Permuting the PGF signature motif blocks both archaeosortase-dependent C-terminal cleavage and prenyl lipid attachment for the Haloferax volcanii S-layer glycoprotein

Journal of Bacteriology

Volumn 198, Issue 5, 2016, Pages 808-815

  Abdul Halim, Mohd Farid ^a   Karch, Kelly R ^b   Zhou, Yitian ^a   Haft, Daniel H ^c   Garcia, Benjamin A ^b   Pohlschroder, Mechthild ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c NATIONAL INSTITUTES OF HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARCHAEOSORTASE A; GLYCINE; GLYCOPROTEIN; MEVALONIC ACID; PEPTIDASE; PHENYLALANINE; PROLINE GLYCINE PHENYLALANINE; S LAYER GLYCOPROTEIN; SIGNAL PEPTIDASE I; THREONINE; TRIPEPTIDE; UNCLASSIFIED DRUG; ARCHAEAL PROTEIN; LIPID; MEMBRANE PROTEIN; PEPTIDE HYDROLASE; PROLINE; S-LAYER PROTEINS;

AMINO TERMINAL SEQUENCE; ARTICLE; BACTERIAL GROWTH; BACTERIAL STRAIN; BACTERIUM COLONY; CARBOXY TERMINAL SEQUENCE; CELL MEMBRANE; CELL SHAPE; CELL SIZE; CELL STRUCTURE; CELL TRANSFORMATION; CELL WALL; CHROMOSOME DELETION; COMPUTER MODEL; CONTROLLED STUDY; ENZYME ANALYSIS; GENE INSERTION; GENE MUTATION; GENE OVEREXPRESSION; GENETIC CODE; GENETIC VARIABILITY; GROWTH RATE; HALOFERAX VOLCANII; HOMOLOGOUS RECOMBINATION; ISOTOPE LABELING; MICROENVIRONMENT; MOLECULAR WEIGHT; NONHUMAN; PEPTIDE ANALYSIS; PHENOTYPE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN CLEAVAGE; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN GLYCOSYLATION; PROTEIN MODIFICATION; PROTEIN MOTIF; PROTEIN PROCESSING; PROTEIN STABILITY; PROTEIN STRUCTURE; THICKNESS; CHEMISTRY; CYTOLOGY; GENE EXPRESSION REGULATION; GENETICS; LIPID METABOLISM; METABOLISM; PHYSIOLOGY;

AMINO ACID MOTIFS; ARCHAEAL PROTEINS; CELL MEMBRANE; GENE EXPRESSION REGULATION, ARCHAEAL; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GLYCINE; HALOFERAX VOLCANII; LIPID METABOLISM; LIPIDS; MEMBRANE GLYCOPROTEINS; PEPTIDE HYDROLASES; PHENYLALANINE; PROLINE;

EID: 84961149365     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.00849-15     Document Type: Article

References (39)

