., Richardson J. P.. ( 1997a;). Function of the novel subdomain in the RNA binding domain of transcription termination factor Rho from Micrococcus luteus. . J Biol Chem 272:, 2207–2211. [CrossRef][PubMed]
    [Google Scholar]
  44. Nowatzke W. L., Keller E., Koch G., Richardson J. P.. ( 1997b;). Transcription termination factor Rho is essential for Micrococcus luteus. . J Bacteriol 179:, 5238–5240.[PubMed]
    [Google Scholar]
  45. Opperman T., Richardson J. P.. ( 1994;). Phylogenetic analysis of sequences from diverse bacteria with homology to the Escherichia coli rho gene. . J Bacteriol 176:, 5033–5043.[PubMed]
    [Google Scholar]
  46. Peters J. M., Mooney R. A., Kuan P. F., Rowland J. L., Keles S., Landick R.. ( 2009;). Rho directs widespread termination of intragenic and stable RNA transcription. . Proc Natl Acad Sci U S A 106:, 15406–15411. [CrossRef][PubMed]
    [Google Scholar]
  47. Peters J. M., Vangeloff A. D., Landick R.. ( 2011;). Bacterial transcription terminators: the RNA 3′-end chronicles. . J Mol Biol 412:, 793–813. [CrossRef][PubMed]
    [Google Scholar]
  48. Peters J. M., Mooney R. A., Grass J. A., Jessen E. D., Tran F., Landick R.. ( 2012;). Rho and NusG suppress pervasive antisense transcription in Escherichia coli. . Genes Dev 26:, 2621–2633. [CrossRef][PubMed]
    [Google Scholar]
  49. Pichoff S., Alibaud L., Guédant A., Castanié M. P., Bouché J. P.. ( 1998;). An Escherichia coli gene (yaeO) suppresses temperature-sensitive mutations in essential genes by modulating Rho-dependent transcription termination. . Mol Microbiol 29:, 859–869. [CrossRef][PubMed]
    [Google Scholar]
  50. Piette F., D’Amico S., Struvay C., Mazzucchelli G., Renaut J., Tutino M. L., Danchin A., Leprince P., Feller G.. ( 2010;). Proteomics of life at low temperatures: trigger factor is the primary chaperone in the Antarctic bacterium Pseudoalteromonas haloplanktis TAC125. . Mol Microbiol 76:, 120–132. [CrossRef][PubMed]
    [Google Scholar]
  51. Quirk P. G., Dunkley E. A. Jr, Lee P., Krulwich T. A.. ( 1993;). Identification of a putative Bacillus subtilis rho gene. . J Bacteriol 175:, 8053.[PubMed]
    [Google Scholar]
  52. Rabhi M., Tuma R., Boudvillain M.. ( 2010a;). RNA remodeling by hexameric RNA helicases. . RNA Biol 7:, 655–666. [CrossRef][PubMed]
    [Google Scholar]
  53. Rabhi M., Rahmouni A. R., Boudvillain M.. ( 2010b;). Transcription termination factor Rho: a ring-shaped RNA helicase from bacteria. . In RNA Helicases, vol. 19, pp. 243–271. Edited by Jankowsky E... Cambridge, UK:: RSC Publishing;. [CrossRef]
    [Google Scholar]
  54. Rabhi M., Gocheva V., Jacquinot F., Lee A., Margeat E., Boudvillain M.. ( 2011a;). Mutagenesis-based evidence for an asymmetric configuration of the ring-shaped transcription termination factor Rho. . J Mol Biol 405:, 497–518. [CrossRef][PubMed]
    [Google Scholar]
  55. Rabhi M., Espéli O., Schwartz A., Cayrol B., Rahmouni A. R., Arluison V., Boudvillain M.. ( 2011b;). The Sm-like RNA chaperone Hfq mediates transcription antitermination at Rho-dependent terminators. . EMBO J 30:, 2805–2816. [CrossRef][PubMed]
    [Google Scholar]
  56. Schmidt M. C., Chamberlin M. J.. ( 1984;). Binding of rho factor to Escherichia coli RNA polymerase mediated by NusA protein. . J Biol Chem 259:, 15000–15002.[PubMed]
    [Google Scholar]
