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Volume 7, Issue 3

Genera specific distribution of DEAD-box RNA helicases in cyanobacteria Open Access

Abstract

Although RNA helicases are essentially ubiquitous and perform roles in all stages of RNA metabolism, phylogenetic analysis of the DEAD (Asp-Glu-Ala-Asp)-box RNA helicase family in a single phylum has not been performed. Here, we performed a phylogenetic analysis on DEAD-box helicases from all currently available cyanobacterial genomes, comprising a total of 362 helicase protein sequences from 280 strains. DEAD-box helicases belonging to three distinct clades were observed. Two clades, the CsdA (cold shock DEAD-box A)-like and RhlE (RNA helicase E)-like helicases, cluster with the homologous proteins from . The third clade, the CrhR (cyanobacterial RNA helicase Redox)-like helicases, is unique to cyanobacteria and characterized by a conserved sequence motif in the C-terminal extension. Restricted distribution is observed across cyanobacterial diversity with respect to both helicase type and strain. CrhR-like and CsdA-like helicases essentially never occur together, while RhlE always occurs with either a CrhR-like or CsdA-like helicase. CrhR-like and RhlE-like proteins occurred in filamentous cyanobacteria of the orders , and . Similarly, CsdA- and RhlE-like proteins are restricted to unicellular cyanobacteria of the genera and . In addition, the unexpected occurrence of RhlE in two strains suggests recent acquisition and evolutionary divergence. This study, therefore, raises physiological and evolutionary questions as to why DEAD-box RNA helicases encoded in cyanobacterial lineages display restricted distributions, suggesting niches that require either CrhR or CsdA RNA helicase activity but not both. Extensive conservation of gene synteny surrounding the previously described operon is also observed, indicating a role in the maintenance of photosynthesis. The analysis provides insights into the evolution, origin and dissemination of sequences within a single gene family to yield divergent functional roles.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): CrhR , cyanobacteria , DEAD-box RNA helicase and phylogenetic analysis
Funding
This study was supported by the:
  • Natural Sciences and Engineering Research Council of Canada (Award 171319)
    • Principle Award Recipient: GeorgeW. Owttrim
© 2021 The Authors
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License.
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2021-02-04
2024-04-26
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References

  1. Herschlag D. RNA chaperones and the RNA folding problem. J Biol Chem 1995; 270:20871–20874 [View Article][PubMed]
     [Google Scholar]
  2. Woodson SA, Panja S, Santiago-Frangos A. Proteins that chaperone RNA regulation. In Storz G, Papenfort K. eds Regulating with RNA in Bacteria and Archaea Washington, DC: American Society for Microbiology; 2019 pp 385–397
     [Google Scholar]
  3. Cordin O, Banroques J, Tanner NK, Linder P. The DEAD-box protein family of RNA helicases. Gene 2006; 367:17–37 [View Article][PubMed]
     [Google Scholar]
  4. Jankowsky E. RNA helicases at work: binding and rearranging. Trends Biochem Sci 2011; 36:19–29 [View Article][PubMed]
     [Google Scholar]
  5. Linder P, Fuller-Pace F. Happy birthday: 25 years of DEAD-box proteins. Methods Mol Biol 2015; 1259:17–33 [View Article][PubMed]
     [Google Scholar]
  6. Jarmoskaite I, Russell R. RNA helicase proteins as chaperones and remodelers. Annu Rev Biochem 2014; 83:697–725 [View Article][PubMed]
     [Google Scholar]
  7. Linder P, Jankowsky E. From unwinding to clamping – the DEAD box RNA helicase family. Nat Rev Mol Cell Biol 2011; 12:505–516 [View Article][PubMed]
     [Google Scholar]
  8. Tanner NK, Linder P. DExD/H box RNA helicases: from generic motors to specific dissociation functions. Mol Cell 2001; 8:251–262 [View Article][PubMed]
     [Google Scholar]
