N-Linked glycosylation in archaea: A structural, functional, and genetic analysis

Microbiology and Molecular Biology Reviews

Volumn 78, Issue 2, 2014, Pages 304-341

  Jarrell, Ken F ^a   Ding, Yan ^a   Meyer, Benjamin H ^b   Albers, Sonja Verena ^b   Kaminski, Lina ^c   Eichler, Jerry ^c  

^a QUEEN S UNIVERSITY   (Canada)

^b MAX PLANCK INSTITUTE FOR TERRESTRIAL MICROBIOLOGY   (Germany)

^c BEN GURION UNIVERSITY OF THE NEGEV   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

ASPARAGINE LINKED OLIGOSACCHARIDE; GLYCOPROTEIN; GREEN FLUORESCENT PROTEIN; URIDINE DIPHOSPHATE GALACTOSE; URIDINE DIPHOSPHATE GLUCOSE; URIDINE DIPHOSPHATE GLUCOSE DEHYDROGENASE; DOLICHYL-DIPHOSPHOOLIGOSACCHARIDE - PROTEIN GLYCOTRANSFERASE; GLYCOSYLTRANSFERASE; MEMBRANE PROTEIN; POLYSACCHARIDE;

ARCHAEAL VIRUS; ARCHAEON; CELLULAR DISTRIBUTION; DELETION MUTANT; ENZYME ACTIVE SITE; GENE DELETION; GENETIC ANALYSIS; HALOARCULA MARISMORTUI; HALOBACTERIUM SALINARUM; HALOFERAX VOLCANII; HALOPHILE; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; IN VITRO STUDY; MASS SPECTROMETRY; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; METHANOCOCCUS; METHANOCOCCUS MARIPALUDIS; METHANOCOCCUS VOLTAE; METHANOGEN; METHANOTHERMUS FERVIDUS; N LINKED GLYCOSYLATION; NONHUMAN; POLYACRYLAMIDE GEL ELECTROPHORESIS; PROTEIN DEGRADATION; PROTEIN FUNCTION; PROTEIN GLYCOSYLATION; PROTEIN STRUCTURE; PYROCOCCUS FURIOSUS; REVIEW; SULFOLOBUS ACIDOCALDARIUS; SULFOLOBUS SOLFATARICUS; TANDEM MASS SPECTROMETRY; THERMOPLASMA ACIDOPHILUM; TRANS GOLGI NETWORK; GENETICS; GLYCOSYLATION; METABOLISM; PROKARYOTIC CELL; PROTEIN PROCESSING;

ARCHAEA; GLYCOSYLATION; HEXOSYLTRANSFERASES; MEMBRANE PROTEINS; METABOLIC NETWORKS AND PATHWAYS; POLYSACCHARIDES; PROKARYOTIC CELLS; PROTEIN PROCESSING, POST-TRANSLATIONAL;

EID: 84901001807     PISSN: 10922172     EISSN: 10985557     Source Type: Journal    
DOI: 10.1128/MMBR.00052-13     Document Type: Review

References (233)

1. Prabakaran S, Lippens G, Steen H, Gunawardena J. 2012. Posttranslational modification: nature's escape from genetic imprisonment and the basis for dynamic information encoding. Wiley Interdiscip. Rev. Syst. Biol. Med. 4:565-583. http://dx.doi.org/10.1002/wsbm.1185.
2. Eichler J, Adams MW. 2005. Posttranslational protein modification in Archaea. Microbiol. Mol. Biol. Rev. 69:393-425. http://dx.doi.org/10 .1128/MMBR.69.3.393-425.2005.
3. Apweiler R, Hermjakob H, Sharon N. 1999. On the frequency of protein glycosylation, as deduced from analysis of the SWISS-PROT database. Biochim. Biophys. Acta 1473:4-8. http://dx.doi.org/10.1016 /S0304-4165(99)00165-8.
4. Aebi M. 2013. N-linked protein glycosylation in the ER. Biochim. Biophys. Acta 1833:2430-2437. http://dx.doi.org/10.1016/j.bbamcr.2013 .04.001.
5. Breitling J, Aebi M. 2013. N-linked protein glycosylation in the endoplasmic reticulum. Cold Spring Harb. Perspect. Biol. 5:a013359. http: //dx.doi.org/10.1101/cshperspect.a013359.
6. Eichler J. 2013. Extreme sweetness: protein glycosylation in Archaea. Nat. Rev. Microbiol. 11:151-156. http://dx.doi.org/10.1038/nrmicro 2957.
7. Larkin A, Imperiali B. 2011. The expanding horizons of asparaginelinked glycosylation. Biochemistry 50:4411-4426. http://dx.doi.org/10 .1021/bi200346n.
8. Zarschler K, Janesch B, Pabst M, Altmann F, Messner P, Schäffer C. 2010. Protein tyrosine O-glycosylation-a rather unexplored prokaryotic glycosylation system. Glycobiology 20:787-798. http://dx.doi.org/10 .1093/glycob/cwq035.
9. Iwashkiw JA, Vozza NF, Kinsella RL, Feldman MF. 2013. Pour some sugar on it: the expanding world of bacterial protein O-linked glycosylation. Mol. Microbiol. 89:14-28. http://dx.doi.org/10.1111/mmi .12265.
10. Kinoshita T, Fujita M, Maeda Y. 2008. Biosynthesis, remodelling and functions of mammalian GPI-anchored proteins: recent progress. J. Biochem. 144:287-294. http://dx.doi.org/10.1093/jb/mvn090.
11. Eisenhaber B, Bork P, Eisenhaber F. 2001. Post-translational GPI lipid anchor modification of proteins in kingdoms of life: analysis of protein sequence data from complete genomes. Protein Eng. 14:17-25. http://dx .doi.org/10.1093/protein/14.1.17.
12. Kobayashi T, Nishizaki R, Ikezawa H. 1997. The presence of GPI-linked protein(s) in an archaeobacterium, Sulfolobus acidocaldarius, closely related to eukaryotes. Biochim. Biophys. Acta 1334:1-4. http://dx.doi .org/10.1016/S0304- 4165(96)00099-2.
13. Ilg T. 2000. Proteophosphoglycans of Leishmania. Parasitol. Today 16: 489-497. http://dx.doi.org/10.1016/S0169-4758(00)01791-9.
14. Haynes PA. 1998. Phosphoglycosylation: a new structural class of glycosylation?. Glycobiology 8:1-5. http://dx.doi.org/10.1093/glycob/8.1.1.
15. Lippert DN, Dwyer DW, Li F, Olafson RW. 1999. Phosphoglycosylation of a secreted acid phosphatase from Leishmania donovani. Glycobiology 9:627-636. http://dx.doi.org/10.1093/glycob/9.6.627.
16. Freeze HH, Ichikawa M. 1995. Identification of N-acetylglucosaminealpha- 1-phosphate transferase activity in Dictyostelium discoideum: an enzyme that initiates phosphoglycosylation. Biochem. Biophys. Res. Commun. 208:384-389.
17. Krieg J, Hartmann S, Vicentini A, Gläsner W, Hess D, Hofsteenge J. 1998. Recognition signal for C-mannosylation of Trp-7 in RNase 2 consists of sequence Trp-x-x-Trp. Mol. Biol. Cell 9:301-309. http://dx.doi .org/10.1091/mbc.9.2.301.
18. Doucey MA, Hess D, Cacan R, Hofsteenge J. 1998. Protein Cmannosylation is enzyme-catalysed and uses dolichyl-phosphatemannose as a precursor. Mol. Biol. Cell 9:291-300. http://dx.doi.org/10 .1091/mbc.9.2.291.
19. Julenius K. 2007. NetCGlyc 1.0: prediction of mammalian Cmannosylation sites. Glycobiology 17:868-876. http://dx.doi.org/10 .1093/glycob/cwm050.
20. Furmanek A, Hofsteenge J. 2000. Protein C-mannosylation: facts and questions. Acta Biochim. Pol. 47:781-789. http://www.actabp.pl/pdf/3- 2000/781.pdf.
21. Spiro RG. 2002. Protein glycosylation: nature, distribution, enzymatic formation, and disease implications of glycopeptide bonds. Glycobiology 12:43R-56R. http://dx.doi.org/10.1093/glycob/12.4.43R.
22. Marshall RD. 1972. Glycoproteins. Annu. Rev. Biochem. 41:673-702.
23. Gavel Y, von Heijne G. 1990. Sequence differences between glycosylated and non-glycosylated Asn-X-Thr/Ser acceptor sites: implications for protein engineering. Protein Eng. 3:433-442. http://dx.doi.org/10.1093 /protein/3.5.433.
