1887

Abstract

Poly(A) polymerases (PAPs) and tRNA nucleotidyltransferases belong to a superfamily of nucleotidyltransferases and modify RNA 3′-ends. The product of the gene, PAP I, has been characterized in a few β-, γ- and δ-. Using the PAP I signature sequence, putative PAPs were identified in bacterial species from the α- and ε- and from four other bacterial phyla (, , and ). Phylogenetic analysis, alien index and G+C content calculations strongly suggest that the PAPs in the species identified in this study arose by horizontal gene transfer from the β- and γ-.

  • This is an open-access article distributed under the terms of the Creative Commons Attribution License.
Loading

Article metrics loading...

/content/journal/mgen/10.1099/mgen.0.000508
2021-01-27
2024-04-19
Loading full text...

Full text loading...

/deliver/fulltext/mgen/7/2/mgen000508.html?itemId=/content/journal/mgen/10.1099/mgen.0.000508&mimeType=html&fmt=ahah

References

  1. Jones GH. Phylogeny and evolution of RNA 3'-nucleotidyltransferases in bacteria. J Mol Evol 2019; 87:254–270 [View Article][PubMed]
    [Google Scholar]
  2. Sarkar N. Polyadenylation of mRNA in bacteria. Microbiology 1996; 142:3125–3133 [View Article][PubMed]
    [Google Scholar]
  3. Sarkar N. Polyadenylation of mRNA in prokaryotes. Annu Rev Biochem 1997; 66:173–197 [View Article][PubMed]
    [Google Scholar]
  4. Liu JD, Parkinson JS. Genetics and sequence analysis of the pcnB locus, an Escherichia coli gene involved in plasmid copy number control. J Bacteriol 1989; 171:1254–1261 [View Article][PubMed]
    [Google Scholar]
  5. Cao GJ, Sarkar N. Identification of the gene for an Escherichia coli poly(A) polymerase. Proc Natl Acad Sci USA 1992; 89:10380–10384 [View Article][PubMed]
    [Google Scholar]
  6. Joanny G, Le Derout J, Bréchemier-Baey D, Labas V, Vinh J et al. Polyadenylation of a functional mRNA controls gene expression in Escherichia coli . Nucleic Acids Res 2007; 35:2494–2502 [View Article][PubMed]
    [Google Scholar]
  7. Maes A, Gracia C, Bréchemier D, Hamman P, Chatre E et al. Role of polyadenylation in regulation of the flagella cascade and motility in Escherichia coli . Biochimie 2013; 95:410–418 [View Article][PubMed]
    [Google Scholar]
  8. He L, Söderbom F, Wagner EG, Binnie U, Binns N et al. PcnB is required for the rapid degradation of RNAI, the antisense RNA that controls the copy number of ColE1-related plasmids. Mol Microbiol 1993; 9:1131–1142 [View Article][PubMed]
    [Google Scholar]
  9. Maes A, Gracia C, Hajnsdorf E, Régnier P. Search for poly(A) polymerase targets in E. coli reveals its implication in surveillance of Glu tRNA processing and degradation of stable RNAs. Mol Microbiol 2012; 83:436–451 [View Article][PubMed]
    [Google Scholar]
  10. Li Z, Reimers S, Pandit S, Deutscher MP. RNA quality control: degradation of defective transfer RNA. EMBO J 2002; 21:1132–1138 [View Article][PubMed]
    [Google Scholar]
  11. Mohanty BK, Maples VF, Kushner SR. Polyadenylation helps regulate functional tRNA levels in Escherichia coli . Nucleic Acids Res 2012; 40:4589–4603 [View Article][PubMed]
    [Google Scholar]
  12. Mohanty BK, Kushner SR. Bacterial/archaeal/organellar polyadenylation. Wiley Interdiscip Rev RNA 2011; 2:256–276 [View Article][PubMed]
    [Google Scholar]
  13. Yue D, Maizels N, Weiner AM. CCA-adding enzymes and poly(A) polymerases are all members of the same nucleotidyltransferase superfamily: characterization of the CCA-adding enzyme from the archaeal hyperthermophile Sulfolobus shibatae . RNA 1996; 2:895–908[PubMed]
    [Google Scholar]
  14. Bralley P, Jones GH. cDNA cloning confirms the polyadenylation of RNA decay intermediates in Streptomyces coelicolor . Microbiology 2002; 148:1421–1425 [View Article][PubMed]
    [Google Scholar]
  15. Bralley P, Gust B, Chang S, Chater KF, Jones GH. RNA 3'-tail synthesis in Streptomyces: in vitro and in vivo activities of RNase PH, the SCO3896 gene product and polynucleotide phosphorylase. Microbiology 2006; 152:627–636 [View Article][PubMed]
    [Google Scholar]
  16. Sohlberg B, Huang J, Cohen SN. The Streptomyces coelicolor polynucleotide phosphorylase homologue, and not the putative poly(A) polymerase, can polyadenylate RNA. J Bacteriol 2003; 185:7273–7278 [View Article][PubMed]