  9. Schmid SR, Linder P. D-E-A-D protein family of putative RNA helicases. Mol Microbiol 1992; 6:283–291 [View Article][PubMed]
     [Google Scholar]
  10. Schütz P, Karlberg T, van den Berg S, Collins R, Lehtiö L et al. Comparative structural analysis of human DEAD-box RNA helicases. PLoS One 2010; 5:e12791 [View Article][PubMed]
     [Google Scholar]
  11. Walker JE, Saraste M, Runswick MJ, Gay NJ. Distantly related sequences in the alpha- and beta-subunits of ATP synthase, myosin, kinases and other ATP-requiring enzymes and a common nucleotide binding fold. EMBO J 1982; 1:945–951 [View Article][PubMed]
     [Google Scholar]
  12. Yang Q, Jankowsky E. The DEAD-box protein Ded1 unwinds RNA duplexes by a mode distinct from translocating helicases. Nat Struct Mol Biol 2006; 13:981–986 [View Article][PubMed]
     [Google Scholar]
  13. Liu F, Putnam AA, Jankowsky E. DEAD-box helicases form nucleotide-dependent, long-lived complexes with RNA. Biochemistry 2014; 53:423–433 [View Article][PubMed]
     [Google Scholar]
  14. Redder P, Hausmann S, Khemici V, Yasrebi H, Linder P. Bacterial versatility requires DEAD-box RNA helicases. FEMS Microbiol Rev 2015; 39:392–412 [View Article][PubMed]
     [Google Scholar]
  15. Khemici V, Linder P. RNA helicases in bacteria. Curr Opin Microbiol 2016; 30:58–66 [View Article][PubMed]
     [Google Scholar]
  16. Owttrim GW. RNA helicases: diverse roles in prokaryotic response to abiotic stress. RNA Biol 2013; 10:96–110 [View Article][PubMed]
     [Google Scholar]
  17. López-Ramírez V, Alcaraz LD, Moreno-Hagelsieb G, Olmedo-Álvarez G. Phylogenetic distribution and evolutionary history of bacterial DEAD-box proteins. J Mol Evol 2011; 72:413–431 [View Article][PubMed]
     [Google Scholar]
  18. Diges CM, Uhlenbeck OC. Escherichia coli DbpA is an RNA helicase that requires hairpin 92 of 23S rRNA. EMBO J 2001; 20:5503–5512 [View Article][PubMed]
     [Google Scholar]
  19. Kossen K, Uhlenbeck OC. Cloning and biochemical characterization of Bacillus subtilis YxiN, a DEAD protein specifically activated by 23S rRNA: delineation of a novel sub-family of bacterial DEAD proteins. Nucleic Acids Res 1999; 27:3811–3820 [View Article][PubMed]
     [Google Scholar]
  20. Nicol SM, Fuller-Pace FV. The "DEAD box" protein DbpA interacts specifically with the peptidyltransferase center in 23S rRNA. Proc Natl Acad Sci USA 1995; 92:11681–11685 [View Article][PubMed]
     [Google Scholar]
  21. Charollais J, Dreyfus M, Iost I. CsdA, a cold-shock RNA helicase from Escherichia coli, is involved in the biogenesis of 50S ribosomal subunit. Nucleic Acids Res 2004; 32:2751–2759 [View Article][PubMed]
     [Google Scholar]
  22. Lehnik-Habrink M, Rempeters L, Kovács Ákos T, Wrede C, Baierlein C et al. DEAD-box RNA helicases in Bacillus subtilis have multiple functions and act independently from each other. J Bacteriol 2013; 195:534–544 [View Article][PubMed]
     [Google Scholar]
  23. Peil L, Virumäe K, Remme J. Ribosome assembly in Escherichia coli strains lacking the RNA helicase DeaD/CsdA or DbpA. FEBS J 2008; 275:3772–3782 [View Article][PubMed]
     [Google Scholar]
  24. Baumgartner RJ, Van Kranendonk MJ, Wacey D, Fiorentini ML, Saunders M et al. Nano−porous pyrite and organic matter in 3.5-billion-year-old stromatolites record primordial life. Geology 2019; 47:1039–1043 [View Article]
     [Google Scholar]
  25. Beck C, Knoop H, Axmann IM, Steuer R. The diversity of cyanobacterial metabolism: genome analysis of multiple phototrophic microorganisms. BMC Genomics 2012; 13:56 [View Article][PubMed]
     [Google Scholar]
  26. Soo RM, Hemp J, Parks DH, Fischer WW, Hugenholtz P. On the origins of oxygenic photosynthesis and aerobic respiration in Cyanobacteria. Science 2017; 355:1436–1440 [View Article][PubMed]
     [Google Scholar]
  27. Fuchsman CA, Palevsky HI, Widner B, Duffy M, Carlson MCG et al. Cyanobacteria and cyanophage contributions to carbon and nitrogen cycling in an oligotrophic oxygen-deficient zone. ISME J 2019; 13:2714–2726 [View Article][PubMed]