24. Bause E, Hettkamp H. 1979. Primary structural requirements for N-glycosylation of peptides in rat liver. FEBS Lett. 108:341-344. http://dx.doi .org/10.1016/0014-5793(79)80559-1.
25. Nothaft H, Szymanski CM. 2010. Protein glycosylation in bacteria: sweeter than ever. Nat. Rev. Microbiol. 8:765-778. http://dx.doi.org/10 .1038/nrmicro2383.
26. Wacker M, Linton D, Hitchen PG, Nita-Lazar M, Haslam SM, North SJ, Panico M, Morris HR, Dell A, Wren BW, Aebi M. 2002. N-linked glycosylation in Campylobacter jejuni and its functional transfer into E. coli. Science 298:1790-1793. http://dx.doi.org/10.1126/science.298.5599 .1790.
27. Karaoglu D, Kelleher DJ, Gilmore R. 1997. The highly conserved Stt3 protein is a subunit of the yeast oligosaccharyltransferase and forms a subcomplex with Ost3p and Ost4p. J. Biol. Chem. 272:32513-32520. http://dx.doi.org/10.1074/jbc.272.51.32513.
28. Spirig U, Glavas M, Bodmer D, Reiss G, Burda P, Lippuner V, te Heesen S, Aebi M. 1997. The STT3 protein is a component of the yeast oligosaccharyltransferase complex. Mol. Gen. Genet. 256:628-637. http: //dx.doi.org/10.1007/s004380050611.
29. Kelleher DJ, Gilmore R. 2006. An evolving view of the eukaryotic oligosaccharyltransferase. Glycobiology 16:47R-62R. http://dx.doi.org/10 .1093/glycob/cwj066.
30. Igura M, Maita N, Kamishikiryo J, Yamada M, Obita T, Maenaka K, Kohda D. 2008. Structure-guided identification of a new catalytic motif of oligosaccharyltransferase. EMBO J. 27:234-243. http://dx.doi.org/10 .1038/sj.emboj.7601940.
31. Yan Q, Lennarz WJ. 1999. Oligosaccharyltransferase: a complex multisubunit enzyme of the endoplasmic reticulum. Biochem. Biophys. Res. Commun. 266:684-689. http://dx.doi.org/10.1006/bbrc.1999.1886.
32. Grass S, Lichti CF, Townsend RR, Gross J, St Geme JW, III. 2010. The Haemophilus influenzae HMW1C protein is a glycosyltransferase that transfers hexose residues to asparagine sites in theHMW1adhesin. PLoS One 6:e1000919. http://dx.doi.org/10.1371/journal.ppat.1000919.
33. Gross J, Grass S, Davis AE, Gilmore-Erdmann P, Townsend RR, St Geme JW, III. 2008. The Haemophilus influenzae HMW1 adhesin is a glycoprotein with an unusual N-linked carbohydrate modification. J. Biol. Chem. 283:26010-26015. http://dx.doi.org/10.1074/jbc.M80181 9200.
34. Helenius J, Ng DT, Marolda CL, Walter P, Valvano MA, Aebi M. 2002. Translocation of lipid-linked oligosaccharides across the ER membrane requires Rft1 protein. Nature 415:447-450. http://dx.doi.org/10.1038 /415447a.
35. Frank CG, Sanyal S, Rush JS, Waechter CJ, Menon AK. 2008. Does Rft1 flip an N-glycan lipid precursor?. Nature 454:E3-E4; discussion E4- E5. http://dx.doi.org/10.1038/nature07165.
36. Rush JS, Gao N, Lehrman MA, Matveev S, Waechter CJ. 2009. Suppression of Rft1 expression does not impair the transbilayer movement of Man5GlcNAc2-P-P-dolichol in sealed microsomes from yeast. J. Biol. Chem. 284:19835-19842. http://dx.doi.org/10.1074/jbc.M109.000893.
37. Jelk J, Gao N, Serricchio M, Signorell A, Schmidt RS, Bangs JD, Acosta-Serrano A, Lehrman MA, Bütikofer P, Menon AK. 2013. Glycoprotein biosynthesis in a eukaryote lacking the membrane protein Rft1. J. Biol. Chem. 288:20616-20623. http://dx.doi.org/10.1074/jbc .M113.479642.
38. Sanyal S, Menon AK. 2010. Stereoselective transbilayer translocation of mannosyl phosphoryl dolichol by an endoplasmic reticulum flippase. Proc. Natl. Acad. Sci. U. S. A. 107:11289-11294. http://dx.doi.org/10 .1073/pnas.1002408107.
39. Gemmill TR, Trimble RB. 1999. Overview of N- and O-linked oligosaccharide structures found in various yeast species. Biochim. Biophys. Acta 1426:227-237. http://dx.doi.org/10.1016/S0304-4165(98)00126-3.
40. Neuberger A. 1938. Carbohydrates in protein: the carbohydrate component of crystalline egg albumin. Biochem. J. 32:1435-1451.
41. Ventosa A, Oren A. 1996. Halobacterium salinarum nom. corrig., a name to replace Halobacterium salinarium (Elazari-Volcani) and to include Halobacterium halobium and Halobacterium cutirubrum. Int. J. Syst. Evol. Microbiol. 46:347.
42. Koncewicz MA. 1972. Glycoproteins in the cell envelope of Halobacterium halobium. Biochem. J. 128:124P.
43. Mescher MF, Strominger JL, Watson SW. 1974. Protein and carbohydrate composition of the cell envelope of Halobacterium salinarium. J. Bacteriol. 120:945-954.
44. Mescher MF, Strominger JL. 1976. Purification and characterization of a prokaryotic glucoprotein from the cell envelope of Halobacterium salinarium. J. Biol. Chem. 251:2005-2014.
45. Sleytr UB, Thorne KJ. 1976. Chemical characterization of the regularly arranged surface layers of Clostridium thermosaccharolyticum and Clostridium thermohydrosulfuricum. J. Bacteriol. 126:377-383.
46. Schäffer C, Messner P. 2004. Surface-layer glycoproteins: an example for the diversity of bacterial glycosylation with promising impacts on nanobiotechnology. Glycobiology 14:31R-42R. http://dx.doi.org/10 .1093/glycob/cwh064.
47. Messner P. 2009. Prokaryotic protein glycosylation is rapidly expanding from "curiosity" to "ubiquity." Chembiochem 10:2151-2154. http://dx .doi.org/10.1002/cbic.200900388.
48. Szymanski CM, Yao R, Ewing CP, Trust TJ, Guerry P. 1999. Evidence for a system of general protein glycosylation in Campylobacter jejuni. Mol. Microbiol. 32:1022-1030. http://dx.doi.org/10.1046/j.1365-2958 .1999.01415.x.
49. Young NM, Brisson JR, Kelly J, Watson DC, Tessier L, Lanthier PH, Jarrell HC, Cadotte N, St Michael F, Aberg E, Szymanski CM. 2002. Structure of the N-linked glycan present on multiple glycoproteins in the Gram-negative bacterium, Campylobacter jejuni. J. Biol. Chem. 277: 42530-42539. http://dx.doi.org/10.1074/jbc.M206114200.
50. Nothaft H, Liu X, McNally DJ, Szymanski CM. 2010. N-linked protein glycosylation in a bacterial system. Methods Mol. Biol. 600:227-243. http://dx.doi.org/10.1007/978-1-60761-454-8-16.
51. Nothaft H, Szymanski CM. 2013. Bacterial protein N-glycosylation: new perspectives and applications. J. Biol. Chem. 288:6912-6920. http: //dx.doi.org/10.1074/jbc.R112.417857.
52. Szymanski CM, Wren BW. 2005. Protein glycosylation in bacterial mucosal pathogens. Nat. Rev. Microbiol. 3:225-237. http://dx.doi.org /10.1038/nrmicro1100.
53. Alaimo C, Catrein I, Morf L, Marolda CL, Callewaert N, Valvano MA, Feldman MF, Aebi M. 2006. Two distinct but interchangeable mechanisms for flipping of lipid-linked oligosaccharides. EMBO J. 25:967-976. http://dx.doi.org/10.1038/sj.emboj.7601024.
54. Woese CR, Fox GE. 1977. Phylogenetic structure of the prokaryotic domain: the primary kingdoms. Proc. Natl. Acad. Sci. U. S. A. 74:5088-5090. http://dx.doi.org/10.1073/pnas.74.11.5088.
55. Fox GE, Magrum LJ, Balch WE, Wolfe RS, Woese CR. 1977. Classification of methanogenic bacteria by 16S ribosomalRNAcharacterization. Proc. Natl. Acad. Sci. U. S. A. 74:4537-4541. http://dx.doi.org/10.1073 /pnas.74.10.4537.
56. Schwarz F, Aebi M. 2011. Mechanisms and principles of N-linked protein glycosylation. Curr. Opin. Struct. Biol. 21:576-582. http://dx.doi .org/10.1016/j.sbi.2011.08.005.