    [Google Scholar]
  17. Rott R, Zipor G, Portnoy V, Liveanu V, Schuster G. RNA polyadenylation and degradation in cyanobacteria are similar to the chloroplast but different from Escherichia coli . J Biol Chem 2003; 278:15771–15777 [View Article][PubMed]
    [Google Scholar]
  18. Yehudai-Resheff S, Hirsh M, Schuster G. Polynucleotide phosphorylase functions as both an exonuclease and a poly(A) polymerase in spinach chloroplasts. Mol Cell Biol 2001; 21:5408–5416 [View Article][PubMed]
    [Google Scholar]
  19. Mohanty BK, Kushner SR. Polynucleotide phosphorylase functions both as a 3'→5' exonuclease and a poly(A) polymerase in Escherichia coli . Proc Natl Acad Sci USA 2000; 97:11966–11971 [View Article][PubMed]
    [Google Scholar]
  20. Bralley P, Cozad M, Jones GH. Geobacter sulfurreducens contains separate C- and A-adding tRNA nucleotidyltransferases and a poly(A) polymerase. J Bacteriol 2009; 191:109–114 [View Article][PubMed]
    [Google Scholar]
  21. Raynal LC, Krisch HM, Carpousis AJ. The Bacillus subtilis nucleotidyltransferase is a tRNA CCA-adding enzyme. J Bacteriol 1998; 180:6276–6282 [View Article][PubMed]
    [Google Scholar]
  22. Campos-Guillén J, Bralley P, Jones GH, Bechhofer DH, Olmedo-Alvarez G. Addition of poly(A) and heteropolymeric 3' ends in Bacillus subtilis wild-type and PNPase-deficient strains. J Bacteriol 2005; 187:4698–4706 [View Article][PubMed]
    [Google Scholar]
  23. Moretti S, Armougom F, Wallace IM, Higgins DG, Jongeneel CV et al. The M-Coffee web server: a meta-method for computing multiple sequence alignments by combining alternative alignment methods. Nucleic Acids Res 2007; 35:W645–W648 [View Article][PubMed]
    [Google Scholar]
  24. Wallace IM, O'Sullivan O, Higgins DG, Notredame C. M-Coffee: combining multiple sequence alignment methods with T-Coffee. Nucleic Acids Res 2006; 34:1692–1699 [View Article][PubMed]
    [Google Scholar]
  25. Felsenstein J. PHYLIP - phylogeny inference package (version 3.2). Cladistics 1989; 5:164–166
    [Google Scholar]
  26. Jones DT, Taylor WR, Thornton JM. The rapid generation of mutation data matrices from protein sequences. Comput Appl Biosci 1992; 8:275–282 [View Article][PubMed]
    [Google Scholar]
  27. Hofreiter M, Serre D, Rohland N, Rabeder G, Nagel D et al. Lack of phylogeography in European mammals before the last glaciation. Proc Natl Acad Sci USA 2004; 101:12963–12968 [View Article][PubMed]
    [Google Scholar]
  28. Rancurel C, Legrand L, Danchin EGJ. Alienness: rapid detection of candidate horizontal gene transfers across the tree of life. Genes 2017; 8:248–261 [View Article][PubMed]
    [Google Scholar]
  29. Leplae R, Hebrant A, Wodak SJ, Toussaint A. ACLAME: A CLAssification of Mobile genetic Elements.. Nucleic Acids Res 2004; 32:D45–D49 [View Article][PubMed]
    [Google Scholar]
  30. Leplae R, Lima-Mendez G, Toussaint A. ACLAME: A CLAssification of Mobile genetic Elements, update 2010. Nucleic Acids Res 2010; 38:D57–D61 [View Article][PubMed]
    [Google Scholar]
  31. Martin G, Keller W. Sequence motifs that distinguish ATP(CTP):tRNA nucleotidyl transferases from eubacterial poly(A) polymerases. RNA 2004; 10:899–906 [View Article][PubMed]
    [Google Scholar]
  32. Toh Y, Takeshita D, Nagaike T, Numata T, Tomita K. Mechanism for the alteration of the substrate specificities of template-independent RNA polymerases. Structure 2011; 19:232–243 [View Article][PubMed]
    [Google Scholar]
  33. Zhang X-X, Liu Y-H, Rainey PB. CbrAB-dependent regulation of pcnB, a poly(A) polymerase gene involved in polyadenylation of RNA in Pseudomonas fluorescens . Environ Microbiol 2010; 12:1674–1683 [View Article][PubMed]
    [Google Scholar]
  34. Toh Y, Takeshita D, Numata T, Fukai S, Nureki O et al. Mechanism for the definition of elongation and termination by the class II CCA-adding enzyme. EMBO J 2009; 28:3353–3365 [View Article][PubMed]
    [Google Scholar]
  35. Schulz F, Eloe-Fadrosh EA, Bowers RM, Jarett J, Nielsen T et al. Towards a balanced view of the bacterial tree of life. Microbiome 2017; 5:140–145 [View Article][PubMed]
    [Google Scholar]
