Different polyamine pathways from bacteria have replaced eukaryotic spermidine biosynthesis in ciliates Tetrahymena thermophila and Paramecium tetaurelia

Molecular Microbiology

Volumn 97, Issue 5, 2015, Pages 791-807

  Li, Bin ^a   Kim, Sok Ho ^a   Zhang, Yang ^b   Hanfrey, Colin C ^c,d   Elliott, Katherine A ^c   Ealick, Steven E ^b   Michael, Anthony J ^a  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^b Department of Obstetrics Gynecology   (United States)

^c INSTITUTE OF FOOD RESEARCH   (United Kingdom)

^d Bury St Edmunds County Upper School   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSYLMETHIONINE DECARBOXYLASE; AMINOPROPYLCADAVERINE; BACTERIAL PROTEIN; CADAVERINE; DEOXYHYPUSINE SYNTHASE; HYBRID PROTEIN; POLYAMINE; SPERMIDINE; SPERMIDINE SYNTHASE; UNCLASSIFIED DRUG; HOMOSPERMIDINE SYNTHETASE; N-(3-AMINOPROPYL)CADAVERINE; NORSPERMIDINE; OXIDOREDUCTASE; TRANSFERASE;

ARTICLE; CILIATE; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME STRUCTURE; ENZYME SYNTHESIS; EUKARYOTE; FUNGAL STRAIN; FUNGUS GROWTH; GENETIC CODE; NONHUMAN; PARALOGY; PARAMECIUM TETRAURELIA; PRIORITY JOURNAL; SCHISTOSOMA; SIGNAL TRANSDUCTION; TETRAHYMENA THERMOPHILA; AMINO ACID SEQUENCE; ANALOGS AND DERIVATIVES; ANIMAL; BIOSYNTHESIS; CHEMICAL STRUCTURE; CHEMISTRY; DRUG EFFECTS; GENE FUSION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MOLECULAR GENETICS; PARAMECIUM; PROTEIN PROCESSING; SEQUENCE ALIGNMENT; YEAST;

BACTERIA (MICROORGANISMS); CILIOPHORA; EUKARYOTA; METAZOA; PARAMECIUM; SACCHAROMYCETALES; SCHISTOSOMA; TETRAHYMENA; TETRAHYMENA THERMOPHILA;

ADENOSYLMETHIONINE DECARBOXYLASE; ALKYL AND ARYL TRANSFERASES; AMINO ACID SEQUENCE; ANIMALS; BIOSYNTHETIC PATHWAYS; CADAVERINE; EUKARYOTA; GENE FUSION; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; OXIDOREDUCTASES ACTING ON CH-NH GROUP DONORS; PARAMECIUM; POLYAMINES; PROTEIN PROCESSING, POST-TRANSLATIONAL; SCHISTOSOMA; SEQUENCE ALIGNMENT; SPERMIDINE; SPERMIDINE SYNTHASE; TETRAHYMENA THERMOPHILA; YEASTS;

EID: 84940467133     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/mmi.13066     Document Type: Article

References (58)