57. Kaminski L, Lurie-Weinberger MN, Allers T, Gophna U, Eichler J. 2013. Phylogenetic- and genome-derived insight into the evolution of N-glycosylation in Archaea. Mol. Phylogenet. Evol. 68:327-339. http: //dx.doi.org/10.1016/j. ympev.2013.03.024.
58. Dell A, Galadari A, Sastre F, Hitchen P. 2010. Similarities and differences in the glycosylation mechanisms in prokaryotes and eukaryotes. Int. J. Microbiol. 2010:148178. http://dx.doi.org/10.1155/2010/148178.
59. Calo D, Kaminski L, Eichler J. 2010. Protein glycosylation in Archaea: sweet and extreme. Glycobiology 20:1065-1076. http://dx.doi.org/10 .1093/glycob/cwq055.
60. Weerapana E, Imperiali B. 2006. Asparagine-linked protein glycosylation: from eukaryotic to prokaryotic systems. Glycobiology 16:91R- 101R. http://dx.doi.org/10.1093/glycob/cwj099.
61. Eichler J, Jarrell K, Albers S. 2013. A proposal for the naming of N-glycosylation pathway components in Archaea. Glycobiology 23:620-621. http://dx.doi.org/10.1093/glycob/cwt034.
62. Bhat AH, Mondal H, Chauhan JS, Raghava GP, Methi A, Rao A. 2012. ProGlycProt: a repository of experimentally characterized prokaryotic glycoproteins. Nucleic Acids Res. 40:D388-D393. http://dx.doi.org/10 .1093/nar/gkr911.
63. Sumper M, Berg E, Mengele R, Strobel I. 1990. Primary structure and glycosylation of the S-layer protein of Haloferax volcanii. J. Bacteriol. 172:7111-7118.
64. Eichler J, Maupin-Furlow J. 2013. Post-translation modification in Archaea: lessons from Haloferax volcanii and other haloarchaea. FEMS Microbiol. Rev. 37:583-606. http://dx.doi.org/10.1111/1574-6976.12012.
65. Abu-Qarn M, Eichler J. 2006. Protein N-glycosylation in Archaea: defining Haloferax volcanii genes involved in S-layer glycoprotein glycosylation. Mol. Microbiol. 61:511-525. http://dx.doi.org/10.1111/j.1365-2958.2006.05252.x.
66. Burda P, Aebi M. 1999. The dolichol pathway of N-linked glycosylation. Biochim. Biophys. Acta 1426:239-257. http://dx.doi.org/10.1016/S0304-4165(98) 00127-5.
67. Kornfeld R, Kornfeld S. 1985. Assembly of asparagine-linked oligosaccharides. Annu. Rev. Biochem. 54:631-664. http://dx.doi.org/10.1146 /annurev.bi.54.070185.003215.
68. Yan A, Lennarz WJ. 2005. Unraveling the mechanism of protein N-glycosylation. J. Biol. Chem. 280:3121-3124. http://dx.doi.org/10.1074/jbc .R400036200.
69. Linton D, Dorrell N, Hitchen PG, Amber S, Karlyshev AV, Morris HR, Dell A, Valvano MA, Aebi M, Wren BW. 2005. Functional analysis of the Campylobacter jejuni N-linked protein glycosylation pathway. Mol. Microbiol. 55:1695-1703. http://dx.doi.org/10.1111/j.1365-2958.2005 .04519.x.
70. Allers T, Ngo HP, Mevarech M, Lloyd RG. 2004. Development of additional selectable markers for the halophilic archaeon Haloferax volcanii based on the leuB and trpA genes. Appl. Environ. Microbiol. 70: 943-953. http://dx.doi.org/ 10.1128/AEM.70.2.943-953.2004.
71. Chaban B, Voisin S, Kelly J, Logan SM, Jarrell KF. 2006. Identification of genes involved in the biosynthesis and attachment of Methanococcus voltae N-linked glycans: insight into N-linked glycosylation pathways in Archaea. Mol. Microbiol. 61:259-268. http://dx.doi.org/10.1111/j.1365-2958.2006.05226.x.
72. Abu-Qarn M, Yurist-Doutsch S, Giordano A, Trauner A, Morris HR, Hitchen P, Medalia O, Dell A, Eichler J. 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. http: //dx.doi.org/10.1016/j. jmb.2007.10.042.
73. Kaminski L, Eichler J. 2010. Identification of residues important for the activity of Haloferax volcanii AglD, a component of the archaeal N-glycosylation pathway. Archaea 2010:315108. http://dx.doi.org/10.1155 /2010/315108.
74. Abu-Qarn M, Giordano A, Battaglia F, Trauner A, Hitchen PG, Morris HR, Dell A, Eichler J. 2008. Identification of AglE, a second glycosyltransferase involved in N-glycosylation of the Haloferax volcanii S-layer glycoprotein. J. Bacteriol. 190:3140-3146. http://dx.doi.org/10 .1128/JB.00056-08.
75. Kaminski L, Abu-Qarn M, Guan Z, Naparstek S, Ventura VV, Raetz CR, Hitchen PG, Dell A, Eichler J. 2010. AglJ adds the first sugar of the N-linked pentasaccharide decorating the Haloferax volcanii S-layer gly-coprotein. J. Bacteriol. 192:5572-5579. http://dx.doi.org/10.1128/JB .00705-10.
76. Yurist-Doutsch S, Abu-Qarn M, Battaglia F, Morris HR, Hitchen PG, Dell A, Eichler J. 2008. aglF, aglG and aglI, novel members of a gene island involved in the N-glycosylation of the Haloferax volcanii S-layer glycoprotein. Mol. Microbiol. 69:1234-1245. http://dx.doi.org/10.1111 /j.1365-2958.2008.06352.x.
77. Glucksmann MA, Reuber TL, Walker GC. 1993. Genes needed for the modification, polymerization, export, and processing of succinoglycan by Rhizobium meliloti: a model for succinoglycan biosynthesis. J. Bacteriol. 175:7045-7055.
78. Yurist-Doutsch S, Eichler J. 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. http://dx.doi.org/10.1128 /JB.01838-08.
79. Magidovich H, Yurist-Doutsch S, Konrad Z, Ventura VV, Dell A, Hitchen PG, Eichler J. 2010. AglP is an S-adenosyl-L-methioninedependent methyltransferase that participates in the N-glycosylation pathway in Haloferax volcanii. Mol. Microbiol. 76:190-199. http://dx .doi.org/10.1111/j.1365-2958.2010.07090.x.
80. Yurist-Doutsch S, Magidovich H, Ventura VV, Hitchen PG, Dell A, Eichler J. 2010. N-glycosylation in Archaea: on the coordinated actions of Haloferax volcanii AglF and AglM. Mol. Microbiol. 75:1047-1058. http://dx.doi.org/10.1111/ j.1365-2958.2009.07045.x.
81. Plavner N, Eichler J. 2008. Defining the topology of the N-glycosylation pathway in the halophilic archaeon Haloferax volcanii. J. Bacteriol. 190: 8045-8052. http://dx.doi.org/10.1128/JB.01200-08.
82. Lechner J, Wieland F, Sumper M. 1985. Biosynthesis of sulfated saccharides N-glycosidically linked to the protein via glucose. Purification and identification of sulfated dolichyl monophosphoryl tetrasaccharides from halobacteria. J. Biol. Chem. 260:860-866.
83. Wieland F, Dompert W, Bernhardt G, Sumper M. 1980. Halobacterial glycoprotein saccharides contain covalently linked sulphate. FEBS Lett. 120:110-114. http://dx.doi.org/10.1016/0014-5793(80)81058-1.
84. Wieland F, Lechner J, Sumper M. 1986. Iduronic acid: constituent of sulphated dolichyl phosphate oligosaccharides in halobacteria. FEBS Lett. 195:77-81. http://dx.doi.org/10.1016/0014-5793(86)80134-X.
85. Kuntz C, Sonnenbichler J, Sonnenbichler I, Sumper M, Zeitler R. 1997. Isolation and characterization of dolichol-linked oligosaccharides from Haloferax volcanii. Glycobiology 7:897-904. http://dx.doi.org/10 .1093/glycob/7.7.897.
86. Guan Z, Naparstek S, Kaminski L, Konrad Z, Eichler J. 2010. Distinct glycan-charged phosphodolichol carriers are required for the assembly of the pentasaccharide N-linked to the Haloferax volcanii S-layer glycoprotein. Mol. Microbiol. 78:1294-1303. http://dx.doi.org/10.1111/j .1365-2958.2010.07405.x.
