1887

Chapter 21 : Bacterial Y RNAs: Gates, Tethers, and tRNA Mimics

MyBook is a cheap paperback edition of the original book and will be sold at uniform, low price.

Preview this chapter:
Zoom in
Zoomout

Bacterial Y RNAs: Gates, Tethers, and tRNA Mimics, Page 1 of 2

| /docserver/preview/fulltext/10.1128/9781683670247/9781683670230_Chap21-1.gif /docserver/preview/fulltext/10.1128/9781683670247/9781683670230_Chap21-2.gif

Abstract:

In contrast to most bacterial noncoding RNAs (ncRNAs) ( ), Y RNAs were initially characterized in human cells and only later shown to exist in bacteria. The human RNAs were discovered because they are found complexed with the Ro 60-kDa autoantigen (Ro60), a ring-shaped protein that is a clinically important target of autoantibodies in patients with two systemic autoimmune rheumatic diseases, systemic lupus erythematosus and Sjögren’s syndrome ( ). Y RNAs and their Ro60 protein partner were subsequently shown to be present in all examined animal cells as well as in a subset of bacteria ( ). The number of distinct Y RNAs varies between species, with most characterized organisms having between two and four ( ). Although all experimentally verified Y RNAs are between 69 and 150 nucleotides, homology searches predict that some bacterial Y RNAs may exceed 200 nucleotides ( ).

Citation: Sim S, Wolin S. 2019. Bacterial Y RNAs: Gates, Tethers, and tRNA Mimics, p 369-381. In Storz G, Papenfort K (ed), Regulating with RNA in Bacteria and Archaea. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.RWR-0023-2018
Highlighted Text: Show | Hide
Loading full text...

Full text loading...

Figures

Image of Figure 1
Figure 1

Predicted secondary structures of a human Y RNA and the experimentally identified bacterial Y RNAs. (A) Human Y3 RNA. Modules involved in binding Ro60 and effector proteins are indicated. The portion of the stem containing the Ro60 binding site can form an alternative conformer containing a conserved bulged helix ( ). In the structure of Y3 complexed with Ro60 ( ), the bases shown in green (GGUCCGA) are sites of specific interactions with the Ro60 protein. (B, C) Yrn1 and Yrn2. The sequences that can form the conserved helix are boxed, and the conserved “metazoan motif” GGUCCGA is colored in green. An adenine nucleotide that may represent the second A in the “bacterial motif” is colored orange. On Yrn1, regions for Rsr binding and PNPase binding are indicated. (D, E) Typhimurium YrlA and YrlB. The GNCGAANG motif is in orange. (F, G) YrlA and YrlB. Nucleotides are colored as in panels D and E.

Citation: Sim S, Wolin S. 2019. Bacterial Y RNAs: Gates, Tethers, and tRNA Mimics, p 369-381. In Storz G, Papenfort K (ed), Regulating with RNA in Bacteria and Archaea. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.RWR-0023-2018
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of Figure 2
Figure 2

Structures of Ro60 and Rsr proteins. (A) A molecular surface representation of Ro60 (PDB ID: 1YVR) colored by electrostatic surface potential. (B) A molecular surface representation of Rsr (PDB ID: 2NVO) colored by electrostatic surface potential. For both panels A and B, positive potentials are in blue and negative potentials are in red (–10 kT/e to 10 kT/e). (C) Structure of Ro60 bound to a misfolded 5S rRNA fragment (PDB ID: 2I91). The helix binds the basic outer surface and the single-stranded 3′ end binds in the hole. (D) Structure of Ro60 bound to a fragment of Y RNA stem containing the conserved sequences required for Ro60 binding (PDB ID: 1YVP). Positions of the 5′ and 3′ ends are indicated. Biochemical studies support a model in which other portions of the Y RNA contact a basic platform that overlaps with the misfolded RNA-binding site (dashed line) ( ).

