Towards glycoengineering in archaea: Replacement of Haloferax volcanii AglD with homologous glycosyltransferases from other halophilic archaea

Applied and Environmental Microbiology

Volumn 76, Issue 17, 2010, Pages 5684-5692

  Calo, Doron ^a   Eilam, Yael ^a   Lichtenstein, Rachel G ^a   Eichler, Jerry ^a  

^a BEN GURION UNIVERSITY OF THE NEGEV   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

APPLIED POTENTIALS; ARCHAEA; ARCHAEAL; EUKARYA; GENE MANIPULATION; GLYCOSYL TRANSFERASE; GLYCOSYLTRANSFERASES; HALOFERAX VOLCANII; HALOPHILIC ARCHAEA; IN-CELL; MOLECULAR TOOLS; N-GLYCOSYLATION; N-LINKED; N-LINKED GLYCANS; PENTASACCHARIDES; S-LAYERS;

ENZYMES; ESTERIFICATION; GLYCOSYLATION; MASS SPECTROMETRY; TRANSCRIPTION;

GLYCOPROTEINS;

ARCHAEAL PROTEIN; GLYCOSYLTRANSFERASE; HEXOSE; MEMBRANE PROTEIN; OLIGOSACCHARIDE; RECOMBINANT PROTEIN; S LAYER PROTEINS; S-LAYER PROTEINS;

BACTERIUM; ENZYME ACTIVITY; EUKARYOTE; GENETIC ANALYSIS; GENETIC ENGINEERING; GENOME; PROTEIN;

ARTICLE; CHEMISTRY; ENZYMOLOGY; GENETIC ENGINEERING; GENETIC RECOMBINATION; GENETICS; GLYCOSYLATION; HALOBACTERIUM SALINARUM; HALOFERAX VOLCANII; MASS SPECTROMETRY; METABOLISM;

ARCHAEAL PROTEINS; GENETIC ENGINEERING; GLYCOSYLATION; GLYCOSYLTRANSFERASES; HALOBACTERIUM SALINARUM; HALOFERAX VOLCANII; HEXOSES; MASS SPECTROMETRY; MEMBRANE GLYCOPROTEINS; METABOLIC NETWORKS AND PATHWAYS; OLIGOSACCHARIDES; RECOMBINANT PROTEINS; RECOMBINATION, GENETIC;

ARCHAEA; BACTERIA (MICROORGANISMS); EUKARYOTA; HALOBACTERIA; HALOBACTERIUM SALINARUM; HALOFERAX VOLCANII; HARNESS;

EID: 77956608454     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.00681-10     Document Type: Article

References (40)