87. Abu-Qarn M, Eichler J. 2007. An analysis of amino acid sequences surrounding archaeal glycoprotein sequons. Archaea 2:73-81. http: //www.ncbi.nlm.nih.gov/pmc/articles/PMC2686383/.
88. Swiezewska E, Danikiewicz W. 2005. Polyisoprenoids: structure, biosynthesis and function. Prog. Lipid Res. 44:235-258. http://dx.doi.org/10 .1016/j.plipres.2005.05.002.
89. Naparstek S, Guan Z, Eichler J. 2012. A predicted geranylgeranyl reductase reduces the -position isoprene of dolichol phosphate in the halophilic archaeon, Haloferax volcanii. Biochim. Biophys. Acta 1821: 923-933. http://dx.doi.org/10.1016/j.bbalip.2012.03.002.
90. Kaminski L, Guan Z, Abu-Qarn M, Konrad Z, Eichler J. 2012. AglR is required for addition of the final mannose residue of the N-linked glycan decorating the Haloferax volcanii S-layer glycoprotein. Biochim. Biophys. Acta 1820:1664-1670. http://dx.doi.org/10.1016/j.bbagen.2012.06 .014.
91. Liu D, Cole RA, Reeves PR. 1996. An O-antigen processing function for Wzx (RfbX): a promising candidate for O-unit flippase. J. Bacteriol. 178: 2102-2107.
92. Cohen-Rosenzweig C, Yurist-Doutsch S, Eichler J. 2012. AglS, a novel component of the Haloferax volcanii N-glycosylation pathway, is a dolichol phosphate-mannose mannosyltransferase. J. Bacteriol. 194: 6909-6916. http://dx.doi.org/10.1128/JB.01716-12.
93. Mullakhanbhai MF, Larsen H. 1975. Halobacterium volcanii spec. nov., a Dead Sea halobacterium with a moderate salt requirement. Arch. Microbiol. 104:207-214. http://dx.doi.org/10.1007/BF00447326.
94. Guan Z, Naparstek S, Calo D, Eichler J. 2012. Protein glycosylation as an adaptive response in Archaea: growth at different salt concentrations leads to alterations in Haloferax volcanii S-layer glycoprotein N-glycosylation. Environ. Microbiol. 14:743-753. http://dx.doi.org/10.1111/j .1462-2920.2011.02625.x.
95. Kaminski L, Guan Z, Yurist-Doutsch S, Eichler J. 2013. Two distinct N-glycosylation pathways process the Haloferax volcanii S-layer glycoprotein upon changes in environmental salinity. mBio 4(6):e00716-13. http://dx.doi.org/10.1128/mBio.00716-13.
96. Magidovich H, Eichler J. 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. http://dx.doi.org/10.1111/j.1574-6968.2009.01775.x.
97. Tripepi M, Imam S, Pohlschroder M. 2010. Haloferax volcanii flagella are required for motility but are not involved in PibD-dependent surface adhesion. J. Bacteriol. 192:3093-3102. http://dx.doi.org/10.1128/JB .00133-10.
98. Jarrell KF, Albers SV. 2012. The archaellum: an old motility structure with a new name. Trends Microbiol. 20:307-312. http://dx.doi.org/10 .1016/j.tim.2012.04.007.
99. Tripepi M, You J, Temel S, .Önder Ö, Brisson D, Pohlschröder M. 2012. N-glycosylation of Haloferax volcanii flagellins requires known Agl proteins and is essential for biosynthesis of stable flagella. J. Bacteriol. 194:4876-4887. http://dx.doi.org/10.1128/JB.00731-12.
100. Oren A, Ginzburg M, Ginzburg BZ, Hochstein LI, Volcani BE. 1990. Haloarcula marismortui (Volcani) sp. nov., nom. rev., an extremely halophilic bacterium from the Dead Sea. Int. J. Syst. Bacteriol. 40:209-210. http://dx.doi.org/10.1099/00207713-40-2-209.
101. Calo D, Guan Z, Naparstek S, Eichler J. 2011. Different routes to the same ending: comparing the N-glycosylation processes of Haloferax volcanii and Haloarcula marismortui, two halophilic archaea from the Dead Sea. Mol. Microbiol. 81:1166-1177. http://dx.doi.org/10.1111/j.1365-2958.2011.07781.x.
102. Calo D, Eilam Y, Lichtenstein RG, Eichler J. 2010. Towards glycoengineering in archaea: replacement of Haloferax volcanii AglD with homologous glycosyltransferases from other halophilic archaea. Appl. Environ. Microbiol. 76:5684-5692. http://dx.doi.org/10.1128/AEM .00681-10.
103. Calo D, Guan Z, Eichler J. 2011. Glyco-engineering in Archaea: differential N-glycosylation of the S-layer glycoprotein in a transformed Haloferax volcanii strain. Microb. Biotechnol. 4:461-470. http://dx.doi.org /10.1111/j.1751-7915.2011.00250.x.
104. Jarrell KF, Ding Y, Nair DB, Siu S. 2013. Surface appendages of Archaea: structure, function, genetics and assembly. Life 3:86-117. http: //dx.doi.org/10.3390/life3010086.
105. Kelly JF, Jarrell KF. 2012. Protein glycosylation in the third domain of life: the Archaea, p 108-126. In Reid CW, Twine SM, Reid AN (ed), Bacterial glycomics. Caister Academic Press, Cumberland, RI.
106. Jarrell KF, Jones GM, Nair DB. 2010. Role of N-linked glycosylation in cell surface structures of Archaea with a focus on flagella and S layers. Int. J. Microbiol. 2010:470138. http://dx.doi.org/10.1155/2010/470138.
107. Jarrell KF, Jones GM, Kandiba L, Nair DB, Eichler J. 2010. S-layer glycoproteins and flagellins: reporters of archaeal posttranslational modifications. Archaea 2010:612948. http://dx.doi.org/10.1155/2010 /612948.
108. Namboori SC, Graham DE. 2008. Acetamido sugar biosynthesis in the Euryarchaea. J. Bacteriol. 190:2987-2996. http://dx.doi.org/10.1128/JB .01970-07.
109. Namboori SC, Graham DE. 2008. Enzymatic analysis of uridine diphosphate N-acetyl-D-glucosamine. Anal. Biochem. 301:94-100. http://dx .doi.org/10.1016/j.ab.2008.06.034.
110. Larkin A, Chang MM, Whitworth GE, Imperiali B. 2013. Biochemical evidence for an alternate pathway in N-linked glycoprotein biosynthesis. Nat. Chem. Biol. 9:367-373. http://dx.doi.org/10.1038/nchembio.1249.
111. Voisin S, Houliston RS, Kelly J, Brisson JR, Watson D, Bardy SL, Jarrell KF, Logan SM. 2005. Identification and characterization of the unique N-linked glycan common to the flagellins and S-layer glycoprotein of Methanococcus voltae. J. Biol. Chem. 280:16586-16593. http://dx .doi.org/10.1074/jbc. M500329200.
112. Shams-Eldin H, Chaban B, Niehus S, Schwarz RT, Jarrell KF. 2008. Identification of the archaeal alg7 gene homolog (encoding N-acetylglucosamine- 1-phosphate transferase) of the N-linked glycosylation system by cross-domain complementation in Saccharomyces cerevisiae. J. Bacteriol. 190:2217-2220. http://dx.doi.org/10.1128/JB.01778-07.
113. Chaban B, Logan SM, Kelly JF, Jarrell KF. 2009. AglC and AglK are involved in biosynthesis and attachment of diacetylated glucuronic acid to the N-glycan in Methanococcus voltae. J. Bacteriol. 191:187-195. http: //dx.doi.org/10.1128/JB.00885-08.
114. Kalmokoff ML, Jarrell KF. 1991. Cloning and sequencing of a multigene family encoding the flagellins of Methanococcus voltae. J. Bacteriol. 173: 7113-7125.
115. Bardy SL, Mori T, Komoriya K, Aizawa S, Jarrell KF. 2002. Identification and localization of flagellins FlaA and FlaB3 within flagella of Methanococcus voltae. J. Bacteriol. 184:5223-5233. http://dx.doi.org/10 .1128/JB.184.19.5223- 5233.2002.
116. Thomas NA, Jarrell KF. 2001. Characterization of flagellum gene families of methanogenic archaea and localization of novel flagellum accessory proteins. J. Bacteriol. 183:7154-7164. http://dx.doi.org/10.1128/JB .183.24.7154-7164. 2001.
117. Price NP, Momany FA. 2005. Modeling bacterial UDP-HexNAc: polyprenol- P HexNAc-1-P transferases. Glycobiology 15:29R-42R. http://dx .doi.org/10.1093/ glycob/cwi065.
118. Meyer BH, Albers SV. 2013. Hot and sweet: protein glycosylation in Crenarchaeota. Biochem. Soc. Trans. 41:384-392. http://dx.doi.org/10 .1042/BST20120296.