Citation: Sim S, Wolin S. 2019. Bacterial Y RNAs: Gates, Tethers, and tRNA Mimics, p 369-381. In Storz G, Papenfort K (ed), Regulating with RNA in Bacteria and Archaea. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.RWR-0023-2018
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of Figure 3
Figure 3

YrlA RNAs contain a module that resembles tRNA. (A) Typhimurium YrlA presented to resemble a canonical tRNA. Highly conserved nucleotides between YrlA orthologs are colored orange, while conserved purines and pyrimidines are in blue. Bases shown to be modified ( ) are indicated. AS, D, T, and V denote the acceptor stem, D arm, T arm, and variable arm, respectively. (B) tRNA-Ala-GCA. Nucleotides that are conserved between YrlA RNAs are in orange. All depicted tertiary interactions can potentially form in YrlA RNAs. (C) The genome-encoded sequence of YrlA drawn to emphasize the resemblance to tRNA. The structure of the acceptor stem after cleavage, end nibbling, and posttranscriptional CA addition ( ) is also shown (arrow). Conserved nucleotides are colored as in panel A. (D) Yrn1 presented to resemble tRNA. Nucleotides in the T arm that are conserved between Yrn1 and YrlA RNAs are colored as in panel A.

Citation: Sim S, Wolin S. 2019. Bacterial Y RNAs: Gates, Tethers, and tRNA Mimics, p 369-381. In Storz G, Papenfort K (ed), Regulating with RNA in Bacteria and Archaea. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.RWR-0023-2018
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of Figure 4
Figure 4

Phylogenetic trees of representative Rsr-containing bacterial species. (A) Phylogenetic tree based on the sequences of 16S rRNAs ( ). Each phylum is represented by a distinct color. (B) Phylogenetic tree based on the sequences of Rsr proteins. Sequence alignments were performed using Clustal Omega ( ), and trees were drawn with the Phylogeny Interference Package (PHYLIP) using the maximum likelihood method ( ).

Citation: Sim S, Wolin S. 2019. Bacterial Y RNAs: Gates, Tethers, and tRNA Mimics, p 369-381. In Storz G, Papenfort K (ed), Regulating with RNA in Bacteria and Archaea. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.RWR-0023-2018
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of Figure 5
Figure 5

Role of Yrn1 in scaffolding RYPER formation. (A) Yrn1, Rsr (PDB ID: 2NVO) (light blue), and PNPase (PDB ID: 1E3P) (pink). The Yrn1 modules that bind Rsr and PNPase are indicated. (B) The structure of RYPER predicted by single-particle electron microscopy and three-dimensional reconstruction ( ) (EMDB ID: 5389). The density that likely corresponds to Yrn1 is colored in yellow, while densities corresponding to Rsr and PNPase are colored as in panel A. A possible path for degrading a structured RNA substrate, in which the 3′ end threads from Rsr into the PNPase cavity for degradation, is depicted in blue.

Citation: Sim S, Wolin S. 2019. Bacterial Y RNAs: Gates, Tethers, and tRNA Mimics, p 369-381. In Storz G, Papenfort K (ed), Regulating with RNA in Bacteria and Archaea. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.RWR-0023-2018
Permissions and Reprints Request Permissions
Download as Powerpoint