  57. Schwartz A., Rabhi M., Jacquinot F., Margeat E., Rahmouni A. R., Boudvillain M.. ( 2009;). A stepwise 2′-hydroxyl activation mechanism for the bacterial transcription termination factor Rho helicase. . Nat Struct Mol Biol 16:, 1309–1316. [CrossRef][PubMed]
    [Google Scholar]
  58. Skordalakes E., Brogan A. P., Park B. S., Kohn H., Berger J. M.. ( 2005;). Structural mechanism of inhibition of the Rho transcription termination factor by the antibiotic bicyclomycin. . Structure 13:, 99–109. [CrossRef][PubMed]
    [Google Scholar]
  59. Skourti-Stathaki K., Proudfoot N. J., Gromak N.. ( 2011;). Human senataxin resolves RNA/DNA hybrids formed at transcriptional pause sites to promote Xrn2-dependent termination. . Mol Cell 42:, 794–805. [CrossRef][PubMed]
    [Google Scholar]
  60. Thomsen N. D., Berger J. M.. ( 2009;). Running in reverse: the structural basis for translocation polarity in hexameric helicases. . Cell 139:, 523–534. [CrossRef][PubMed]
    [Google Scholar]
  61. Tuckerman J. R., Gonzalez G., Gilles-Gonzalez M. A.. ( 2011;). Cyclic di-GMP activation of polynucleotide phosphorylase signal-dependent RNA processing. . J Mol Biol 407:, 633–639. [CrossRef][PubMed]
    [Google Scholar]
  62. Vijayan V., Jain I. H., O’Shea E. K.. ( 2011;). A high resolution map of a cyanobacterial transcriptome. . Genome Biol 12:, R47. [CrossRef][PubMed]
    [Google Scholar]
  63. Washburn R. S., Gottesman M. E.. ( 2011;). Transcription termination maintains chromosome integrity. . Proc Natl Acad Sci U S A 108:, 792–797. [CrossRef][PubMed]
    [Google Scholar]
  64. Washburn R. S., Marra A., Bryant A. P., Rosenberg M., Gentry D. R.. ( 2001;). rho is not essential for viability or virulence in Staphylococcus aureus. . Antimicrob Agents Chemother 45:, 1099–1103. [CrossRef][PubMed]
    [Google Scholar]
  65. Washio T., Sasayama J., Tomita M.. ( 1998;). Analysis of complete genomes suggests that many prokaryotes do not rely on hairpin formation in transcription termination. . Nucleic Acids Res 26:, 5456–5463. [CrossRef][PubMed]
    [Google Scholar]
  66. Waterhouse A. M., Procter J. B., Martin D. M., Clamp M., Barton G. J.. ( 2009;). Jalview version 2 – a multiple sequence alignment editor and analysis workbench. . Bioinformatics 25:, 1189–1191. [CrossRef][PubMed]
    [Google Scholar]
  67. Williams R. M., Durham C. A.. ( 1988;). Bicyclomycin: synthetic, mechanistic, and biological studies. . Chem Rev 88:, 511–540. [CrossRef]
    [Google Scholar]
  68. Wolf M., Müller T., Dandekar T., Pollack J. D.. ( 2004;). Phylogeny of Firmicutes with special reference to Mycoplasma (Mollicutes) as inferred from phosphoglycerate kinase amino acid sequence data. . Int J Syst Evol Microbiol 54:, 871–875. [CrossRef][PubMed]
    [Google Scholar]
  69. Yang X., Lewis P. J.. ( 2010;). The interaction between RNA polymerase and the elongation factor NusA. . RNA Biol 7:, 272–275. [CrossRef][PubMed]
    [Google Scholar]
  70. Zhao Y., Davis R. E., Lee I. M.. ( 2005;). Phylogenetic positions of ‘Candidatus Phytoplasma asteris’ and Spiroplasma kunkelii as inferred from multiple sets of concatenated core housekeeping proteins. . Int J Syst Evol Microbiol 55:, 2131–2141. [CrossRef][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.067462-0
Loading
/content/journal/micro/10.1099/mic.0.067462-0
Loading

Data & Media loading...

Supplements

Supplementary material 

PDF
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error