119. Vandyke DJ, Wu J, Logan SM, Kelly JF, Mizuno S, Aizawa SI, Jarrell KF. 2009. Identification of genes involved in the assembly and attachment of a novel flagellin N-linked tetrasaccharide important for motility in the archaeon Methanococcus maripaludis. Mol. Microbiol. 72:633-644. http://dx.doi.org/10. 1111/j.1365-2958.2009.06671.x.
120. Kelly J, Logan SM, Jarrell KF, Vandyke DJ, Vinogradov E. 2009. A novel N-linked flagellar glycan from Methanococcus maripaludis. Carbohydr. Res. 344:648-653. http://dx.doi.org/10.1016/j.carres.2009.01.006.
121. Ng SYM, Wu J, Nair DB, Logan SM, Robotham A, Tessier L, Kelly JF, Uchida K, Aizawa S, Jarrell KF. 2011. Genetic and mass spectrometry analysis of the unusual type IV-like pili of the archaeon Methanococcus maripaludis. J. Bacteriol. 193:804-814. http://dx.doi.org/10.1128/JB .00822-10.
122. Pohlschroder M, Gimenez MI, Jarrell KF. 2005. Protein transport in Archaea: Sec and twin arginine translocation pathways. Curr. Opin. Microbiol. 8:713-719. http://dx.doi.org/10.1016/j.mib.2005.10.006.
123. DiMarco AA, Bobik TA, Wolfe RS. 1990. Unusual coenzymes of methanogenesis. Annu. Rev. Biochem. 59:355-394. http://dx.doi.org/10.1146 /annurev.bi.59.070190.002035.
124. Sauer FD, Blackwell BA, Kramer JK, Marsden BJ. 1990. Structure of a novel cofactor containing N-(7-mercaptoheptanoyl)-O-3- phosphothreonine. Biochemistry 29:7593-7600. http://dx.doi.org/10 .1021/bi00485a008.
125. Jones GM, Wu J, Ding Y, Uchida K, Aizawa S, Robotham A, Logan SM, Kelly J, Jarrell KF. 2012. Identification of genes involved in the acetamidino group modification of the flagellin N-linked glycan of Methanococcus maripaludis. J. Bacteriol. 194:2693-2702. http://dx.doi .org/10.1128/JB.06686-11.
126. Feng L, Senchenkova SN, Tao J, Shashkov AS, Liu B, Shevelev SD, Reeves PR, Xu J, Knirel YA, Wang L. 2005. Structural and genetic characterization of enterohemorrhagic Escherichia coli O145 O antigen and development of an O145 serogroup-specific PCR assay. J. Bacteriol. 187:758-764. http://dx.doi.org/10. 1128/JB.187.2.758-764.2005.
127. Ding Y, Jones GM, Uchida K, Aizawa SI, Robotham A, Logan SM, Kelly J, Jarrell KF. 2013. Identification of genes involved in the biosynthesis of the third and fourth sugars of the Methanococcus maripaludis archaellin N-linked tetrasaccharide. J. Bacteriol. 195:4094-4104. http: //dx.doi.org/10.1128/JB. 00668-13.
128. Amor PA, Yethon JA, Monteiro MA, Whitfield C. 1999. Assembly of the K40 antigen in Escherichia coli: identification of a novel enzyme responsible for addition of L-serine residues to the glycan backbone and its requirement for K40 polymerization. J. Bacteriol. 181:772-780.
129. Menon I, Huber T, Sanyal S, Banerjee S, Barré P, Canis S, Warren JD, Hwa J, Sakmar TP, Menon AK. 2011. Opsin is a phospholipid flippase. Curr. Biol. 21:149-153. http://dx.doi.org/10.1016/j.cub.2010.12.031.
130. Jeffery CJ. 2009. Moonlighting proteins-an update. Mol. Biosyst. 5:345-350. http://dx.doi.org/10.1039/b900658n.
131. Larkin A, Olivier NB, Imperiali B. 2010. Structural analysis of WbpE from Pseudomonas aeruginosa PAO1: a nucleotide sugar aminotransferase involved in O-antigen assembly. Biochemistry 49:7227-7237. http: //dx.doi.org/10.1021/ bi100805b.
132. Keswani J, Orkand S, Premachandran U, Mandelco L, Franklin MJ, Whitman WB. 1996. Phylogeny and taxonomy of mesophilic Methanococcus spp. and comparison of rRNA, DNA hybridization, and phenotypic methods. Int. J. Syst. Bacteriol. 46:727-735. http://dx.doi.org/10 .1099/00207713-46-3-727.
133. Bayley DP, Kalmokoff ML, Jarrell KF. 1993. Effect of bacitracin on flagellar assembly and presumed glycosylation of the flagellins of Methanococcus deltae. Arch. Microbiol. 160:179-185.
134. Siewert G, Strominger JL. 1967. Bacitracin: an inhibitor of the dephosphorylation of lipid pyrophosphate, an intermediate in the biosynthesis of the peptidoglycan of bacterial cell walls. Proc. Natl. Acad. Sci. U. S. A. 57:767-773. http://dx.doi.org/10.1073/pnas.57.3.767.
135. Sumper M. 1987. Halobacterial glycoprotein biosynthesis. Biochim. Biophys. Acta 906:69-79. http://dx.doi.org/10.1016/0304-4157(87) 90005-0.
136. Forterre P, Brochier C, Philippe H. 2002. Evolution of the Archaea. Theor. Popul. Biol. 61:409-422. http://dx.doi.org/10.1006/tpbi.2002 .1592.
137. Peyfoon E, Meyer B, Hitchen PG, Panico M, Morris HR, Haslam SM, Albers SV, Dell A. 2010. The S-layer glycoprotein of the crenarchaeote Sulfolobus acidocaldarius is glycosylated at multiple sites with the chitobiose- linked N-glycans. Archaea 2010:754101. http://dx.doi.org/10.1155 /2010/754101.
138. Zahringer U, Moll H, Hettmann T, Knirel YA, Schafer G. 2000. Cytochrome b558/566 from the archaeon Sulfolobus acidocaldarius has a unique Asn-linked highly branched hexasaccharide chain containing 6-sulfoquinovose. Eur. J. Biochem. 267:4144-4149. http://dx.doi.org/10 .1046/j.1432-1327.2000.01446.x.
139. Karcher U, Schroder H, Haslinger E, Allmaier G, Schreiner R, Wieland F, Haselbeck A, Konig H. 1993. Primary structure of the heterosaccharide of the surface glycoprotein of Methanothermus fervidus. J. Biol. Chem. 268:26821-26826.
140. Wagner M, van Wolferen M, Wagner A, Lassak K, Meyer B, Reimann J, Albers SV. 2012. Versatile genetic toolbox for the crenarchaeote Sulfolobus acidocaldarius. Front. Microbiol. 3:214. http://dx.doi.org/10 .3389/fmicb.2012.00214.
141. McLachlan KR, Krag SS. 1992. Substrate specificity of Nacetylglucosamine 1-phosphate transferase activity in Chinese hamster ovary cells. Glycobiology 2:313-319. http://dx.doi.org/10.1093/glycob/2 .4.313.
142. Lehrman MA. 1991. Biosynthesis of N-acetylglucosamine-P-P-dolichol, the committed step of asparagine-linked oligosaccharide assembly. Glycobiology 1:553-562. http://dx.doi.org/10.1093/glycob/1.6.553.
143. Yamashita S, Hemmi H, Ikeda Y, Nakayama T, Nishino T. 2004. Type 2 isopentenyl diphosphate isomerase from a thermoacidophilic archaeon Sulfolobus shibatae. Eur. J. Biochem. 271:1087-1093. http://dx.doi.org /10.1111/j.1432- 1033.2004.04010.x.
144. Nakatani H, Goda S, Unno H, Nagai T, Yoshimura T, Hemmi H. 2012. Substrate-induced change in the quaternary structure of type 2 isopentenyl diphosphate isomerase from Sulfolobus shibatae. J. Bacteriol. 194: 3216-3224. http://dx.doi.org/10.1128/JB.00068-12.
145. Ohnuma S, Hemmi H, Koyama T, Ogura K, Nishino T. 1998. Recognition of allylic substrates in Sulfolobus acidocaldarius geranylgeranyl diphosphate synthase: analysis using mutated enzymes and artificial allylic substrates. J. Biochem. 123:1036-1040. http://dx.doi.org/10.1093 /oxfordjournals.jbchem. a022040.
146. Ohnuma S, Hirooka K, Hemmi H, Ishida C, Ohto C, Nishino T. 1996. Conversion of product specificity of archaebacterial geranylgeranyldiphosphate synthase. Identification of essential amino acid residues for chain length determination of prenyltransferase reaction. J. Biol. Chem. 271:18831-18837.