     [Google Scholar]
  28. Gilmour DJ. Microalgae for biofuel production. Adv Appl Microbiol 2019; 109:1–30 [View Article][PubMed]
     [Google Scholar]
  29. Georg J. A hidden layer of genetic information – regulatory non-protein-coding RNAs in Synechocystis PCC6803. PhD thesis Universitat Freiburg; Breisgau, Germany: 2010
     [Google Scholar]
  30. Magee WC. Characterization of a cyanobacterial RNA helicase gene. MSc thesis University of Alberta; Edmonton, AB, Canada: 1997
     [Google Scholar]
  31. Chamot D, Magee WC, Yu E, Owttrim GW. A cold shock-induced cyanobacterial RNA helicase. J Bacteriol 1999; 181:1728–1732 [View Article][PubMed]
     [Google Scholar]
  32. Kujat SL, Owttrim GW. Redox-regulated RNA helicase expression. Plant Physiol 2000; 124:703–714 [View Article][PubMed]
     [Google Scholar]
  33. El-Fahmawi B, Owttrim GW. Polar-biased localization of the cold stress-induced RNA helicase, CrhC, in the cyanobacterium Anabaena sp. strain PCC 7120. Mol Microbiol 2003; 50:1439–1448 [View Article][PubMed]
     [Google Scholar]
  34. Ritter SPA, Lewis AC, Vincent SL, Lo LL, Cunha APA et al. Evidence for convergent sensing of multiple abiotic stresses in cyanobacteria. Biochim Biophys Acta 2020; 1864:129462 [View Article][PubMed]
     [Google Scholar]
  35. Rosana ARR, Whitford DS, Fahlman RP, Owttrim GW. Cyanobacterial RNA helicase CrhR localizes to the thylakoid membrane region and cosediments with degradosome and polysome complexes in Synechocystis sp. strain PCC 6803. J Bacteriol 2016; 198:2089–2099 [View Article][PubMed]
     [Google Scholar]
  36. Rosana ARR, Ventakesh M, Chamot D, Patterson-Fortin LM, Tarassova O et al. Inactivation of a low temperature-induced RNA helicase in Synechocystis sp. PCC 6803: physiological and morphological consequences. Plant Cell Physiol 2012; 53:646–658 [View Article][PubMed]
     [Google Scholar]
  37. Sireesha K, Radharani B, Krishna PS, Sreedhar N, Subramanyam R et al. RNA helicase, CrhR is indispensable for the energy redistribution and the regulation of photosystem stoichiometry at low temperature in Synechocystis sp. PCC6803. Biochim Biophys Acta 2012; 1817:1525–1536 [View Article][PubMed]
     [Google Scholar]
  38. Edgar RC. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 2004; 32:1792–1797 [View Article][PubMed]
     [Google Scholar]
  39. Kumar S, Stecher G, Tamura K. mega7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 2016; 33:1870–1874 [View Article][PubMed]
     [Google Scholar]
  40. Lewis PO. NCL: a C++ class library for interpreting data files in NEXUS format. Bioinformatics 2003; 19:2330–2331 [View Article][PubMed]
     [Google Scholar]
  41. Miller MA, Pfeiffer W, Schwartz T. Creating the CIPRES Science Gateway for inference of large phylogenetic trees. Proceedings of the 2010 Gateway Computing Environments Workshop (GCE 2010) New Orleans, LA, USA: ACM; 2010 pp 1–8
     [Google Scholar]
  42. Stamatakis A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 2014; 30:1312–1313 [View Article][PubMed]
     [Google Scholar]
  43. Le SQ, Gascuel O. An improved general amino acid replacement matrix. Mol Biol Evol 2008; 25:1307–1320 [View Article][PubMed]
     [Google Scholar]
  44. Pattengale ND, Alipour M, Bininda-Emonds ORP, Moret BME, Stamatakis A. How many bootstrap replicates are necessary?. J Comput Biol 2010; 17:337–354 [View Article][PubMed]
     [Google Scholar]
  45. Letunic I, Bork P. Interactive tree of life (iTOL) v3: an online tool for the display and annotation of phylogenetic and other trees. Nucleic Acids Res 2016; 44:W242–W245 [View Article][PubMed]
     [Google Scholar]
  46. Micallef L, Rodgers P. eulerAPE: drawing area-proportional 3-Venn diagrams using ellipses. PLoS One 2014; 9:e101717 [View Article][PubMed]
     [Google Scholar]
  47. Crooks GE, Hon G, Chandonia J-M, Brenner SE. WebLogo: a sequence logo generator. Genome Res 2004; 14:1188–1190 [View Article][PubMed]
     [Google Scholar]