References

/content/book/10.1128/9781683670247.chap21
1. Gottesman S,, Storz G . 2011. Bacterial small RNA regulators: versatile roles and rapidly evolving variations. Cold Spring Harb Perspect Biol 3 : a003798.[CrossRef][PubMed]
2. 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.[PubMed]
3. Clark G,, Reichlin M,, Tomasi TB Jr . 1969. Characterization of a soluble cytoplasmic antigen reactive with sera from patients with systemic lupus erythmatosus. J Immunol 102 : 117 122.[PubMed]
4. Lerner MR,, Boyle JA,, Hardin JA,, Steitz JA . 1981. Two novel classes of small ribonucleoproteins detected by antibodies associated with lupus erythematosus. Science 211 : 400 402.[PubMed]
5. Hendrick JP,, Wolin SL,, Rinke J,, Lerner MR,, Steitz JA . 1981. Ro small cytoplasmic ribonucleoproteins are a subclass of La ribonucleoproteins: further characterization of the Ro and La small ribonucleoproteins from uninfected mammalian cells. Mol Cell Biol 1 : 1138 1149.[PubMed]
6. Kato N,, Hoshino H,, Harada F . 1982. Nucleotide sequence of 4.5S RNA (C8 or hY5) from HeLa cells. Biochem Biophys Res Commun 108 : 363 370.[PubMed]
7. Wolin SL,, Steitz JA . 1983. Genes for two small cytoplasmic Ro RNAs are adjacent and appear to be single-copy in the human genome. Cell 32 : 735 744.[PubMed]
8. Reddy R,, Tan EM,, Henning D,, Nohga K,, Busch H . 1983. Detection of a nucleolar 7-2 ribonucleoprotein and a cytoplasmic 8-2 ribonucleoprotein with autoantibodies from patients with scleroderma. J Biol Chem 258 : 1383 1386.[PubMed]
9. Farris AD,, Gross JK,, Hanas JS,, Harley JB . 1996. Genes for murine Y1 and Y3 Ro RNAs have class 3 RNA polymerase III promoter structures and are unlinked on mouse chromosome 6. Gene 174 : 35 42.[PubMed]
10. Van Horn DJ,, Eisenberg D,, O’Brien CA,, Wolin SL . 1995. Caenorhabditis elegans embryos contain only one major species of Ro RNP. RNA 1 : 293 303.[PubMed]
11. Chen X,, Quinn AM,, Wolin SL . 2000. Ro ribonucleoproteins contribute to the resistance of Deinococcus radiodurans to ultraviolet irradiation. Genes Dev 14 : 777 782.[PubMed]
12. Chen X,, Taylor DW,, Fowler CC,, Galan JE,, Wang HW,, Wolin SL . 2013. An RNA degradation machine sculpted by Ro autoantigen and noncoding RNA. Cell 153 : 166 177.[PubMed]
13. Chen X,, Sim S,, Wurtmann EJ,, Feke A,, Wolin SL . 2014. Bacterial noncoding Y RNAs are widespread and mimic tRNAs. RNA 20 : 1715 1724.[PubMed]
14. Wolin SL,, Steitz JA . 1984. The Ro small cytoplasmic ribonucleoproteins: identification of the antigenic protein and its binding site on the Ro RNAs. Proc Natl Acad Sci U S A 81 : 1996 2000.
15. Pruijn GJM,, Slobbe RL,, van Venrooij WJ . 1991. Analysis of protein-RNA interactions within Ro ribonucleoprotein complexes. Nucleic Acids Res 19 : 5173 5180.[PubMed]
16. Green CD,, Long KS,, Shi H,, Wolin SL . 1998. Binding of the 60-kDa Ro autoantigen to Y RNAs: evidence for recognition in the major groove of a conserved helix. RNA 4 : 750 765.[PubMed]
17. Labbé JC,, Hekimi S,, Rokeach LA . 1999. The levels of the RoRNP-associated Y RNA are dependent upon the presence of ROP-1, the Caenorhabditis elegans Ro60 protein. Genetics 151 : 143 150.[PubMed]
18. Chen X,, Smith JD,, Shi H,, Yang DD,, Flavell RA,, Wolin SL . 2003. The Ro autoantigen binds misfolded U2 small nuclear RNAs and assists mammalian cell survival after UV irradiation. Curr Biol 13 : 2206 2211.[PubMed]
19. Xue D,, Shi H,, Smith JD,, Chen X,, Noe DA,, Cedervall T,, Yang DD,, Eynon E,, Brash DE,, Kashgarian M,, Flavell RA,, Wolin SL . 2003. A lupus-like syndrome develops in mice lacking the Ro 60-kDa protein, a major lupus autoantigen. Proc Natl Acad Sci U S A 100 : 7503 7508.[PubMed]