147. Guan Z, Eichler J. 2011. Liquid chromatography/tandem mass spectrometry of dolichols and polyprenols, lipid sugar carriers across evolution. Biochim. Biophys. Acta 1811:800-806. http://dx.doi.org/10.1016/j .bbalip.2011.04.009.
148. Anderson MS, Eveland SS, Price NP. 2000. Conserved cytoplasmic motifs that distinguish sub-groups of the polyprenol phosphate:Nacetylhexosamine- 1-phosphate transferase family. FEMS Microbiol. Lett. 191:169-175. http://dx.doi.org/10.1111/j.1574-6968.2000.tb09 335.x.
149. Lehrer J, Vigeant KA, Tatar LD, Valvano MA. 2007. Functional characterization and membrane topology of Escherichia coli WecA, a sugarphosphate transferase initiating the biosynthesis of enterobacterial common antigen and O-antigen lipopolysaccharide. J. Bacteriol. 189:2618-2628. http://dx.doi.org/10.1128/JB.01905-06.
150. Heinz E. 1993. Recent investigations on the biosynthesis of the plant sulfolipid, p 163-178. In De Kok LJ (ed), Sulfur nutrition and assimilation in higher plants. SPB Academic Publishers, The Hague, The Netherlands.
151. Benning C. 1998. Membrane lipids in anoxygenic bacteria, p 83-101. In Siegenthaler PA, Murata N (ed), Lipids in photosynthesis: structure, function and genetics. Kluwer Academic Publishers, Boston, MA.
152. Benning C, Beatty JT, Prince RC, Somerville CR. 1993. The sulfolipid sulfoquinovosyldiacylglycerol is not required for photosynthetic electron transport in Rhodobacter sphaeroides but enhances growth under phosphate limitation. Proc. Natl. Acad. Sci. U. S. A. 90:1561-1565. http: //dx.doi.org/10.1073/pnas.90.4.1561.
153. Benning C, Somerville CR. 1992. Identification of an operon involved in sulfolipid biosynthesis in Rhodobacter sphaeroides. J. Bacteriol. 174: 6479-6487.
154. Benning C, Somerville CR. 1992. Isolation and genetic complementation of a sulfolipid-deficient mutant of Rhodobacter sphaeroides. J. Bacteriol. 147:2352-2360.
155. Meyer BH, Zolghadr B, Peyfoon E, Pabst M, Panico M, Morris HR, Haslam SM, Messner P, Schäffer C, Dell A, Albers SV. 2011. Sulfoquinovose synthase-an important enzyme in the N-glycosylation pathway of Sulfolobus acidocaldarius. Mol. Microbiol. 82:1150-1163. http: //dx.doi.org/10.1111/j.1365-2958.2011.07875. x.
156. Meyer BH, Peyfoon E, Dietrich C, Hitchen P, Dell A, Albers SV. 2013. Agl16, a thermophilic glycosyltransferase, mediating the last step of the N-glycan biosynthesis in the thermoacidophilic crenarchaeon Sulfolobus acidocaldarius. J. Bacteriol. 195:2177-2186. http://dx.doi.org/10.1128/JB .00035-13.
157. Guan Z, Meyer BH, Albers SV, Eichler J. 2011. The thermoacidophilic archaeon Sulfolobus acidocaldarius contains an unusually short, highly reduced dolichyl phosphate. Biochim. Biophys. Acta 1811:607-616. http://dx.doi.org/10. 1016/j.bbalip.2011.06.022.
158. Southam G, Kalmokoff ML, Jarrell KF, Koval SF, Beveridge TJ. 1990. Isolation, characterization, and cellular insertion of the flagella from two strains of the archaebacterium Methanospirillum hungatei. J. Bacteriol. 172:3221-3228.
159. Kalmokoff ML, Koval SF, Jarrell KF. 1992. Relatedness of the flagellins from methanogens. Arch. Microbiol. 157:481-487.
160. Francoleon DR, Boontheung P, Yang Y, Kin U, Ytterberg AJ, Denny PA, Denny PC, Loo JA, Gunsalus RP, Loo RR. 2009. S-layer, surfaceaccessible, and concanavalin A binding proteins of Methanosarcina acetivorans and Methanosarcina mazei. J. Proteome Res. 8:1972-1982. http: //dx.doi.org/10.1021/pr800923e.
161. Rohlin L, Leon DR, Kim U, Loo JA, Ogorzalek-Loo RR, Gunsalus RP. 2012. Identification of the major expressed S-layer and cell surface-layerrelated proteins in the model methanogenic archaea: Methanosarcina barkeri Fusaro and Methanosarcina acetivorans C2A. Archaea 2012: 873589. http://dx.doi.org/10.1155/ 2012/873589.
162. Faguy DM, Bayley DP, Kostyukova AS, Thomas NA, Jarrell KF. 1996. Isolation and characterization of flagella and flagellin proteins from the thermoacidophilic archaea Thermoplasma volcanium and Sulfolobus shibatae. J. Bacteriol. 178:902-905.
163. Sergenova IS, Polosina YY, Kostyukova AS, Metlina AL, Pyatibratov MG, Fedorov OV. 1995. Flagella of halophilic archaea: biochemical and genetic analysis. Biochemistry (Mosc.) 60:953-957.
164. Peters J, Nitsch M, Kuhlmorgen B, Golbik R, Lupas A, Kellermann J, Engelhardt H, Pfander JP, Muller S, Goldie K. 1995. Tetrabrachion: a filamentous archaebacterial surface protein assembly of unusual structure and extreme stability. J. Mol. Biol. 245:385-401. http://dx.doi.org /10.1006/jmbi.1994.0032.
165. Kamekura M, Dyall-Smith M, Upasani V, Ventosa A, Kates M. 1997. Diversity of alkaliphilic halobacteria: proposals for transfer of Natronobacterium vacuolatum, Natronobacterium magadii, and Natronobacterium pharaonis to Halorubrum, Natrialba, and Natronomonas gen. nov., respectively, as Halorubrum vacuolatum comb. nov., Natrialba magadii comb. nov., and Natronomonas pharaonis comb. nov., respectively. Int. J. Syst. Bacteriol. 47:853-857. http://dx.doi.org/10.1099/00207713-47-3-853.
166. Kim BK, Pihl TD, Reeve JN, Daniels L. 1995. Purification of the copper response extracellular proteins secreted by the copper-resistant methanogen Methanobacterium bryantii BKYH and cloning, sequencing, and transcription of the gene encoding these proteins. J. Bacteriol. 177:7178-7185.
167. Claus H, Akça E, Debaerdemaeker T, Evrard C, Declercq JP, König H. 2002. Primary structure of selected archaeal mesophilic and extremely thermophilic outer surface layer proteins. Syst. Appl. Microbiol. 25:3-12. http://dx.doi.org/10.1078/0723-2020-00100.
168. Lechner J, Wieland F. 1989. Structure and biosynthesis of prokaryotic glycoproteins. Annu. Rev. Biochem. 58:173-194. http://dx.doi.org/10 .1146/annurev.bi.58.070189.001133.
169. Wieland F. 1988. Structure and biosynthesis of prokaryotic glycoproteins. Biochimie. 70:1493-1504. http://dx.doi.org/10.1016/0300-9084 (88)90286-6.
170. Paul G, Wieland F. 1987. Sequence of the halobacterial glycosaminoglycan. J. Biol. Chem. 262:9587-9593.
171. Paul G, Lottspeich F, Wieland F. 1986. Asparaginyl-Nacetylgalactosamine: linkage unit of halobacterial glycosaminoglycan. J. Biol. Chem. 261:1020-1024.
172. Lechner J, Wieland F, Sumper M. 1985. Transient methylation of dolichyl oligosaccharides is an obligatory step in halobacterial sulfated glycoprotein biosynthesis. J. Biol. Chem. 260:8984-8989.
173. Raetz CR, Whitfield C. 2002. Lipopolysaccharide endotoxins. Annu. Rev. Biochem. 71:635-700. http://dx.doi.org/10.1146/annurev.biochem .71.110601.135414.
174. Lechner J, Sumper M. 1987. The primary structure of a procaryotic glycoprotein. Cloning and sequencing of the cell surface glycoprotein gene of halobacteria. J. Biol. Chem. 262:9724-9729.
175. Mengele R, Sumper M. 1992. Drastic differences in glycosylation of related S-layer glycoproteins from moderate and extreme halophiles. J. Biol. Chem. 267:8182-8185.
176. Jervis AJ, Langdon R, Hitchen P, Lawson AJ, Wood A, Fothergill JL, Morris HR, Dell A, Wren B, Linton D. 2010. Characterization of N-linked protein glycosylation in Helicobacter pullorum. J. Bacteriol. 192: 5228-5236. http://dx.doi.org/10.1128/JB.00211-10.