1. Abu-Qarn, M., and J. Eichler. 2006. Protein N-glycosylation in Archaea: defining Haloferax volcanii genes involved in S-layer glycoprotein glycosylation. Mol. Microbiol. 61:511-525.
2. Abu-Qarn, M., S. Yurist-Doutsch, A. Giordano, A. Trauner, H. R. Morris, P. Hitchen, O. Medalia, A. Dell, and J. Eichler. 2007. Haloferax volcanii AglB and AglD are involved in N-glycosylation of the S-layer glycoprotein and proper assembly of the surface layer. J. Mol. Biol. 374:1224-1236.
3. Abu-Qarn, M., A. Giordano, F. Battaglia, A. Trauner, P. Hitchen, H. R. Morris, A. Dell, and J. Eichler. 2008. Identification of AglE, a second glycosyltransferase involved in N-glycosylation of the Haloferax volcanii S-layer glycoprotein. J. Bacteriol. 190:3140-3146.
4. Abu-Qarn, M., J. Eichler, and N. Sharon. 2008. Not just for Eukarya anymore: N-glycosylation in Bacteria and Archaea. Curr. Opin. Struct. Biol. 18:544-550.
5. Baliga, N. S., R. Bonneau, M. T. Tacciotti, M. Pan, G. Glusman, E. W. Deutsch, P. Shannon, Y. Chui, R. S. Weng, R. R. Gan, P. Hung, S. V. Date, E. Marcotte, L. Hood, and W. V. Ng. 2004. Genome sequence of Haloarcula marismortui: a halophilic archaeon from the Dead Sea. Genome Res. 14:2221-2234.
6. Bisle, B., A. Schmidt, B. Scheibe, C. Klein, A. Tebbe, J. Kellermann, F. Siedler, F. Pfeiffer, F. Lottspeich, and D. Oesterhelt. 2006. Quantitative profiling of the membrane proteome in a halophilic archaeon. Mol. Cell Proteomics 5:1543-1558.
7. Bolhuis, H., P. Palm, A. Wende, M. Falb, M. Rampp, F. Rodriguez-Valera, F. Pfeiffer, and D. Oesterhelt. 2006. The genome of the square archaeon Haloquadratum walsbyi: life at the limits of water activity. BMC Genomics 7:169.
8. Breton, C., L. Snajdrová, C. Jeanneau, J. Koca, and A. Imberty. 2006. Structures and mechanisms of glycosyltransferases. Glycobiology 16:29R-37R.
9. Burns, D. G., P. H. Janssen, T. Itoh, M. Kamekura, Z. Li, G. Jensen, F. Rodriguez-Valera, H. Bolhuis, and M. L. Dyall-Smith. 2007. Haloquadratum walsbyi gen. nov., sp. nov., the square haloarchaeon of Walsby, isolated from saltern crystallizers in Australia and Spain. Int. J. Syst. Evol. Microbiol. 57:387-392.
10. Calo, D., L. Kaminski, and J. Eichler. 2010. Protein glycosylation in Archaea: sweet and extreme. Glycobiology [Epub ahead of print.] doi:10.1093/glycob/cwq055.
11. Dubray, G., and G. Bezard. 1982. A highly sensitive periodic acid-silver stain for 1, 2-diol groups of glycoproteins and polysaccharides in polyacrylamide gels. Anal. Biochem. 119:325-329.
12. Eichler, J., and M. W. W. Adams. 2005. Posttranslational protein modification in Archaea. Microbiol. Mol. Biol. Rev. 69:393-425.
13. Falb, M., F. Pfeiffer, P. Palm, K. Rodewald, V. Hickmann, J. Tittor, and D. Oesterhelt. 2005. Living with two extremes: conclusions from the genome sequence of Natronomonas pharaonis. Genome Res. 15:1336-1343.
14. Faridmoayer, A., M. A. Fentabil, D. C. Mills, J. S. Klassen, and M. F. Feldman. 2007. Functional characterization of bacterial oligosaccharyltransferases involved in O-linked protein glycosylation. J. Bacteriol. 189:8088-8098.
15. Faridmoayer, A., M. A. Fentabil, M. F. Haurat, W. Yi, R. Woodward, P. G. Wang, and M. F. Feldman. 2008. Extreme substrate promiscuity of the Neisseria oligosaccharyltransferase involved in protein O-glycosylation. J. Biol. Chem. 283:34596-34604.
16. Feldman, M. F., M. Wacker, M. Hernandez, P. G. Hitchen, C. L. Marolda, M. Kowarik, H. R. Morris, A. Dell, M. A. Valvano, and M. Aebi. 2005. Engineering N-linked protein glycosylation with diverse O antigen lipopolysaccharide structures in Escherichia coli. Proc. Natl. Acad. Sci. U. S. A. 102:3016-3021.
17. Kaminski, L., and J. Eichler. 6 May 2010, posting date. Identification of residues important for the activity of Haloferax volcanii AglD, a component of the archaeal N-glycosylation pathway. Archaea doi:10.1155/2010/315108.
18. Kowarik, M., N. M. Young, S. Numao, B. L. Schulz, I. Hug, N. Callewaert, D. C. Mills, D. C. Watson, M. Hernandez, J. F. Kelly, M. Wacker, and M. Aebi. 2006. Definition of the bacterial N-glycosylation site consensus sequence. EMBO J. 25:1957-1966.
19. Lechner, J., and F. Wieland. 1989. Structure and biosynthesis of prokaryotic glycoproteins. Annu. Rev. Biochem. 58:173-194.
20. Magidovich, H., and J. Eichler. 2009. Glycosyltransferases and oligosaccharyltransferases in Archaea: putative components of the N-glycosylation pathway in the third domain of life. FEMS Microbiol. Lett. 300:122-130.