1. Albers, E. (2009) Metabolic characteristics and importance of the universal methionine salvage pathway recycling methionine from 5′-methylthioadenosine. IUBMB Life 61: 1132-1142.
2. Aury, J.M., Jaillon, O., Duret, L., Noel, B., Jubin, C., Porcel, B.M., etal. (2006) Global trends of whole-genome duplications revealed by the ciliate Paramecium tetraurelia. Nature 444: 171-178.
3. Balasundaram, D., Dinman, J.D., Tabor, C.W., and Tabor, H. (1994) SPE1 and SPE2: two essential genes in the biosynthesis of polyamines that modulate +1 ribosomal frameshifting in Saccharomyces cerevisiae. J Bacteriol 176: 7126-7128.
4. Bale, S., and Ealick, S.E. (2010) Structural biology of S-adenosylmethionine decarboxylase. Amino Acids 38: 451-460.
5. Bale, S., Baba, K., McCloskey, D.E., Pegg, A.E., and Ealick, S.E. (2010) Complexes of Thermotoga maritima S-adenosylmethionine decarboxylase provide insights into substrate specificity. Acta Crystallogr D Biol Crystallogr 66: 181-189.
6. Burrell, M., Hanfrey, C.C., Murray, E.J., Stanley-Wall, N.R., and Michael, A.J. (2010) Evolution and multiplicity of arginine decarboxylases in polyamine biosynthesis and essential role in Bacillus subtilis biofilm formation. J Biol Chem 285: 39224-39238.
7. Chattopadhyay, M.K., Murakami, Y., and Matsufuji, S. (2001) Antizyme regulates the degradation of ornithine decarboxylase in fission yeast Schizosaccharomyces pombe. Study in the spe2 knockout strains. J Biol Chem 276: 21235-21241.
8. Chawla, B., Jhingran, A., Singh, S., Tyagi, N., Park, M.H., Srinivasan, N., etal. (2010) Identification and characterization of a novel deoxyhypusine synthase in Leishmania donovani. J Biol Chem 285: 453-463.
9. Coyne, R.S., Thiagarajan, M., Jones, K.M., Wortman, J.R., Tallon, L.J., Haas, B.J., etal. (2008) Refined annotation and assembly of the Tetrahymena thermophila genome sequence through EST analysis, comparative genomic hybridization, and targeted gap closure. BMC Genomics 9: 562.
10. Dever, T.E., Gutierrez, E., and Shin, B.S. (2014) The hypusine-containing translation factor eIF5A. Crit Rev Biochem Mol Biol 49: 413-425.
11. Eisen, J.A., Coyne, R.S., Wu, M., Wu, D., Thiagarajan, M., Wortman, J.R., etal. (2006) Macronuclear genome sequence of the ciliate Tetrahymena thermophila, a model eukaryote. PLoS Biol 4: e286.
12. Emsley, P., and Cowtan, K. (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr D Biol Crystallogr 60: 2126-2132.
13. Fuell, C., Elliott, K.A., Hanfrey, C.C., Franceschetti, M., and Michael, A.J. (2010) Polyamine biosynthetic diversity in plants and algae. Plant Physiol Biochem 48: 513-520.
14. Gogendeau, D., Beisson, J., de Loubresse, N.G., Le Caer, J.P., Ruiz, F., Cohen, J., etal. (2007) An Sfi1p-like centrin-binding protein mediates centrin-based Ca2+ -dependent contractility in Paramecium tetraurelia. Eukaryot Cell 6: 1992-2000.
15. Green, R., Hanfrey, C.C., Elliott, K.A., McCloskey, D.E., Wang, X., Kanugula, S., etal. (2011) Independent evolutionary origins of functional polyamine biosynthetic enzyme fusions catalysing de novo diamine to triamine formation. Mol Microbiol 81: 1109-1124.
16. Hamasaki-Katagiri, N., Katagiri, Y., Tabor, C.W., and Tabor, H. (1998) Spermine is not essential for growth of Saccharomyces cerevisiae: identification of the SPE4 gene (spermine synthase) and characterization of a spe4 deletion mutant. Gene 210: 195-201.
17. Imai, A., Matsuyama, T., Hanzawa, Y., Akiyama, T., Tamaoki, M., Saji, H., etal. (2004) Spermidine synthase genes are essential for survival of Arabidopsis. Plant Physiol 135: 1565-1573.
18. Kaiser, A., Vollmert, M., Tholl, D., Graves, M.V., Gurnon, J.R., Xing, W., etal. (1999) Chlorella virus PBCV-1 encodes a functional homospermidine synthase. Virology 263: 254-262.
19. Kim, A.D., Graham, D.E., Seeholzer, S.H., and Markham, G.D. (2000) S-Adenosylmethionine decarboxylase from the archaeon Methanococcus jannaschii: identification of a novel family of pyruvoyl enzymes. J Bacteriol 182: 6667-6672.