20. Wolin SL,, Belair C,, Boccitto M,, Chen X,, Sim S,, Taylor DW,, Wang HW . 2013. Non-coding Y RNAs as tethers and gates: insights from bacteria. RNA Biol 10 : 1602 1608.[PubMed]
21. O’Brien CA,, Harley JB . 1990. A subset of hY RNAs is associated with erythrocyte Ro ribonucleoproteins. EMBO J 9 : 3683 3689.[PubMed]
22. Perreault J,, Perreault JP,, Boire G . 2007. Ro-associated Y RNAs in metazoans: evolution and diversification. Mol Biol Evol 24 : 1678 1689.[PubMed]
23. Mosig A,, Guofeng M,, Stadler BM,, Stadler PF . 2007. Evolution of the vertebrate Y RNA cluster. Theory Biosci 126 : 9 14.[PubMed]
24. Bateman A,, Kickhoefer V . 2003. The TROVE module: a common element in Telomerase, Ro and Vault ribonucleoproteins. BMC Bioinformatics 4 : 49.[CrossRef][PubMed]
25. Stein AJ,, Fuchs G,, Fu C,, Wolin SL,, Reinisch KM . 2005. Structural insights into RNA quality control: the Ro autoantigen binds misfolded RNAs via its central cavity. Cell 121 : 529 539.[PubMed]
26. Ramesh A,, Savva CG,, Holzenburg A,, Sacchettini JC . 2007. Crystal structure of Rsr, an ortholog of the antigenic Ro protein, links conformational flexibility to RNA binding activity. J Biol Chem 282 : 14960 14967.[PubMed]
27. O’Brien CA,, Wolin SL . 1994. A possible role for the 60-kD Ro autoantigen in a discard pathway for defective 5S rRNA precursors. Genes Dev 8 : 2891 2903.[PubMed]
28. Shi H,, O’Brien CA,, Van Horn DJ,, Wolin SL . 1996. A misfolded form of 5S rRNA is complexed with the Ro and La autoantigens. RNA 2 : 769 784.[PubMed]
29. Fuchs G,, Stein AJ,, Fu C,, Reinisch KM,, Wolin SL . 2006. Structural and biochemical basis for misfolded RNA recognition by the Ro autoantigen. Nat Struct Mol Biol 13 : 1002 1009.[PubMed]
30. Chen X,, Wurtmann EJ,, Van Batavia J,, Zybailov B,, Washburn MP,, Wolin SL . 2007. An ortholog of the Ro autoantigen functions in 23S rRNA maturation in D. radiodurans. Genes Dev 21 : 1328 1339.[PubMed]
31. Sim S,, Weinberg DE,, Fuchs G,, Choi K,, Chung J,, Wolin SL . 2009. The subcellular distribution of an RNA quality control protein, the Ro autoantigen, is regulated by noncoding Y RNA binding. Mol Biol Cell 20 : 1555 1564.[PubMed]
32. Sim S,, Yao J,, Weinberg DE,, Niessen S,, Yates JR III,, Wolin SL . 2012. The zipcode-binding protein ZBP1 influences the subcellular location of the Ro 60-kDa autoantigen and the noncoding Y3 RNA. RNA 18 : 100 110.[PubMed]
33. Christov CP,, Gardiner TJ,, Szüts D,, Krude T . 2006. Functional requirement of noncoding Y RNAs for human chromosomal DNA replication. Mol Cell Biol 26 : 6993 7004.[PubMed]
34. Collart C,, Christov CP,, Smith JC,, Krude T . 2011. The midblastula transition defines the onset of Y RNA-dependent DNA replication in Xenopus laevis. Mol Cell Biol 31 : 3857 3870.[PubMed]
35. White O,, Eisen JA,, Heidelberg JF,, Hickey EK,, Peterson JD,, Dodson RJ,, Haft DH,, Gwinn ML,, Nelson WC,, Richardson DL,, Moffat KS,, Qin H,, Jiang L,, Pamphile W,, Crosby M,, Shen M,, Vamathevan JJ,, Lam P,, McDonald L,, Utterback T,, Zalewski C,, Makarova KS,, Aravind L,, Daly MJ,, Minton KW,, Fleischmann RD,, Ketchum KA,, Nelson KE,, Salzberg S,, Smith HO,, Venter JC,, Fraser CM . 1999. Genome sequence of the radioresistant bacterium Deinococcus radiodurans R1. Science 286 : 1571 1577.[PubMed]
36. Cox MM,, Battista JR . 2005. Deinococcus radiodurans—the consummate survivor. Nat Rev Microbiol 3 : 882 892.[PubMed]
37. Slade D,, Radman M . 2011. Oxidative stress resistance in Deinococcus radiodurans. Microbiol Mol Biol Rev 75 : 133 191.[PubMed]