  36. Gupta RS. Impact of genomics on the understanding of microbial evolution and classification: the importance of Darwin's views on classification. FEMS Microbiol Rev 2016; 40:520–553 [View Article][PubMed]
    [Google Scholar]
  37. Bocchetta M, Gribaldo S, Sanangelantoni A, Cammarano P. Phylogenetic depth of the bacterial genera Aquifex and Thermotoga inferred from analysis of ribosomal protein, elongation factor, and RNA polymerase subunit sequences. J Mol Evol 2000; 50:366–380 [View Article][PubMed]
    [Google Scholar]
  38. Wolf YI, Rogozin IB, Grishin NV, Koonin EV. Genome trees and the tree of life. Trends Genet 2002; 18:472–479 [View Article][PubMed]
    [Google Scholar]
  39. Cho HD, Verlinde CLMJ, Weiner AM. Reengineering CCA-adding enzymes to function as (U,G)- or dCdCdA-adding enzymes or poly(C,A) and poly(U,G) polymerases. Proc Natl Acad Sci USA 2007; 104:54–59 [View Article][PubMed]
    [Google Scholar]
  40. Betat H, Rammelt C, Martin G, Mörl M. Exchange of regions between bacterial poly(A) polymerase and the CCA-adding enzyme generates altered specificities. Mol Cell 2004; 15:389–398 [View Article][PubMed]
    [Google Scholar]
  41. Gladyshev EA, Meselson M, Arkhipova IR. Massive horizontal gene transfer in bdelloid rotifers. Science 2008; 320:1210–1213 [View Article][PubMed]
    [Google Scholar]
  42. Ku C, Martin WF. A natural barrier to lateral gene transfer from prokaryotes to eukaryotes revealed from genomes: the 70 % rule. BMC Biol 2016; 14:89–100 [View Article][PubMed]
    [Google Scholar]
  43. Koski LB, Golding GB. The closest BLAST hit is often not the nearest neighbor. J Mol Evol 2001; 52:540–542 [View Article][PubMed]
    [Google Scholar]
  44. Sokhi UK, DeSalle R, Bacolod MD, Das SK, Dasgupta S et al. Evolutionary dynamics of polynucelotide phosphorylases. Mol Phylogenet Evol 2014; 73:77–86 [View Article][PubMed]
    [Google Scholar]
  45. Daubin V, Lerat E, Perrière G. The source of laterally transferred genes in bacterial genomes. Genome Biol 2003; 4:R57 [View Article][PubMed]
    [Google Scholar]
  46. Cortez D, Delaye L, Lazcano A, Becerra A. Composition-based methods to identify horizontal gene transfer. Methods Mol Biol 2009; 532:215–225 [View Article][PubMed]
    [Google Scholar]
  47. Ravenhall M, Škunca N, Lassalle F, Dessimoz C. Inferring horizontal gene transfer. PLoS Comput Biol 2015; 11:e1004095 [View Article][PubMed]
    [Google Scholar]
  48. Siefert JL. Defining the mobilome. Methods Mol Biol 2009; 532:13–27 [View Article][PubMed]
    [Google Scholar]
  49. Carr VR, Shkoporov A, Hill C, Mullany P, Moyes DL. Probing the mobilome: discoveries in the dynamic microbiome. Trends Microbiol 2020 11 May 2020 [View Article][PubMed]
    [Google Scholar]
  50. Mohanty BK, Kushner SR. Analysis of the function of Escherichia coli poly(A) polymerase I in RNA metabolism. Mol Microbiol 1999; 34:1094–1108 [View Article][PubMed]
    [Google Scholar]
  51. Yehudai-Resheff S, Schuster G. Characterization of the E. coli poly(A) polymerase: nucleotide specificity, RNA-binding affinities and RNA structure dependence. Nucleic Acids Res 2000; 28:1139–1144 [View Article][PubMed]
    [Google Scholar]
  52. Albrecht M, Sharma CM, Dittrich MT, Müller T, Reinhardt R et al. The transcriptional landscape of Chlamydia pneumoniae . Genome Biol 2011; 12:R98 [View Article][PubMed]
    [Google Scholar]
  53. Caimano MJ, Sivasankaran SK, Allard A, Hurley D, Hokamp K et al. A model system for studying the transcriptomic and physiological changes associated with mammalian host-adaptation by Leptospira interrogans serovar Copenhageni. PLoS Pathog 2014; 10:e1004004 [View Article][PubMed]
    [Google Scholar]
  54. Williams KP, Gillespie JJ, Sobral BWS, Nordberg EK, Snyder EE et al. Phylogeny of gammaproteobacteria. J Bacteriol 2010; 192:2305–2314 [View Article][PubMed]
    [Google Scholar]
  55. Luo Y, Fu C, Zhang D-Y, Lin K. Overlapping genes as rare genomic markers: the phylogeny of gamma-Proteobacteria as a case study. Trends Genet 2006; 22:593–596 [View Article][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/mgen/10.1099/mgen.0.000508
Loading
/content/journal/mgen/10.1099/mgen.0.000508
Loading

Data & Media loading...

Supplements

Supplementary material 1

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