20. Knight, R.D., Freeland, S.J., and Landweber, L.F. (2001) Rewiring the keyboard: evolvability of the genetic code. Nat Rev Genet 2: 49-58.
21. Koonin, E.V. (2014) Bacterial genes in eukaryotes: relatively rare but real and important (Comment on DOI 10.1002/bies.201300095). Bioessays 36: 8.
22. Korolev, S., Ikeguchi, Y., Skarina, T., Beasley, S., Arrowsmith, C., Edwards, A., etal. (2002) The crystal structure of spermidine synthase with a multisubstrate adduct inhibitor. Nat Struct Biol 9: 27-31.
23. Krzywicka, A., Beisson, J., Keller, A.M., Cohen, J., Jerka-Dziadosz, M., and Klotz, C. (2001) KIN241: a gene involved in cell morphogenesis in Paramecium tetraurelia reveals a novel protein family of cyclophilin-RNA interacting proteins (CRIPs) conserved from fission yeast to man. Mol Microbiol 42: 257-267.
24. Li, Y.F., Hess, S., Pannell, L.K., White Tabor, C., and Tabor, H. (2001) In vivo mechanism-based inactivation of S-adenosylmethionine decarboxylases from Escherichia coli, Salmonella typhimurium, and Saccharomyces cerevisiae. Proc Natl Acad Sci USA 98: 10578-10583.
25. MacRae, M., Kramer, D.L., and Coffino, P. (1998) Developmental effect of polyamine depletion in Caenorhabditis elegans. Biochem J 333: 309-315.
26. Marcotte, E.M., Pellegrini, M., Ng, H.L., Rice, D.W., Yeates, T.O., and Eisenberg, D. (1999) Detecting protein function and protein-protein interactions from genome sequences. Science 285: 751-753.
27. Michael, A.J. (2011) Molecular machines encoded by bacterially-derived multi-domain gene fusions that potentially synthesize, N-methylate and transfer long chain polyamines in diatoms. FEBS Lett 585: 2627-2634.
28. Michael, A.J., Furze, J.M., Rhodes, M.J., and Burtin, D. (1996) Molecular cloning and functional identification of a plant ornithine decarboxylase cDNA. Biochem J 314: 241-248.
29. Mishra, A.K., Agnihotri, P., Srivastava, V.K., and Pratap, J.V. (2015) Novel protein-protein interaction between spermidine synthase and S-adenosylmethionine decarboxylase from Leishmania donovani. Biochem Biophys Res Commun 456: 637-642.
30. Nakano, T., Ohki, I., Yokota, A., and Ashida, H. (2013) MtnBD is a multifunctional fusion enzyme in the methionine salvage pathway of Tetrahymena thermophila. PLoS ONE 8: e67385.
31. Nguyen, S., Jones, D.C., Wyllie, S., Fairlamb, A.H., and Phillips, M.A. (2013) Allosteric activation of trypanosomatid deoxyhypusine synthase by a catalytically dead paralog. J Biol Chem 288: 15256-15267.
32. Nishimura, K., Nakatsu, F., Kashiwagi, K., Ohno, H., Saito, T., and Igarashi, K. (2002) Essential role of S-adenosylmethionine decarboxylase in mouse embryonic development. Genes Cells 7: 41-47.
33. Nishimura, K., Lee, S.B., Park, J.H., and Park, M.H. (2012) Essential role of eIF5A-1 and deoxyhypusine synthase in mouse embryonic development. Amino Acids 42: 703-710.
34. Page, R.D. (1996) TreeView: an application to display phylogenetic trees on personal computers. Comput Appl Biosci 12: 357-358.
35. Park, J.H., Aravind, L., Wolff, E.C., Kaevel, J., Kim, Y.S., and Park, M.H. (2006) Molecular cloning, expression, and structural prediction of deoxyhypusine hydroxylase: a HEAT-repeat-containing metalloenzyme. Proc Natl Acad Sci USA 103: 51-56.
36. Park, M.H., Cooper, H.L., and Folk, J.E. (1981) Identification of hypusine, an unusual amino acid, in a protein from human lymphocytes and of spermidine as its biosynthetic precursor. Proc Natl Acad Sci USA 78: 2869-2873.
37. Park, M.H., Wolff, E.C., Smit-McBride, Z., Hershey, J.W., and Folk, J.E. (1991) Comparison of the activities of variant forms of eIF-4D. The requirement for hypusine or deoxyhypusine. J Biol Chem 266: 7988-7994.
38. Park, M.H., Joe, Y.A., and Kang, K.R. (1998) Deoxyhypusine synthase activity is essential for cell viability in the yeast Saccharomyces cerevisiae. J Biol Chem 273: 1677-1683.