38. Sim S,, Wolin SL . 2011. Emerging roles for the Ro 60-kDa autoantigen in noncoding RNA metabolism. Wiley Interdiscip Rev RNA 2 : 686 699.[PubMed]
39. Pedulla ML,, Ford ME,, Houtz JM,, Karthikeyan T,, Wadsworth C,, Lewis JA,, Jacobs-Sera D,, Falbo J,, Gross J,, Pannunzio NR,, Brucker W,, Kumar V,, Kandasamy J,, Keenan L,, Bardarov S,, Kriakov J,, Lawrence JG,, Jacobs WR Jr,, Hendrix RW,, Hatfull GF . 2003. Origins of highly mosaic mycobacteriophage genomes. Cell 113 : 171 182.
40. Nawrocki EP,, Eddy SR . 2013. Infernal 1.1: 100-fold faster RNA homology searches. Bioinformatics 29 : 2933 2935.[PubMed]
41. Burroughs AM,, Aravind L . 2016. RNA damage in biological conflicts and the diversity of responding RNA repair systems. Nucleic Acids Res 44 : 8525 8555.[PubMed]
42. Greiling TM,, Dehner C,, Chen X,, Hughes K,, Iñiguez AJ,, Boccitto M,, Zegarra Ruiz D,, Renfroe SC,, Vieira SM,, Ruff WE,, Sim S,, Kriegel C,, Glanternik J,, Chen X,, Girardi M,, Degnan P,, Costenbader KH,, Goodman AL,, Wolin SL,, Kriegel MA . Commensal orthologs of the human autoantigen Ro60 as triggers of autoimmunity in lupus. Sci Transl Med 10 : eaan2306.[CrossRef][PubMed]
43. Gwizdek C,, Ossareh-Nazari B,, Brownawell AM,, Doglio A,, Bertrand E,, Macara IG,, Dargemont C . 2003. Exportin-5 mediates nuclear export of minihelix-containing RNAs. J Biol Chem 278 : 5505 5508.[PubMed]
44. Teunissen SW,, Kruithof MJ,, Farris AD,, Harley JB,, Venrooij WJ,, Pruijn GJ . 2000. Conserved features of Y RNAs: a comparison of experimentally derived secondary structures. Nucleic Acids Res 28 : 610 619.[PubMed]
45. Bouffard P,, Barbar E,, Brière F,, Boire G . 2000. Interaction cloning and characterization of RoBPI, a novel protein binding to human Ro ribonucleoproteins. RNA 6 : 66 78.[PubMed]
46. Fabini G,, Raijmakers R,, Hayer S,, Fouraux MA,, Pruijn GJ,, Steiner G . 2001. The heterogeneous nuclear ribonucleoproteins I and K interact with a subset of the Ro ribonucleoprotein-associated Y RNAs in vitro and in vivo. J Biol Chem 276 : 20711 20718.[PubMed]
47. Fouraux MA,, Bouvet P,, Verkaart S,, van Venrooij WJ,, Pruijn GJ . 2002. Nucleolin associates with a subset of the human Ro ribonucleoprotein complexes. J Mol Biol 320 : 475 488.[PubMed]
48. Hogg JR,, Collins K . 2007. Human Y5 RNA specializes a Ro ribonucleoprotein for 5S ribosomal RNA quality control. Genes Dev 21 : 3067 3072.[PubMed]
49. Köhn M,, Lederer M,, Wächter K,, Hüttelmaier S . 2010. Near-infrared (NIR) dye-labeled RNAs identify binding of ZBP1 to the noncoding Y3-RNA. RNA 16 : 1420 1428.[PubMed]
50. Symmons MF,, Jones GH,, Luisi BF . 2000. A duplicated fold is the structural basis for polynucleotide phosphorylase catalytic activity, processivity, and regulation. Structure 8 : 1215 1226.
51. Chan CW,, Chetnani B,, Mondragón A . 2013. Structure and function of the T-loop structural motif in noncoding RNAs. Wiley Interdiscip Rev RNA 4 : 507 522.[PubMed]
52. Altman S,, Kirsebom L,, Talbot S . 1993. Recent studies of ribonuclease P. FASEB J 7 : 7 14.[PubMed]
53. Wurtmann EJ,, Wolin SL . 2010. A role for a bacterial ortholog of the Ro autoantigen in starvation-induced rRNA degradation. Proc Natl Acad Sci U S A 107 : 4022 4027.[PubMed]
54. Tanaka M,, Earl AM,, Howell HA,, Park MJ,, Eisen JA,, Peterson SN,, Battista JR . 2004. Analysis of Deinococcus radiodurans’s transcriptional response to ionizing radiation and desiccation reveals novel proteins that contribute to extreme radioresistance. Genetics 168 : 21 33.[PubMed]
55. Labbé JC,, Burgess J,, Rokeach LA,, Hekimi S . 2000. ROP-1, an RNA quality-control pathway component, affects Caenorhabditis elegans dauer formation. Proc Natl Acad Sci U S A 97 : 13233 13238.[PubMed]
