Acinetobacter strains carry two functional oligosaccharyltransferases, one devoted exclusively to type IV pilin, and the other one dedicated to O-glycosylation of multiple proteins

Molecular Microbiology

Volumn 96, Issue 5, 2015, Pages 1023-1041

  Harding, Christian M ^a,b   Nasr, Mohamed A ^c   Kinsella, Rachel L ^c   Scott, Nichollas E ^d   Foster, Leonard J ^d   Weber, Brent S ^c   Fiester, Steve E ^e   Actis, Luis A ^e   Tracy, Erin N ^a   Munson, Robert S ^a   Feldman, Mario F ^c  

^a THE RESEARCH INSTITUTE AT NATIONWIDE CHILDREN S HOSPITAL   (United States)

^b THE OHIO STATE UNIVERSITY COLLEGE OF MEDICINE   (United States)

^c UNIVERSITY OF ALBERTA   (Canada)

^d UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^e MIAMI UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADP1 PROTEIN; BACTERIAL ENZYME; HEXOSE; MAJOR POLYSACCHARIDE ANTIGEN; N ACETYLDEOXYHEXOSE; OLIGOSACCHARYLTRANSFERASE; PILA PROTEIN; PILIN; POLYSACCHARIDE; TETRASACCHARIDE; TFPO PROTEIN; TYPE IV PILIN; UNCLASSIFIED DRUG; BACTERIAL PROTEIN; DOLICHYL-DIPHOSPHOOLIGOSACCHARIDE - PROTEIN GLYCOTRANSFERASE; FIMBRIA PROTEIN; GLYCOPEPTIDE; GLYCOSYLTRANSFERASE; LIGASE; MEMBRANE PROTEIN;

ACINETOBACTER; ACINETOBACTER BAYLYI; ACINETOBACTER NOSOCOMIALIS; ARTICLE; BACTERIAL STRAIN; CONTROLLED STUDY; MASS SPECTROMETRY; NEISSERIA; NONHUMAN; PRIORITY JOURNAL; PROTEIN GLYCOSYLATION; PROTEIN PROCESSING; PROTEOMICS; PSEUDOMONAS AERUGINOSA; BIOLOGY; CHEMISTRY; ENZYMOLOGY; GENETICS; GLYCOSYLATION; METABOLISM; PATHOGENICITY;

ACINETOBACTER; BACTERIA (MICROORGANISMS); NEISSERIA; PSEUDOMONAS AERUGINOSA;

ACINETOBACTER; BACTERIAL PROTEINS; COMPUTATIONAL BIOLOGY; FIMBRIAE PROTEINS; GLYCOPEPTIDES; GLYCOSYLATION; GLYCOSYLTRANSFERASES; HEXOSYLTRANSFERASES; LIGASES; MEMBRANE PROTEINS; NEISSERIA; POLYSACCHARIDES;

EID: 84929704176     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/mmi.12986     Document Type: Article

References (72)