1. Albers S-V, Meyer BH. 2011. The archaeal cell envelope. Nat Rev Microbiol 9:414-426. http://dx.doi.org/10.1038/nrmicro2576.
2. Foster TJ, Geoghegan JA, Ganesh VK, Höök M. 2014. Adhesion, invasion and evasion: the many functions of the surface proteins of Staphylococcus aureus. Nat Rev Microbiol 12:49-62. http://dx.doi.org/10.1038/nrmicro3161.
3. Thanassi DG, Bliska JB, Christie PJ. 2012. Surface organelles assembled by secretion systems of Gram-negative bacteria: diversity in structure and function. FEMS Microbiol Rev 36:1046-1082. http://dx.doi.org/10.1111/j.1574-6976.2012.00342.x.
4. Renthal R. 2010. Helix insertion into bilayers and the evolution of membrane proteins. Cell Mol Life Sci 67:1077-1088. http://dx.doi.org/10.1007/s00018-009-0234-9.
5. Pohlschröder M, Hartmann E, Hand NJ, Dilks K, Haddad A. 2005. Diversity and evolution of protein translocation. Annu Rev Microbiol 59:91-111. http://dx.doi.org/10.1146/annurev.micro.59.030804.121353.
6. Zückert WR. 2014. Secretion of bacterial lipoproteins: through the cytoplasmic membrane, the periplasm and beyond. Biochim Biophys Acta 1843:1509-1516. http://dx.doi.org/10.1016/j.bbamcr.2014.04.022.
7. Hutchings MI, Palmer T, Harrington DJ, Sutcliffe IC. 2009. Lipoprotein biogenesis in Gram-positive bacteria: knowing when to hold 'em, knowing when to fold 'em. Trends Microbiol 17:13-21. http://dx.doi.org/10.1016/j.tim.2008.10.001.
8. Buddelmeijer N. 2015. The molecular mechanism of bacterial lipoprotein modification-how, when and why? FEMS Microbiol Rev 39:246-261. http://dx.doi.org/10.1093/femsre/fuu006.
9. Schneewind O, Missiakas D. 2014. Sec-secretion and sortase-mediated anchoring of proteins in Gram-positive bacteria. Biochim Biophys Acta 1843:1687-1697. http://dx.doi.org/10.1016/j.bbamcr.2013.11.009.
10. Ton-That H, Liu G, Mazmanian SK, Faull KF, Schneewind O. 1999. Purification and characterization of sortase, the transpeptidase that cleaves surface proteins of Staphylococcus aureus at the LPXTG motif. Proc Natl Acad SciUSA96:12424-12429. http://dx.doi.org/10.1073/pnas.96.22.12424.
11. Perry AM, Ton-That H, Mazmanian SK, Schneewind O. 2002. Anchoring of surface proteins to the cell wall of Staphylococcus aureus. III. Lipid II is an in vivo peptidoglycan substrate for sortase-catalyzed surface protein anchoring. J Biol Chem 277:16241-16248.
12. Haft DH, Payne SH, Selengut JD. 2012. Archaeosortases and exosortases are widely distributed systems linking membrane transit with posttranslational modification. J Bacteriol 194:36-48. http://dx.doi.org/10.1128/JB.06026-11.
13. Haft DH, Paulsen IT, Ward N, Selengut JD. 2006. Exopolysaccharideassociated protein sorting in environmental organisms: the PEP-CTERM/EpsH system. Application of a novel phylogenetic profiling heuristic. BMC Biol 4:29.
14. Abdul Halim MF, Pfeiffer F, Zou J, Frisch A, Haft D, Wu S, Tolic N, Brewer H, Payne SH, Pasa-Tolic L, Pohlschroder M. 2013. Haloferax volcanii archaeosortase is required for motility, mating, and C-terminal processing of the S-layer glycoprotein. Mol Microbiol 88:1164-1175. http://dx.doi.org/10.1111/mmi.12248.
15. 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.
16. Kikuchi A, Sagami H, Ogura K. 1999. Evidence for covalent attachment of diphytanylglyceryl phosphate to the cell-surface glycoprotein of Halobacterium halobium. J Biol Chem 274:18011-18016. http://dx.doi.org/10.1074/jbc.274.25.18011.
17. Konrad Z, Eichler J. 2002. Lipid modification of proteins in Archaea: attachment of a mevalonic acid-based lipid moiety to the surface-layer glycoprotein of Haloferax volcanii follows protein translocation. Biochem J 366:959-964. http://dx.doi.org/10.1042/bj20020757.
18. Kandiba L, Guan Z, Eichler J. 2013. Lipid modification gives rise to two distinct Haloferax volcanii S-layer glycoprotein populations. Biochim Biophys Acta 1828:938-943. http://dx.doi.org/10.1016/j.bbamem.2012.11.023.