  48. Finn RD, Mistry J, Tate J, Coggill P, Heger A et al. The Pfam protein families database. Nucleic Acids Res 2010; 38:D211–D222 [View Article][PubMed]
     [Google Scholar]
  49. Cordin O, Tanner NK, Doère M, Linder P, Banroques J. The newly discovered Q motif of DEAD-box RNA helicases regulates RNA-binding and helicase activity. EMBO J 2004; 23:2478–2487 [View Article][PubMed]
     [Google Scholar]
  50. Pause A, Méthot N, Sonenberg N. The HRIGRXXR region of the DEAD box RNA helicase eukaryotic translation initiation factor 4A is required for RNA binding and ATP hydrolysis. Mol Cell Biol 1993; 13:6789–6798 [View Article][PubMed]
     [Google Scholar]
  51. Sugita C, Ogata K, Shikata M, Jikuya H, Takano J et al. Complete nucleotide sequence of the freshwater unicellular cyanobacterium Synechococcus elongatus PCC 6301 chromosome: gene content and organization. Photosynth Res 2007; 93:55–67 [View Article][PubMed]
     [Google Scholar]
  52. Moreira D, Tavera R, Benzerara K, Skouri-Panet F, Couradeau E et al. Description of Gloeomargarita lithophora gen. nov., sp. nov., a thylakoid-bearing, basal-branching cyanobacterium with intracellular carbonates, and proposal for Gloeomargaritales ord. nov. Int J Syst Evol Microbiol 2017; 67:653–658 [View Article][PubMed]
     [Google Scholar]
  53. Rippka R, Waterbury J, Cohen-Bazire GA. A cyanobacterium which lacks thylakoids. Arch Microbiol 1974; 100:419–436 [View Article]
     [Google Scholar]
  54. Rosana ARR, Whitford DS, Migur A, Steglich C, Kujat-Choy SL et al. RNA helicase-regulated processing of the Synechocystis rimO-crhR operon results in differential cistron expression and accumulation of two sRNAs. J Biol Chem 2020; 295:6372–6386 [View Article][PubMed]
     [Google Scholar]
  55. Dandekar T, Snel B, Huynen M, Bork P. Conservation of gene order: a fingerprint of proteins that physically interact. Trends Biochem Sci 1998; 23:324–328 [View Article][PubMed]
     [Google Scholar]
  56. Robertson BR, Tezuka N, Watanabe MM. Phylogenetic analyses of Synechococcus strains (cyanobacteria) using sequences of 16S rDNA and part of the phycocyanin operon reveal multiple evolutionary lines and reflect phycobilin content. Int J Syst Evol Microbiol 2001; 51:861–871 [View Article][PubMed]
     [Google Scholar]
  57. Juteršek M, Klemenčič M, Dolinar M. Discrimination between Synechocystis members (cyanobacteria) based on heterogeneity of their 16S rRNA and ITS regions. Acta Chim Slov 2017; 64:804–817 [View Article][PubMed]
     [Google Scholar]
  58. Shih PM, Wu D, Latifi A, Axen SD, Fewer DP et al. Improving the coverage of the cyanobacterial phylum using diversity-driven genome sequencing. Proc Natl Acad Sci USA 2013; 110:1053–1058 [View Article][PubMed]
     [Google Scholar]
  59. Shimura Y, Hirose Y, Misawa N, Wakazuki S, Fujisawa T et al. Complete genome sequence of a coastal cyanobacterium, Synechococcus sp. strain NIES-970. Genome Announc 2017; 5:e00139–17 [View Article][PubMed]
     [Google Scholar]
  60. Yoshino T, Honda T, Tanaka M, Tanaka T. Draft genome sequence of marine cyanobacterium Synechococcus sp. strain NKBG15041c. Genome Announc 2013; 1:e00954-13 [View Article][PubMed]
     [Google Scholar]
  61. Swingley WD, Chen M, Cheung PC, Conrad AL, Dejesa LC et al. Niche adaptation and genome expansion in the chlorophyll d-producing cyanobacterium Acaryochloris marina . Proc Natl Acad Sci USA 2008; 105:2005–2010 [View Article][PubMed]
     [Google Scholar]
  62. Banroques J, Doère M, Dreyfus M, Linder P, Tanner NK. Motif III in superfamily 2 "helicases" helps convert the binding energy of ATP into a high-affinity RNA binding site in the yeast DEAD-box protein Ded1. J Mol Biol 2010; 396:949–966 [View Article][PubMed]
     [Google Scholar]
  63. Nelson WC, Maezato Y, Wu Y-W, Romine MF, Lindemann SR. Identification and resolution of microdiversity through metagenomic sequencing of parallel consortia. Appl Environ Microbiol 2015; 82:255–267 [View Article][PubMed]