1. Aas, F.E., Egge-Jacobsen, W., Winther-Larsen, H.C., Løvold, C., Hitchen, P.G., Dell, A., and Koomey, M. (2006) Neisseria gonorrhoeae type IV pili undergo multisite, hierarchical modifications with phosphoethanolamine and phosphocholine requiring an enzyme structurally related to lipopolysaccharide phosphoethanolamine transferases. J Biol Chem 281: 27712-27723.
2. Abd-El-Haleem, D., Moawad, H., Zaki, E.A., and Zaki, S. (2002) Molecular characterization of phenol-degrading bacteria isolated from different Egyptian ecosystems. Microb Ecol 43: 217-224.
3. Arroyo, L.A., Mateos, I., González, V., and Aznar, J. (2009) In vitro activities of tigecycline, minocycline, and colistin-tigecycline combination against multi- and pandrug-resistant clinical isolates of Acinetobacter baumannii group. Antimicrob Agents Chemother 53: 1295-1296.
4. Balonova, L., Mann, B.F., Cerveny, L., Alley, W.R., Chovancova, E., Forslund, A.-L., etal. (2012) Characterization of protein glycosylation in Francisella tularensis subsp. holarctica: identification of a novel glycosylated lipoprotein required for virulence. Mol Cell Proteomics 11: M111.015016.
5. Boucher, C.A., Barberis, P.A., and Demery, D.A. (1985) Transposon Mutagenesis of Pseudomonas solanacearum: isolation of Tn5-Induced Avirulent Mutants. Microbiology 131: 2449-2457.
6. Børud, B., Viburiene, R., Hartley, M.D., Paulsen, B.S., Egge-Jacobsen, W., Imperiali, B., and Koomey, M. (2011) Genetic and molecular analyses reveal an evolutionary trajectory for glycan synthesis in a bacterial protein glycosylation system. Proc Natl Acad Sci USA 108: 9643-9648.
7. Brzoska, A.J., Hassan, K.A., de Leon, E.J., Paulsen, I.T., and Lewis, P.J. (2013) Single-step selection of drug resistant Acinetobacter baylyi ADP1 mutants reveals a functional redundancy in the recruitment of multidrug efflux systems. PLoS ONE 8: e56090.
8. Cagatay, T.I., and Hickford, J.G.H. (2008) Glycosylation of type-IV fimbriae of Dichelobacter nodosus. Vet Microbiol 126: 160-167.
9. Carruthers, M.D., Nicholson, P.A., Tracy, E.N., and Munson, R.S. (2013a) Acinetobacter baumannii Utilizes a Type VI Secretion System for Bacterial Competition. PLoS ONE 8: e59388.
10. Carruthers, M.D., Harding, C.M., Baker, B.D., Bonomo, R.A., Hujer, K.M., Rather, P.N., and Munson, R.S., Jr. (2013b) Draft genome sequence of the clinical isolate Acinetobacter nosocomialis strain M2. Genome Announc 1: e00906-13.
11. Castric, P. (1995) pilO, a gene required for glycosylation of Pseudomonas aeruginosa 1244 pilin. Microbiology 141: 1247-1254.
12. Charbonneau, M.-E., Girard, V., Nikolakakis, A., Campos, M., Berthiaume, F., Dumas, F., etal. (2007) O-linked glycosylation ensures the normal conformation of the autotransporter adhesin involved in diffuse adherence. J Bacteriol 189: 8880-8889.
13. Choi, A.H.K., Slamti, L., Avci, F.Y., Pier, G.B., and Maira-Litrán, T. (2009) The pgaABCD locus of Acinetobacter baumannii encodes the production of poly-beta-1-6-N-acetylglucosamine, which is critical for biofilm formation. J Bacteriol 191: 5953-5963.
14. Choi, C.H., Hyun, S.H., Lee, J.Y., Lee, J.S., Lee, Y.S., Kim, S.A., etal. (2008) Acinetobacter baumannii outer membrane protein A targets the nucleus and induces cytotoxicity. Cell Microbiol 10: 309-319.
15. Comer, J.E., Marshall, M.A., Blanch, V.J., Deal, C.D., and Castric, P. (2002) Identification of the Pseudomonas aeruginosa 1244 pilin glycosylation site. Infect Immun 70: 2837-2845.
16. Coyne, M.J., Fletcher, C.M., Chatzidaki-Livanis, M., Posch, G., Schaffer, C., and Comstock, L.E. (2013) Phylum-wide general protein O-glycosylation system of the Bacteroidetes. Mol Microbiol 88: 772-783.
17. Côté, J.-P., Charbonneau, M.-È., and Mourez, M. (2013) Glycosylation of the Escherichia coli TibA self-associating autotransporter influences the conformation and the functionality of the protein. PLoS ONE 8: e80739.