21. Magidovich, H., S. Yurist-Doutsch, Z. Konrad, V. V. Ventura, A. Dell, P. G. Hitchen, and J. Eichler. 2010. AglP is a cytoplasmic S-adenosyl-L-methionine- dependent methyltransferase that participates in the N-glycosylation pathway of Haloferax volcanii. Mol. Microbiol. 76:190-199.
22. Mevarech, M., and R. Werczberger. 1985. Genetic transfer in Halobacterium volcanii. J. Bacteriol. 162:461-462.
23. Mevarech, M., W. Leicht, and M. M. Werber. 1976. Hydrophobic chromatography and fractionation of enzymes from extremely halophilic bacteria using decreasing concentration gradients of ammonium sulfate. Biochemistry 15:2383-2387.
24. Ng, W. V., S. P. Kennedy, G. G. Mahairas, B. Berquist, M. Pan, H. D. Shukla, S. R. Lasky, N. S. Baliga, V. Thorsson, J. Sbrogna, S. Swartzell, D. Weir, J. Hall, T. A. Dahl, R. Welti, Y. A. Goo, B. Leithauser, K. Keller, R. Cruz, M. J. Danson, D. W. Hough, D. G. Maddocks, P. E. Jablonski, M. P. Krebs, C. M. Angevine, H. Dale, T. A. Isenbarger, R. F. Peck, M. Pohlschroder, J. L. Spudich, K. W. Jung, M. Alam, T. Freitas, S. Hou, C. J. Daniels, P. P. Dennis, A. D. Omer, H. Ebhardt, T. M. Lowe, P. Liang, M. Riley, L. Hood, and S. Das Sarma. 2000. Genome sequence of Halobacterium species NRC-1. Proc. Natl. Acad. Sci. U. S. A. 97:12176-12181.
25. Oesterhelt, D., and G. Krippahl. 1983. Phototrophic growth of halobacteria and its use for isolation of photosynthetically-deficient mutants. Ann. Microbiol. (Paris) 134B: 137-150.
26. Pfeiffer, F., S. C. Schuster, A. Broicher, M. Falb, P. Palm, K. Rodewald, A. Ruepp, J. Soppa, J. Tittor, and D. Oesterhelt. 2008. Evolution in the laboratory: the genome of Halobacterium salinarum strain R1 compared to that of strain NRC-1. Genomics 91:335-346.
27. Plavner, N., and J. Eichler. 2008. Defining the topology of the N-glycosylation pathway in the halophilic archaeon Haloferax volcanii. J. Bacteriol. 190:8045-8052.
28. Schwarz, F., W. Huang, C. Li, B. L. Schulz, C. Lizak, A. Palumbo, S. Numao
29. D. Neri, M. Aebi, and L. X. Wang. 2010. A combined method for producing homogeneous glycoproteins with eukaryotic N-glycosylation. Nat. Chem. Biol. 6:264-266.
30. Sumper, M., E. Berg, R. Mengele, and I. Strobel. 1990. Primary structure and glycosylation of the S-layer protein of Haloferax volcanii. J. Bacteriol. 172:7111-7118.
31. Szymanski, C. M., R. Yao, C. P. Ewing, T. J. Trust, and P. Guerry. 1999. Evidence for a system of general protein glycosylation in Campylobacter jejuni. Mol. Microbiol. 32:1022-1030.
32. Tamura, K., J. Dudley, M. Nei, and S. Kumar. 2007. MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol. Biol. Evol. 24:1596-1599.
33. Twellmeyer, J., A. Wende, J. Wolfertz, F. Pfeiffer, M. Panhuysen, A. Zaigler, J. Soppa, G. Welzl, and D. Oesterhelt. 2007. Microarray analysis in the archaeon Halobacterium salinarum strain R1. PLoS One 2: e1064.
34. Wacker, M., D. Linton, P. G. Hitchen, M. Nita-Lazar, S. M. Haslam, S. J. North, M. Panico, H. R. Morris, A. Dell, B. W. Wren, and M. Aebi. 2002. N-linked glycosylation in Campylobacter jejuni and its functional transfer into E. coli. Science 298:1790-1793.
35. Wacker, M., M. F. Feldman, N. Callewaert, M. Kowarik, B. R. Clarke, N. L. Pohl, M. Hernandez, E. D. Vines, M. A. Valvano, C. Whitfield, and M. Aebi. 2006. Substrate specificity of bacterial oligosaccharyltransferase suggests a common transfer mechanism for the bacterial and eukaryotic systems. Proc. Natl. Acad. Sci. U. S. A. 103:7088-7093.
36. Young, N. M., J. R. Brisson, J. Kelly, D. C. Watson, L. Tessier, P. H. Lanthier, H. C. Jarrell, N. Cadotte, F. St Michael, E. Aberg, and C. M. Szymanski. 2002. Structure of the N-linked glycan present on multiple glycoproteins in the Gram-negative bacterium, Campylobacter jejuni. J. Biol. Chem. 277:42530-42539.
37. Yurist-Doutsch, S., and J. Eichler. 2009. Manual annotation, transcriptional analysis and protein expression studies reveal novel genes in the agl cluster responsible for N-glycosylation in the halophilic archaeon Haloferax volcanii. J. Bacteriol. 191:3068-3075.
38. Yurist-Doutsch, S., B. Chaban, D. Van Dyke, K. F. Jarrell, and J. Eichler. 2008. Sweet to the extreme: protein glycosylation in Archaea. Mol. Microbiol. 68:1079-1084.
39. Yurist-Doutsch, S., M. Abu-Qarn, F. Battaglia, H. R. Morris, P. G. Hitchen, A. Dell, and J. Eichler. 2008. aglF, aglG, and aglI, novel members of a gene cluster involved in the N-glycosylation of the Haloferax volcanii S-layer glycoprotein. Mol. Microbiol. 69:1234-1245.
40. Yurist-Doutsch, S., H. Magidovich, V. V. Ventura, P. G. Hitchen, A. Dell, and J. Eichler. 2010. N-glycosylation in Archaea: on the coordinated actions of Haloferax volcanii AglF and AglM. Mol. Microbiol. 75:1047-1058.