56. Evguenieva-Hackenberg E,, Hou L,, Glaeser S,, Klug G . 2014. Structure and function of the archaeal exosome. Wiley Interdiscip Rev RNA 5 : 623 635.[PubMed]
57. Zinder JC,, Lima CD . 2017. Targeting RNA for processing or destruction by the eukaryotic RNA exosome and its cofactors. Genes Dev 31 : 88 100.[PubMed]
58. Bonneau F,, Basquin J,, Ebert J,, Lorentzen E,, Conti E . 2009. The yeast exosome functions as a macromolecular cage to channel RNA substrates for degradation. Cell 139 : 547 559.[PubMed]
59. Górna MW,, Carpousis AJ,, Luisi BF . 2012. From conformational chaos to robust regulation: the structure and function of the multi-enzyme RNA degradosome. Q Rev Biophys 45 : 105 145.[PubMed]
60. Viegas SC,, Pfeiffer V,, Sittka A,, Silva IJ,, Vogel J,, Arraiano CM . 2007. Characterization of the role of ribonucleases in Salmonella small RNA decay. Nucleic Acids Res 35 : 7651 7664.[PubMed]
61. Englert M,, Sheppard K,, Aslanian A,, Yates JR III,, Söll D . 2011. Archaeal 3′-phosphate RNA splicing ligase characterization identifies the missing component in tRNA maturation. Proc Natl Acad Sci U S A 108 : 1290 1295.[PubMed]
62. Popow J,, Englert M,, Weitzer S,, Schleiffer A,, Mierzwa B,, Mechtler K,, Trowitzsch S,, Will CL,, Lührmann R,, Söll D,, Martinez J . 2011. HSPC117 is the essential subunit of a human tRNA splicing ligase complex. Science 331 : 760 764.[PubMed]
63. Kosmaczewski SG,, Edwards TJ,, Han SM,, Eckwahl MJ,, Meyer BI,, Peach S,, Hesselberth JR,, Wolin SL,, Hammarlund M . 2014. The RtcB RNA ligase is an essential component of the metazoan unfolded protein response. EMBO Rep 15 : 1278 1285.[PubMed]
64. Temmel H,, Müller C,, Sauert M,, Vesper O,, Reiss A,, Popow J,, Martinez J,, Moll I . 2017. The RNA ligase RtcB reverses MazF-induced ribosome heterogeneity in Escherichia coli. Nucleic Acids Res 45 : 4708 4721.[PubMed]
65. Hartman CE,, Samuels DJ,, Karls AC . 2016. Modulating Salmonella Typhimurium’s response to a changing environment through bacterial enhancer-binding proteins and the RpoN regulon. Front Mol Biosci 3 : 41.[CrossRef][PubMed]
66. Westermann AJ,, Förstner KU,, Amman F,, Barquist L,, Chao Y,, Schulte LN,, Müller L,, Reinhardt R,, Stadler PF,, Vogel J . 2016. Dual RNA-seq unveils noncoding RNA functions in host-pathogen interactions. Nature 529 : 496 501.[PubMed]
67. Das U,, Shuman S . 2013. 2′-Phosphate cyclase activity of RtcA: a potential rationale for the operon organization of RtcA with an RNA repair ligase RtcB in Escherichia coli and other bacterial taxa. RNA 19 : 1355 1362.[PubMed]
68. Popow J,, Jurkin J,, Schleiffer A,, Martinez J . 2014. Analysis of orthologous groups reveals archease and DDX1 as tRNA splicing factors. Nature 511 : 104 107.[PubMed]
69. Desai KK,, Cheng CL,, Bingman CA,, Phillips GN Jr,, Raines RT . 2014. A tRNA splicing operon: archease endows RtcB with dual GTP/ATP cofactor specificity and accelerates RNA ligation. Nucleic Acids Res 42 : 3931 3942.[PubMed]
70. Quast C,, Pruesse E,, Yilmaz P,, Gerken J,, Schweer T,, Yarza P,, Peplies J,, Glöckner FO . 2013. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res 41( Database issue) : D590 D596.[PubMed]
71. Sievers F,, Wilm A,, Dineen D,, Gibson TJ,, Karplus K,, Li W,, Lopez R,, McWilliam H,, Remmert M,, Söding J,, Thompson JD,, Higgins DG . 2011. Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol Syst Biol 7 : 539.[CrossRef][PubMed]
72. Felsenstein J . 1989. PHYLIP—Phylogeny Interference Package (Version 3.2). Cladistics 5 : 164 166.

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