177. Nair DB, Uchida K, Aizawa SI, Jarrell KF. 2014. Genetic analysis of a type IV pili-like locus in the archaeon Methanococcus mariplaudis. Arch. Microbiol. 196:179-191. http://dx.doi.org/10.1007/s00203-014-0956-4.
178. Hartmann E, Konig H. 1989. Uridine and dolichyl diphosphate activated oligosaccharides are intermediates in the biosynthesis of the S-layer glycoprotein of Methanothermus fervidus. Arch. Microbiol. 151:274-281. http://dx.doi.org/10.1007/BF00413142.
179. Pellerin P, Fournet B, Debeire P. 1990. Evidence for the glycoprotein nature of the cell sheath of Methanosaeta-like cells in the culture of Methanothrix soehngenii strain FE. Can. J. Microbiol. 39:631-636.
180. Hettmann T, Schmidt CL, Anemüller S, Zähringer U, Moll H, Petersen A, Schäfer G. 1998. Cytochrome b558/566 from the archaeon Sulfolobus acidocaldarius: a novel highly glycosylated, membrane-bound Btype hemoprotein. J. Biol. Chem. 273:12032-12040. http://dx.doi.org/10 .1074/jbc.273.20.12032.
181. Palmieri G, Balestrieri M, Peter-Katalinić J, Pohlentz G, Rossi M, Fiume I, Pocsfalvi G. 2013. Surface-exposed glycoproteins of hyperthermophilic Sulfolobus solfataricus P2 show a common N-glycosylation profile. J. Proteome Res. 12:2779-2790. http://dx.doi.org/10.1021 /pr400123z.
182. Vinogradov E, Deschatelets L, Lamoureux M, Patel GB, Tremblay TL, Robotham A, Goneau MF, Cummings-Lorbetskie C, Watson DC, Brisson JR, Kelly JF, Gilbert M. 2012. Cell surface glycoproteins from Thermoplasma acidophilum are modified with an N-linked glycan containing 6-C-sulfofucose. Glycobiology 22:1256-1267. http://dx.doi.org /10.1093/glycob/cws094.
183. Yang LL, Haug A. 1979. Purification and partial characterization of a procaryotic glycoprotein from the plasma membrane of Thermoplasma acidophilum. Biochim. Biophys. Acta 556:265-277. http://dx.doi.org/10 .1016/0005-2736(79) 90047-6.
184. Matsumoto S, Igura M, Nyirenda J, Matsumoto M, Yuzawa S, Noda N, Inagaki F, Kohda D. 2012. Crystal structure of the C-terminal globular domain of oligosaccharyltransferase from Archaeoglobus fulgidus at 1.75 Å resolution. Biochemistry 51:4157-4166. http://dx.doi.org/10 .1021/bi300076u.
185. Kohda D, Yamada M, Igura M, Kamishikiryo J, Maenaka K. 2007. New oligosaccharyltransferase assay method. Glycobiology 17:1175-1182. http://dx.doi.org/10.1093/glycob/cwm087.
186. Kandiba L, Aitio O, Helin J, Guan Z, Permi P, Bamford DH, Eichler J, Roine E. 2012. Diversity in prokaryotic glycosylation: an archaealderived N-linked glycan contains legionaminic acid. Mol. Microbiol. 84: 578-593. http://dx.doi.org/10.1111/j.1365-2958.2012.08045.x.
187. McNally DJ, Aubry AJ, Hui JP, Khieu NH, Whitfield D, Ewing CP, Guerry P, Brisson JR, Logan SM, Soo EC. 2007. Targeted metabolomics analysis of Campylobacter coli VC167 reveals legionaminic acid derivatives as novel flagellar glycans. J. Biol. Chem. 282:14463-14475. http://dx .doi.org/10.1074/jbc.M611027200.
188. Kandiba L, Eichler J. 2013. Analysis of putative nonulosonic acid biosynthesis pathways in Archaea reveals a complex evolutionary history. FEMS Microbiol. Lett. 345:110-120. http://dx.doi.org/10.1111/1574-6968.12193.
189. Mohorko E, Glockshuber R, Aebi M. 2011. Oligosaccharyltransferase: the central enzyme of N-linked protein glycosylation. J. Inherit. Metab. Dis. 34:869-878. http://dx.doi.org/10.1007/s10545-011-9337-1.
190. Igura M, Kohda D. 2011. Quantitative assessment of the preferences for the amino acid residues flanking archaeal N-linked glycosylation sites. Glycobiology 21:575-583. http://dx.doi.org/10.1093/glycob/cwq196.
191. Hese K, Otto C, Routier FH, Lehle L. 2009. The yeast oligosaccharyltransferase complex can be replaced by STT3 from Leishmania major. Glycobiology 19:160-171. http://dx.doi.org/10.1093/glycob/cwn118.
192. Maita N, Nyirenda J, Igura M, Kamishikiryo J, Kohda D. 2010. Comparative structural biology of eubacterial and archaeal oligosaccharyltransferases. J. Biol. Chem. 285:4941-4950. http://dx.doi.org/10.1074 /jbc.M109.081752.
193. Yan Q, Lennarz WJ. 2002. Studies on the function of oligosaccharyl transferase subunits. Stt3p is directly involved in the glycosylation process. J. Biol. Chem. 277:47692-47700. http://dx.doi.org/10.1074/jbc .M208136200.
194. Lizak C, Gerber S, Numao S, Aebi M, Locher KP. 2011. X-ray structure of a bacterial oligosaccharyltransferase. Nature 474:350-355. http://dx .doi.org/10.1038/nature10151.
195. Li L, Woodward R, Ding Y, Liu XW, Yi W, Bhatt VS, Chen M, Zhang LW, Wang PG. 2010. Overexpression and topology of bacterial oligosaccharyltransferase PglB. Biochem. Biophys. Res. Commun. 394:1069-1074. http://dx.doi.org/10.1016/j. bbrc.2010.03.126.
196. Kim H, von Heijne G, Nilsson I. 2005. Membrane topology of the STT3 subunit of the oligosaccharyl transferase complex. J. Biol. Chem. 280: 20261-20267. http://dx.doi.org/10.1074/jbc.M412213200.
197. Matsumoto S, Shimada A, Nyirenda J, Igura M, Kawano Y, Kohda D. 2013. Crystal structures of an archaeal oligosaccharyltransferase provides insights into the catalytic cycle of N-linked protein glycosylation. Proc. Natl. Acad. Sci. U. S. A. 110:17868-17873. http://dx.doi.org/10.1073 /pnas.1309777110.
198. Jaffee MB, Imperiali B. 2011. Exploiting topological constraints to reveal buried sequence motifs in the membrane-bound N-linked oligosaccharyl transferases. Biochemistry 50:7557-7567. http://dx.doi.org/10 .1021/bi201018d.
199. Izquierdo L, Schulz BL, Rodrigues JA, Güther ML, Procter JB, Barton GJ, Aebi M, Ferguson MA. 2009. Distinct donor and acceptor specificities of Trypanosoma brucei oligosaccharyltransferases. EMBO J. 28: 2650-2661. http://dx.doi.org/10.1038/emboj.2009.203.
200. Igura M, Kohda D. 2011. Selective control of oligosaccharide transfer efficiency for the N-glycosylation sequon by a point mutation in oligosaccharyltransferase. J. Biol. Chem. 286:13255-13260. http://dx.doi.org /10.1074/jbc.M110.213900.
201. Jaffee MB, Imperiali B. 2013. Optimized protocol for expression and purification of membrane-bound PglB, a bacterial oligosaccharyl transferase. Protein Expr. Purif. 89:241-250. http://dx.doi.org/10.1016/j.pep .2013.04.001.
202. Nyirenda J, Matsumoto S, Saitoh T, Maita N, Noda NN, Inagaki F, Kohda D. 2013. Crystallographic and NMR evidence for flexibility in oligosaccharyltransferases and its catalytic significance. Structure 21:32-41. http://dx.doi.org/10.1016/j.str.2012.10.011.
203. Igura M, Maita N, Obita T, Kamishikiryo J, Maenaka K, Kohda D. 2007. Purification, crystallization and preliminary X-ray diffraction studies of the soluble domain of the oligosaccharyltransferase STT3 subunit from the thermophilic archaeon Pyrococcus furiosus. Acta Crystallogr. Sect. F Struct. Biol. Cryst. Commun. 63:798-801. http://dx.doi.org /10.1107/S1744309107040134.
204. Chaban B, Ng SY, Jarrell KF. 2006. Archaeal habitats-from the extreme to the ordinary. Can. J. Microbiol. 52:73-116. http://dx.doi.org/10 .1139/w05-147.