39. Pegg, A.E. (2009) S-Adenosylmethionine decarboxylase. Essays Biochem 46: 25-45.
40. Pegg, A.E., and Michael, A.J. (2010) Spermine synthase. Cell Mol Life Sci 67: 113-121.
41. Pendeville, H., Carpino, N., Marine, J.C., Takahashi, Y., Muller, M., Martial, J.A., and Cleveland, J.L. (2001) The ornithine decarboxylase gene is essential for cell survival during early murine development. Mol Cell Biol 21: 6549-6558.
42. Pirkov, I., Norbeck, J., Gustafsson, L., and Albers, E. (2008) A complete inventory of all enzymes in the eukaryotic methionine salvage pathway. FEBS J 275: 4111-4120.
43. Roberts, S.C., Scott, J., Gasteier, J.E., Jiang, Y., Brooks, B., Jardim, A., etal. (2002) S-adenosylmethionine decarboxylase from Leishmania donovani. Molecular, genetic, and biochemical characterization of null mutants and overproducers. J Biol Chem 277: 5902-5909.
44. Salim, H.M., Negritto, M.C., and Cavalcanti, A.R. (2009) 1+1 = 3: a fusion of 2 enzymes in the methionine salvage pathway of Tetrahymena thermophila creates a trifunctional enzyme that catalyzes 3 steps in the pathway. PLoS Genet 5: e1000701.
45. Sauter, M., Moffatt, B., Saechao, M.C., Hell, R., and Wirtz, M. (2013) Methionine salvage and S-adenosylmethionine: essential links between sulfur, ethylene and polyamine biosynthesis. Biochem J 451: 145-154.
46. Schonknecht, G., Weber, A.P., and Lercher, M.J. (2014) Horizontal gene acquisitions by eukaryotes as drivers of adaptive evolution. Bioessays 36: 9-20.
47. Schwede, T., Kopp, J., Guex, N., and Peitsch, M.C. (2003) SWISS-MODEL: an automated protein homology-modeling server. Nucleic Acids Res 31: 3381-3385.
48. Sekowska, A., Coppee, J.Y., Le Caer, J.P., Martin-Verstraete, I., and Danchin, A. (2000) S-adenosylmethionine decarboxylase of Bacillus subtilis is closely related to archaebacterial counterparts. Mol Microbiol 36: 1135-1147.
49. Shaw, F.L., Elliott, K.A., Kinch, L.N., Fuell, C., Phillips, M.A., and Michael, A.J. (2010) Evolution and multifarious horizontal transfer of an alternative biosynthetic pathway for the alternative polyamine sym-homospermidine. J Biol Chem 285: 14711-14723.
50. Stanley, B.A., Pegg, A.E., and Holm, I. (1989) Site of pyruvate formation and processing of mammalian S-adenosylmethionine decarboxylase proenzyme. J Biol Chem 264: 21073-21079.
51. Steglich, C., and Schaeffer, S.W. (2006) The ornithine decarboxylase gene of Trypanosoma brucei: evidence for horizontal gene transfer from a vertebrate source. Infect Genet Evol 6: 205-219.
52. Swofford, D.L. (2000) PAUP*: Phylogenetic Analysis Using Parsimony (and Other Methods). Sunderland, MA: Sinauer Associates, Inc.
53. Thompson, J.D., Gibson, T.J., Plewniak, F., Jeanmougin, F., and Higgins, D.G. (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25: 4876-4882.
54. Toms, A.V., Kinsland, C., McCloskey, D.E., Pegg, A.E., and Ealick, S.E. (2004) Evolutionary links as revealed by the structure of Thermotoga maritima S-adenosylmethionine decarboxylase. J Biol Chem 279: 33837-33846.
55. Urano, K., Hobo, T., and Shinozaki, K. (2005) Arabidopsis ADC genes involved in polyamine biosynthesis are essential for seed development. FEBS Lett 579: 1557-1564.
56. Willert, E.K., and Phillips, M.A. (2008) Regulated expression of an essential allosteric activator of polyamine biosynthesis in African trypanosomes. PLoS Pathog 4: e1000183.
57. Wu, H., Min, J., Zeng, H., McCloskey, D.E., Ikeguchi, Y., Loppnau, P., etal. (2008) Crystal structure of human spermine synthase: implications of substrate binding and catalytic mechanism. J Biol Chem 283: 16135-16146.
58. Wuitschick, J.D., and Karrer, K.M. (1999) Analysis of genomic G + C content, codon usage, initiator codon context and translation termination sites in Tetrahymena thermophila. J Eukaryot Microbiol 46: 239-247.