18. De Berardinis, V., Vallenet, D., Castelli, V., Besnard, M., Pinet, A., Cruaud, C., etal. (2008) A complete collection of single-gene deletion mutants of Acinetobacter baylyi ADP1. Mol Syst Biol 4: 174.
19. Egge-Jacobsen, W., Salomonsson, E.N., Aas, F.E., Forslund, A.-L., Winther-Larsen, H.C., Maier, J., etal. (2011) O-linked glycosylation of the PilA pilin protein of Francisella tularensis: identification of the endogenous protein-targeting oligosaccharyltransferase and characterization of the native oligosaccharide. J Bacteriol 193: 5487-5497.
20. Faridmoayer, A., Fentabil, M.A., Mills, D.C., Klassen, J.S., and Feldman, M.F. (2007) Functional characterization of bacterial oligosaccharyltransferases involved in O-linked protein glycosylation. J Bacteriol 189: 8088-8098.
21. Feldman, M.F., Wacker, M., Hernandez, M., Hitchen, P.G., Marolda, C.L., Kowarik, M., etal. (2005) Engineering N-linked protein glycosylation with diverse O antigen lipopolysaccharide structures in Escherichia coli. Proc Natl Acad Sci USA 102: 3016-3021.
22. Gebhart, C., Ielmini, M.V., Reiz, B., Price, N.L., Aas, F.E., Koomey, M., and Feldman, M.F. (2012) Characterization of exogenous bacterial oligosaccharyltransferases in Escherichia coli reveals the potential for O-linked protein glycosylation in Vibrio cholerae and Burkholderia thailandensis. Glycobiology 22: 962-974.
23. Gordon, N.C., and Wareham, D.W. (2010) Multidrug-resistant Acinetobacter baumannii: mechanisms of virulence and resistance. Int J Antimicrob Agents 35: 219-226.
24. Göttig, S., Gruber, T.M., Higgins, P.G., Wachsmuth, M., Seifert, H., and Kempf, V.A.J. (2014) Detection of pan drug-resistant Acinetobacter baumannii in Germany. J Antimicrob Chemother 69: 2578-2579.
25. Gross, J., Grass, S., Davis, A.E., Gilmore-Erdmann, P., Townsend, R.R., and St Geme, J.W. (2008) The Haemophilus influenzae HMW1 adhesin is a glycoprotein with an unusual N-linked carbohydrate modification. J Biol Chem 283: 26010-26015.
26. Harding, C.M., Tracy, E.N., Carruthers, M.D., Rather, P.N., Actis, L.A., and Munson, R.S. (2013) Acinetobacter baumannii strain M2 produces type IV pili which play a role in natural transformation and twitching motility but not surface-associated motility. mBio 4: e00360-13.
27. Hu, D., Liu, B., Dijkshoorn, L., Wang, L., and Reeves, P.R. (2013) Diversity in the major polysaccharide antigen of Acinetobacter baumannii assessed by DNA sequencing, and development of a molecular serotyping scheme. PLoS ONE 8: e70329.
28. Hug, I., and Feldman, M.F. (2011) Analogies and homologies in lipopolysaccharide and glycoprotein biosynthesis in bacteria. Glycobiology 21: 138-151.
29. Ielmini, M.V., and Feldman, M.F. (2011) Desulfovibrio desulfuricans PglB homolog possesses oligosaccharyltransferase activity with relaxed glycan specificity and distinct protein acceptor sequence requirements. Glycobiology 21: 734-742.
30. Iwashkiw, J.A., Seper, A., Weber, B.S., Scott, N.E., Vinogradov, E., Stratilo, C., etal. (2012) Identification of a General O-linked Protein Glycosylation System in Acinetobacter baumannii and Its Role in Virulence and Biofilm Formation. PLoS Pathog 8: e1002758.
31. Iwashkiw, J.A., Vozza, N.F., Kinsella, R.L., and Feldman, M.F. (2013) Pour some sugar on it: the expanding world of bacterial protein O-linked glycosylation. Mol Microbiol 89: 14-28.
32. Kus, J.V., Tullis, E., Cvitkovitch, D.G., and Burrows, L.L. (2004) Significant differences in type IV pilin allele distribution among Pseudomonas aeruginosa isolates from cystic fibrosis (CF) versus non-CF patients. Microbiology 150: 1315-1326.
33. Lees-Miller, R.G., Iwashkiw, J.A., Scott, N.E., Seper, A., Vinogradov, E., Schild, S., and Feldman, M.F. (2013) A common pathway for O-linked protein-glycosylation and synthesis of capsule in Acinetobacter baumannii. Mol Microbiol 89: 816-830.