205. Matsumoto S, Shimada A, Kohda D. 2013. Crystal structure of the C-terminal globular domain of the third paralog of the Archaeoglobus fulgidus oligosaccharyltransferases. BMC Struct. Biol. 13:11. http://dx .doi.org/10.1186/1472-6807-13-11.
206. Glover KJ, Weerapana E, Numao S, Imperiali B. 2005. Chemoenzymatic synthesis of glycopeptides with PglB, a bacterial oligosaccharyl transferase from Campylobacter jejuni. Chem. Biol. 12:1311-1315. http: //dx.doi.org/10.1016/ j.chembiol.2005.10.004.
207. Chavan M, Rekowicz M, Lennarz W. 2003. Insight into functional aspects of Stt3p, a subunit of the oligosaccharyl transferase. Evidence for interaction of the N-terminal domain of Stt3p with the protein kinase C cascade. J. Biol. Chem. 278:51441-51447. http://dx.doi.org/10.1074/jbc .M310456200.
208. Wacker M, Feldman MF, Callewaert N, Kowarik M, Clarke BR, Pohl NL, Hernandez M, Vines ED, Valvano MA, Whitfield C, Aebi M. 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. http://dx.doi.org/10.1073 /pnas.0509207103.
209. Kowarik M, Young NM, Numao S, Schulz BL, Hug I, Callewaert N, Mills DC, Watson DC, Hernandez M, Kelly JF, Wacker M, Aebi M. 2006. Definition of the bacterial N-glycosylation site consensus sequence.EMBOJ. 25:1957-1966. http://dx.doi.org/10.1038/sj.emboj.7601087.
210. Brockl G, Behr M, Fabry S, Hensel R, Kaudewitz H, Biendl E, Konig H. 1991. Analysis and nucleotide sequence of the genes encoding the surfacelayer glycoproteins of the hyperthermophilic methanogens Methanothermus fervidus and Methanothermus sociabilis. Eur. J. Biochem. 199:147-152. http: //dx.doi.org/10.1111/j.1432-1033.1991.tb16102.x.
211. Bardy SL, Jarrell KF. 2003. Cleavage of preflagellins by an aspartic acid signal peptidase is essential for flagellation in the archaeon Methanococcus voltae. Mol. Microbiol. 50:1339-1347. http://dx.doi.org/10.1046/j .1365-2958.2003.03758.x.
212. Valliere-Douglass JF, Eakin CM, Wallace A, Ketchem RR, Wang W, Treuheit MJ, Balland A. 2010. Glutamine-linked and non-consensus asparagine-linked oligosaccharides present in human recombinant antibodies define novel protein glycosylation motifs. J. Biol. Chem. 285: 16012-16022. http://dx.doi.org/10. 1074/jbc.M109.096412.
213. Schwarz F, Lizak C, Fan YY, Fleurkens S, Kowarik M, Aebi M. 2011. Relaxed acceptor site specificity of bacterial oligosaccharyltransferase in vivo. Glycobiology 21:45-54. http://dx.doi.org/10.1093/glycob /cwq130.
214. Zeitler R, Hochmuth E, Deutzmann R, Sumper M. 1998. Exchange of Ser-4 for Val, Leu or Asn in the sequon Asn-Ala-Ser does not prevent N-glycosylation of the cell surface glycoprotein from Halobacterium halobium. Glycobiology 8:1157-1164.
215. Tai VW, Imperiali B. 2001. Substrate specificity of the glycosyl donor for oligosaccharyl transferase. J. Org. Chem. 66:6217-6228. http://dx.doi .org/10.1021/jo0100345.
216. Feldman MF, Wacker M, Hernandez M, Hitchen PG, Marolda CL, Kowarik M, Morris HR, Dell A, Valvano MA, Aebi M. 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. http://dx.doi.org/10.1073/pnas.0500044102.
217. Schwarz F, Fan YY, Schubert M, Aebi M. 2011. Cytoplasmic Nglycosyltransferase of Actinobacillus pleuropneumoniae is an inverting enzyme and recognizes the NX(S/T) consensus sequence. J. Biol. Chem. 286:35267-35274. http://dx.doi.org/10.1074/jbc.M111.277160.
218. Wieland F, Heitzer R, Schaefer W. 1983. Asparaginylglucose: novel type of carbohydrate linkage. Proc. Natl. Acad. Sci. U. S. A. 80:5470-5474. http://dx.doi.org/10.1073/pnas.80.18.5470.
219. Wieland F, Paul G, Sumper M. 1985. Halobacterial flagellins are sulfated glycoproteins. J. Biol. Chem. 260:15180-15185.
220. Meyer W, Schäfer G. 1992. Characterization and purification of a membrane- bound archaebacterial pyrophosphatase from Sulfolobus acidocaldarius. Eur. J. Biochem. 207:741-746. http://dx.doi.org/10.1111/j.1432-1033.1992. tb17104.x.
221. Kaminski L, Naparstek S, Kandiba L, Cohen-Rosenzweig C, Arbiv A, Konrad Z, Eichler J. 2013. Add salt, add sugar: N-glycosylation in Haloferax volcanii. Biochem. Soc. Trans. 41:432-435. http://dx.doi.org/10 .1042/BST20120142.
222. Deatherage JF, Taylor KA, Amos LA. 1983. Three-dimensional arrangement of the cell wall protein of Sulfolobus acidocaldarius. J. Mol. Biol. 167:823-848. http://dx.doi.org/10.1016/S0022-2836(83)80113-2.
223. Albers SV, Meyer BH. 2011. The archaeal cell envelope. Nat. Rev. Microbiol. 9:414-426. http://dx.doi.org/10.1038/nrmicro2576.
224. Sleytr UB, Beveridge TJ. 1999. Bacterial S-layers. Trends Microbiol. 7:253-260. http://dx.doi.org/10.1016/S0966-842X(99)01513-9.
225. Claus H, Akca E, Debaerdemaeker T, Evrard C, Declercq JP, Harris JR, Schlott B, König H. 2005. Molecular organization of selected prokaryotic S-layer proteins. Can. J. Microbiol. 51:731-743. http://dx.doi.org/10 .1139/w05-093.
226. Engelhardt H, Peters J. 1998. Structural research on surface layers: a focus on stability, surface layer homology domains, and surface layer-cell wall interactions. J. Struct. Biol. 124:276-302. http://dx.doi.org/10.1006 /jsbi.1998.4070.
227. Akca E, Claus H, Schultz N, Karbach G, Schlott B, Debaerdemaeker T, Declercq JP, Konig H. 2002. Genes and derived amino acid sequences of S-layer proteins from mesophilic, thermophilic, and extremely thermophilic methanococci. Extremophiles 6:351-358. http://dx.doi.org/10 .1007/s00792-001-0264-1.
228. VanDyke DJ, Wu J, Ng SY, Kanbe M, Chaban B, Aizawa SI, Jarrell KF. 2008. Identification of putative acetyltransferase gene, MMP0350, which affects proper assembly of both flagella and pili in the archaeon Methanococcus maripaludis. J. Bacteriol. 190:5300-5307. http://dx.doi.org/10 .1128/JB.00474-08.
229. Jarrell KF, Stark M, Nair DB, Chong JPJ. 2011. Flagella and pili are both necessary for efficient attachment of Methanococcus maripaludis to surfaces. FEMS Microbiol. Lett. 319:44-50. http://dx.doi.org/10.1111/j .1574-6968.2011.02264.x.
230. Terra VS, Mills DC, Yates LE, Abouelhadid S, Cuccui J, Wren BW. 2012. Recent developments in bacterial protein glycan coupling technology and glycoconjugate vaccine design. J. Med. Microbiol. 61:919-926. http://dx.doi.org/10.1099/jmm.0.039438-0.
231. Jervis AJ, Butler JA, Lawson AJ, Langdon R, Wren BW, Linton D. 2012. Characterization of the structurally diverse N-linked glycans of Campylobacter species. J. Bacteriol. 194:2355-2362. http://dx.doi.org/10 .1128/JB.00042-12.
232. Valderrama-Rincon JD, Fisher AC, Merritt JH, Fan YY, Reading CA, Chhiba K, Heiss C, Azadi P, Aebi M, DeLisa MP. 2012. An engineered eukaryotic protein glycosylation pathway in Escherichia coli. Nat. Chem. Biol. 8:434-436. http://dx.doi.org/10.1038/nchembio.921.
233. Leigh JA, Albers SV, Atomi H, Allers T. 2011. Model organisms for genetics in the domain archaea: methanogens, halophiles, Thermococcales and Sulfolobales. FEMS Microbiol. Rev. 35:577-608. http://dx.doi .org/10.1111/j.1574-6976.2011.00265.x.