19. Nishimura Y, Eguchi T. 2006. Biosynthesis of archaeal membrane lipids: digeranylgeranylglycerophospholipid reductase of the thermoacidophilic archaeon Thermoplasma acidophilum. J Biochem 139:1073-1081. http://dx.doi.org/10.1093/jb/mvj118.
20. Dyall-Smith M. 2004. The Halohandbook-protocols for haloarchaeal genetics. University of Melbourne, Victoria, Australia. http://www.haloarchaea.com/resources/halohandbook/Halohandbook_2009_v7.2mds.pdf.
21. Blattner FR, Williams BG, Blechl AE, Denniston-Thompson K, Faber HE, Furlong L, Grunwald DJ, Kiefer DO, Moore DD, Schumm JW, Sheldon EL, Smithies O. 1977. Charon phages: safer derivatives of bacteriophage lambda for DNA cloning. Science 196:161-169. http://dx.doi.org/10.1126/science.847462.
22. Allers T, Ngo H-P, 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.
23. 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.
24. Allers T, Barak S, Liddell S, Wardell K, Mevarech M. 2010. Improved strains and plasmid vectors for conditional overexpression of His-tagged proteins in Haloferax volcanii. Appl Environ Microbiol 76:1759-1769. http://dx.doi.org/10.1128/AEM.02670-09.
25. 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.
26. Lin S, Garcia BA. 2012. Examining histone posttranslational modification patterns by high-resolution mass spectrometry. Methods Enzymol 512:3-28. http://dx.doi.org/10.1016/B978-0-12-391940-3.00001-9.
27. Shevchenko A, Tomas H, Havlis J, Olsen JV, Mann M. 2006. In-gel digestion for mass spectrometric characterization of proteins and proteomes. Nat Protoc 1:2856-2860.
28. Steinberg TH, Pretty On Top K, Berggren KN, Kemper C, Jones L, Diwu Z, Haugland RP, Patton WF. 2001. Rapid and simple single nanogram detection of glycoproteins in polyacrylamide gels and on electroblots. Proteomics 1:841-855.
29. Rath A, Glibowicka M, Nadeau VG, Chen G, Deber CM. 2009. Detergent binding explains anomalous SDS-PAGE migration of membrane proteins. Proc Natl Acad Sci U S A 106:1760-1765. http://dx.doi.org/10.1073/pnas.0813167106.
30. Storf S, Pfeiffer F, Dilks K, Chen ZQ, Imam S, Pohlschröder M. 2010. Mutational and bioinformatic analysis of haloarchaeal lipobox-containing proteins. Archaea 2010. http://dx.doi.org/10.1155/2010/410975.
31. 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.
32. 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:e00716-13. http://dx.doi.org/10.1128/mBio.00716-13.
33. Rosenshine I, Tchelet R, Mevarech M. 1989. The mechanism of DNA transfer in the mating system of an archaebacterium. Science 245:1387-1389. http://dx.doi.org/10.1126/science.2818746.
34. Duggin IG, Aylett CH, Walsh JC, Michie KA, Wang Q, Turnbull L, Dawson EM, Harry EJ, Whitchurch CB, Amos LA, Lowe J. 2015. CetZ tubulin-like proteins control archaeal cell shape. Nature 519:362-365. http://dx.doi.org/10.1038/nature13983.
35. Mescher MF, Strominger JL. 1976. Structural (shape-maintaining) role of the cell surface glycoprotein of Halobacterium salinarium. Proc Natl Acad Sci U S A 73:2687-2691. http://dx.doi.org/10.1073/pnas.73.8.2687.
36. Dalbey RE, Wang P, Kuhn A. 2011. Assembly of bacterial inner membrane proteins. Annu Rev Biochem 80:161-187. http://dx.doi.org/10.1146/annurev-biochem-060409-092524.
37. Luirink J, Yu Z, Wagner S, de Gier J-W. 2012. Biogenesis of inner membrane proteins in Escherichia coli. Biochim Biophys Acta 1817:965-976. http://dx.doi.org/10.1016/j.bbabio.2011.12.006.
38. Giménez MI, Dilks K, Pohlschröder M. 2007. Haloferax volcanii twinarginine translocation substates include secreted soluble, C-terminally anchored and lipoproteins. Mol Microbiol 66:1597-1606. http://dx.doi.org/10.1111/j.1365-2958.2007.06034.x.
39. Blyn LB, Braaten BA, Low DA. 1990. Regulation of pap pilin phase variation by a mechanism involving differential dam methylation states. EMBO J 9:4045-4054.