34. Lithgow, K.V., Scott, N.E., Iwashkiw, J.A., Thomson, E.L.S., Foster, L.J., Feldman, M.F., and Dennis, J.J. (2014) A general protein O-glycosylation system within the Burkholderia cepacia complex is involved in motility and virulence. Mol Microbiol 92: 116-137.
35. Logan, S.M. (2006) Flagellar glycosylation - a new component of the motility repertoire? Microbiology 152: 1249-1262.
36. Mara, K., Decorosi, F., Viti, C., Giovannetti, L., Papaleo, M.C., Maida, I., etal. (2012) Molecular and phenotypic characterization of Acinetobacter strains able to degrade diesel fuel. Res Microbiol 163: 161-172.
37. Marchler-Bauer, A., and Bryant, S.H. (2004) CD-Search: protein domain annotations on the fly. Nucleic Acids Res 32 (W): 327-331.
38. Marchler-Bauer, A., Anderson, J.B., Chitsaz, F., Derbyshire, M.K., DeWeese-Scott, C., Fong, J.H., etal. (2009) CDD: specific functional annotation with the Conserved Domain Database. Nucleic Acids Res 37 (D): 205-210.
39. Marchler-Bauer, A., Lu, S., Anderson, J.B., Chitsaz, F., Derbyshire, M.K., DeWeese-Scott, C., etal. (2011) CDD: a Conserved Domain Database for the functional annotation of proteins. Nucleic Acids Res 39 (D): 225-229.
40. Mescher, M.F., and Strominger, J.L. (1976) Structural (shape-maintaining) role of the cell surface glycoprotein of Halobacterium salinarium. Proc Natl Acad Sci USA 73: 2687-2691.
41. Musumeci, M.A., Faridmoayer, A., Watanabe, Y., and Feldman, M.F. (2014) Evaluating the role of conserved amino acids in bacterial O-oligosaccharyltransferases by in vivo, in vitro and limited proteolysis assays. Glycobiology 24: 39-50.
42. Neuberger, A. (1938) Carbohydrates in protein: the carbohydrate component of crystalline egg albumin. Biochem J 32: 1435-1451.
43. Nguyen, L.C., Taguchi, F., Tran, Q.M., Naito, K., Yamamoto, M., Ohnishi-Kameyama, M., etal. (2012) Type IV pilin is glycosylated in Pseudomonas syringae pv. tabaci 6605 and is required for surface motility and virulence. Mol Plant Pathol 13: 764-774.
44. Nothaft, H., and Szymanski, C.M. (2010) Protein glycosylation in bacteria: sweeter than ever. Nat Rev Microbiol 8: 765-778.
45. Nothaft, H., Scott, N.E., Vinogradov, E., Liu, X., Hu, R., Beadle, B., etal. (2012) Diversity in the protein N-glycosylation pathways within the Campylobacter genus. Mol Cell Proteomics 11: 1203-1219.
46. Olsen, J., V, Macek, B., Lange, O., Makarov, A., Horning, S., and Mann, M. (2007) Higher-energy C-trap dissociation for peptide modification analysis. Nat Methods 4: 709-712.
47. Pérez, J.M., McGarry, M.A., Marolda, C.L., and Valvano, M.A. (2008) Functional analysis of the large periplasmic loop of the Escherichia coli K-12 WaaL O-antigen ligase. Mol Microbiol 70: 1424-1440.
48. Porstendorfer, D., Gohl, O., Mayer, F., and Averhoff, B. (2000) ComP, a pilin-like protein essential for natural competence in Acinetobacter sp. Strain BD413: regulation, modification, and cellular localization. J Bacteriol 182: 3673-3680.
49. Power, P., and Jennings, M. (2003) The genetics of glycosylation in Gram-negative bacteria. FEMS Microbiol Lett 218: 211-222.
50. Power, P.M., Seib, K.L., and Jennings, M.P. (2006) Pilin glycosylation in Neisseria meningitidis occurs by a similar pathway to wzy-dependent O-antigen biosynthesis in Escherichia coli. Biochem Biophys Res Commun 347: 904-908.
51. Rappsilber, J., Mann, M., and Ishihama, Y. (2007) Protocol for micro-purification, enrichment, pre-fractionation and storage of peptides for proteomics using StageTips. Nat Protoc 2: 1896-1906.
52. Ruan, X., Loyola, D.E., Marolda, C.L., Perez-Donoso, J.M., and Valvano, M.A. (2012) The WaaL O-antigen lipopolysaccharide ligase has features in common with metal ion-independent inverting glycosyltransferases. Glycobiology 22: 288-299.
53. Schulz, B.L., Jen, F.E.C., Power, P.M., Jones, C.E., Fox, K.L., Ku, S.C., etal. (2013) Identification of bacterial protein O-oligosaccharyltransferases and their glycoprotein substrates. PLoS ONE 8: e62768.