     [Google Scholar]
  64. Paul R. Genome sequencing of Leptolyngbya Heron Island, 2a crystal structure of phycoerythrin and spectroscopic investigation of chromatic acclimation. PhD thesis Arizona State University; Tempe, AZ, USA: 2014
     [Google Scholar]
  65. Georg J, Rosana ARR, Chamot D, Migur A, Hess WR et al. Inactivation of the RNA helicase CrhR impacts a specific subset of the transcriptome in the cyanobacterium Synechocystis sp. PCC 6803. RNA Biol 2019; 16:1205–1214 [View Article][PubMed]
     [Google Scholar]
  66. Rosana AR, Chamot D, Owttrim GW. Autoregulation of RNA helicase expression in response to temperature stress in Synechocystis sp. PCC 6803. PLoS One 2012; 7:e48683 [View Article][PubMed]
     [Google Scholar]
  67. Tarassova OS, Chamot D, Owttrim GW. Conditional, temperature-induced proteolytic regulation of cyanobacterial RNA helicase expression. J Bacteriol 2014; 196:1560–1568 [View Article][PubMed]
     [Google Scholar]
  68. Nishiyama Y, Los DA, Murata N. PsbU, a protein associated with photosystem II, is required for the acquisition of cellular thermotolerance in Synechococcus species PCC 7002. Plant Physiol 1999; 120:301–308 [View Article][PubMed]
     [Google Scholar]
  69. Gerdes SY, Kurnasov OV, Shatalin K, Polanuyer B, Sloutsky R et al. Comparative genomics of NAD biosynthesis in cyanobacteria. J Bacteriol 2006; 188:3012–3023 [View Article][PubMed]
     [Google Scholar]
  70. Li W, Schulman S, Dutton RJ, Boyd D, Beckwith J et al. Structure of a bacterial homologue of vitamin K epoxide reductase. Nature 2010; 463:507–512 [View Article][PubMed]
     [Google Scholar]
  71. Wang S, Hu Y, Overgaard MT, Karginov FV, Uhlenbeck OC et al. The domain of the Bacillus subtilis DEAD-box helicase YxiN that is responsible for specific binding of 23S rRNA has an RNA recognition motif fold. RNA 2006; 12:959–967 [View Article][PubMed]
     [Google Scholar]
  72. Sharpe Elles LM, Sykes MT, Williamson JR, Uhlenbeck OC. A dominant negative mutant of the E. coli RNA helicase DbpA blocks assembly of the 50S ribosomal subunit. Nucleic Acids Res 2009; 37:6503–6514 [View Article][PubMed]
     [Google Scholar]
  73. Jones PG, Mitta M, Kim Y, Jiang W, Inouye M. Cold shock induces a major ribosomal-associated protein that unwinds double-stranded RNA in Escherichia coli . Proc Natl Acad Sci USA 1996; 93:76–80 [View Article][PubMed]
     [Google Scholar]
  74. Butland G, Krogan NJ, Xu J, Yang W-H, Aoki H et al. Investigating the in vivo activity of the DeaD protein using protein-protein interactions and the translational activity of structured chloramphenicol acetyltransferase mRNAs. J Cell Biochem 2007; 100:642–652 [View Article][PubMed]
     [Google Scholar]
  75. Prud'homme-Généreux A, Beran RK, Iost I, Ramey CS, Mackie GA et al. Physical and functional interactions among RNase E, polynucleotide phosphorylase and the cold-shock protein, CsdA: evidence for a 'cold shock degradosome'. Mol Microbiol 2004; 54:1409–1421 [View Article][PubMed]
     [Google Scholar]
  76. Vakulskas CA, Pannuri A, Cortés-Selva D, Zere TR, Ahmer BM et al. Global effects of the DEAD-box RNA helicase DeaD (CsdA) on gene expression over a broad range of temperatures. Mol Microbiol 2014; 92:945–958 [View Article][PubMed]
     [Google Scholar]
  77. Jain C. The E. coli RhlE RNA helicase regulates the function of related RNA helicases during ribosome assembly. RNA 2008; 14:381–389 [View Article][PubMed]
     [Google Scholar]
  78. Turner S, Pryer KM, Miao VPW, Palmer JD. Investigating deep phylogenetic relationships among cyanobacteria and plastids by small subunit rRNA sequence analysis. J Eukaryot Microbiol 1999; 46:327–338 [View Article][PubMed]
     [Google Scholar]
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Genera specific distribution of DEAD-box RNA helicases in cyanobacteria
M Gen 7, 000517 (2021); https://doi.org/10.1099/mgen.0.000517
/content/journal/mgen/10.1099/mgen.0.000517
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