54. Scott, N.E., Parker, B.L., Connolly, A.M., Paulech, J., Edwards, A.V.G., Crossett, B., etal. (2011) Simultaneous glycan-peptide characterization using hydrophilic interaction chromatography and parallel fragmentation by CID, higher energy collisional dissociation, and electron transfer dissociation MS applied to the N-linked glycoproteome of Campylobacter jejuni. Mol Cell Proteomics 10: M000031-MCP201.
55. Scott, N.E., Nothaft, H., Edwards, A.V.G., Labbate, M., Djordjevic, S.P., Larsen, M.R., etal. (2012) Modification of the Campylobacter jejuni N-linked glycan by EptC protein-mediated addition of phosphoethanolamine. J Biol Chem 287: 29384-29396.
56. Scott, N.E., Kinsella, R.L., Edwards, A.V.G., Larsen, M.R., Dutta, S., Saba, J., etal. (2014) Diversity Within the O-linked Protein Glycosylation Systems of Acinetobacter Species. Mol Cell Proteomics 13: 2354-2370.
57. Shevchenko, A., Tomas, H., Havlis, J., Olsen, J.V., and Mann, M. (2006) In-gel digestion for mass spectrometric charac-terization of proteins and proteomes. Nat Protoc 1: 2856-2860.
58. Sleytr, U.B. (1975) Heterologous reattachment of regular arrays of glycoproteins on bacterial surfaces. Nature 257: 400-402.
59. Smedley, J.G., Jewell, E., Roguskie, J., Horzempa, J., Syboldt, A., Stolz, D.B., and Castric, P. (2005) Influence of pilin glycosylation on Pseudomonas aeruginosa 1244 pilus function. Infect Immun 73: 7922-7931.
60. Szymanski, C.M., Yao, R., Ewing, C.P., Trust, T.J., and Guerry, P. (1999) Evidence for a system of general protein glycosylation in Campylobacter jejuni. Mol Microbiol 32: 1022-1030.
61. Tang, G., and Mintz, K.P. (2010) Glycosylation of the collagen adhesin EmaA of Aggregatibacter actinomycetemcomitans is dependent upon the lipopolysaccharide biosynthetic pathway. J Bacteriol 192: 1395-1404.
62. Tsai, C.M., and Frasch, C.E. (1982) A sensitive silver stain for detecting lipopolysaccharides in polyacrylamide gels. Anal Biochem 119: 115-119.
63. Vaneechoutte, M., Young, D.M., Ornston, L.N., De Baere, T., Nemec, A., Van Der Reijden, T., etal. (2006) Naturally Transformable Acinetobacter sp. Strain ADP1 Belongs to the Newly Described Species Acinetobacter baylyi. Appl Environ Microbiol 72: 932-936.
64. Varki, A. (1993) Biological roles of oligosaccharides: all of the theories are correct. Glycobiology 3: 97-130.
65. Vik, A., Aas, F.E., Anonsen, J.H., Bilsborough, S., Schneider, A., Egge-Jacobsen, W., and Koomey, M. (2009) Broad spectrum O-linked protein glycosylation in the human pathogen Neisseria gonorrhoeae. Proc Natl Acad Sci USA 106: 4447-4452.
66. Voisin, S., Kus, J., V, Houliston, S., St-Michael, F., Watson, D., Cvitkovitch, D.G., etal. (2007) Glycosylation of Pseudomonas aeruginosa strain Pa5196 type IV pilins with Mycobacterium-like alpha-1, 5-linked d-Araf oligosaccharides. J Bacteriol 189: 151-159.
67. Wang, N., Mackenzie, L., De Souza, A.G., Zhong, H., Goss, G., and Li, L. (2007) Proteome profile of cytosolic component of zebrafish liver generated by LC-ESI MS/MS combined with trypsin digestion and microwave-assisted acid hydrolysis. J Proteome Res 6: 263-272.
68. Weber, B.S., Miyata, S.T., Iwashkiw, J.A., Mortensen, B.L., Skaar, E.P., Pukatzki, S., and Feldman, M.F. (2013) Genomic and functional analysis of the type VI secretion system in Acinetobacter. PLoS ONE 8: e55142.
69. Whitfield, C. (1995) Biosynthesis of lipopolysaccharide O antigens. Trends Microbiol 3: 178-185.
70. Wisplinghoff, H., Paulus, T., Lugenheim, M., Stefanik, D., Higgins, P.G., Edmond, M.B., etal. (2012) Nosocomial bloodstream infections due to Acinetobacter baumannii, Acinetobacter pittii and Acinetobacter nosocomialis in the United States. J Infect 64: 282-290.
71. Yi, E.C., and Hackett, M. (2000) Rapid isolation method for lipopolysaccharide and lipid A from Gram-negative bacteria. Analyst 125: 651-656.
72. Zhou, M., and Wu, H. (2009) Glycosylation and biogenesis of a family of serine-rich bacterial adhesins. Microbiology 155: 317-327.