Dual roles of Pseudomonas aeruginosa AlgE in secretion of the virulence factor alginate and formation of the secretion complex

Applied and Environmental Microbiology

Volumn 79, Issue 6, 2013, Pages 2002-2011

  Rehman, Zahid U ^a   Rehm, Bernd H A ^a  

^a MASSEY UNIVERSITY   (New Zealand)

Author keywords

[No Author keywords available]

Indexed keywords

ACID RESIDUES; ALGINATE BIOSYNTHESIS; AMINO ACID RESIDUES; CELL ENVELOPES; CHROMOSOMAL INTEGRATION; COPY NUMBER; DUAL ROLE; EXTRACELLULAR POLYSACCHARIDES; INNER MEMBRANES; MOLECULAR MECHANISM; MULTI-PROTEIN COMPLEX; OUTER MEMBRANE; PSEUDOMONAS AERUGINOSA; SITE-SPECIFIC; SOLID MEDIA; STABILITY ANALYSIS; TRANSMEMBRANES; TRIPLE MUTANTS; VIRULENCE FACTORS;

AMINO ACIDS; BACTERIA; BIOCHEMISTRY; EPITOPES; PHYSIOLOGY; PROTEINS;

ALGINATE;

ALGINIC ACID; CARRIER PROTEIN; GLUCURONIC ACID; HEXURONIC ACID; MULTIPROTEIN COMPLEX; MUTANT PROTEIN; VIRULENCE FACTOR;

ALGINATE; CHROMOSOME; MEMBRANE; MOLECULAR ANALYSIS; PROTEIN; SECRETION; VIRULENCE;

ARTICLE; CHEMICAL STRUCTURE; GENE DELETION; GENETIC COMPLEMENTATION; GENETICS; METABOLISM; NUCLEOTIDE SEQUENCE; PATHOGENICITY; PROTEIN CONFORMATION; PROTEIN MULTIMERIZATION; PSEUDOMONAS AERUGINOSA; SECRETION (PROCESS); TRANSPORT AT THE CELLULAR LEVEL;

ALGINATES; BIOLOGICAL TRANSPORT; DNA MUTATIONAL ANALYSIS; GENE DELETION; GENETIC COMPLEMENTATION TEST; GLUCURONIC ACID; HEXURONIC ACIDS; MEMBRANE TRANSPORT PROTEINS; MODELS, MOLECULAR; MULTIPROTEIN COMPLEXES; MUTANT PROTEINS; PROTEIN CONFORMATION; PROTEIN MULTIMERIZATION; PSEUDOMONAS AERUGINOSA; VIRULENCE FACTORS;

EID: 84874800387     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.03960-12     Document Type: Article

References (37)

1. Hay ID, Rehman ZU, Ghafoor A, Rehm BHA. 2010. Bacterial biosynthesis of alginates. J. Chem. Technol. Biotechnol. 85752-759.
2. Ghafoor A, Hay ID, Rehm BH. 2011. Role of exopolysaccharides in Pseudomonas aeruginosa biofilm formation and architecture. Appl. Environ. Microbiol. 77:5238 -5246.
3. Pier GB, Coleman F, Grout M, Franklin M, Ohman DE. 2001. Role of alginate O acetylation in resistance of mucoid Pseudomonas aeruginosa to opsonic phagocytosis. Infect. Immun. 69:1895-1901.
4. Chitnis CE, Ohman DE. 1993. Genetic analysis of the alginate biosynthetic gene cluster of Pseudomonas aeruginosa shows evidence of an operonic structure. Mol. Microbiol. 8:583-593.
5. Franklin MJ, Nivens DE, Weadge JT, Howell PL. 2011. Biosynthesis of the Pseudomonas aeruginosa extracellular polysaccharides, alginate, Pel, and Psl. Front. Microbiol. 2:167. doi:10.3389/fmicb.2011.00167.
6. Rehm BH. 2010. Bacterial polymers: biosynthesis, modifications and applications. Nat. Rev. Microbiol. 8:578-592.
7. Olvera C, Goldberg JB, Sanchez R, Soberon-Chavez G. 1999. The Pseudomonas aeruginosa algC gene product participates in rhamnolipid biosynthesis. FEMS Microbiol. Lett. 179:85-90.
8. Ma L, Wang J, Wang S, Anderson EM, Lam JS, Parsek MR, Wozniak DJ. 2012. Synthesis of multiple Pseudomonas aeruginosa biofilm matrix exopolysaccharides is post-transcriptionally regulated. Environ. Microbiol. 14:1995-2005.
9. Remminghorst U, Rehm BH. 2006. Alg44, a unique protein required for alginate biosynthesis in Pseudomonas aeruginosa. FEBS Lett. 580:3883- 3888.
10. Remminghorst U, Rehm BH. 2006. In vitro alginate polymerization and the functional role of Alg8 in alginate production by Pseudomonas aeruginosa. Appl. Environ. Microbiol. 72:298 -305.
11. Merighi M, Lee VT, Hyodo M, Hayakawa Y, Lory S. 2007. The second messenger bis-(3=-5=)-cyclic-GMP and its PilZ domain-containing receptor Alg44 are required for alginate biosynthesis in Pseudomonas aeruginosa. Mol. Microbiol. 65:876-895.
12. Oglesby LL, Jain S, Ohman DE. 2008. Membrane topology and roles of Pseudomonas aeruginosa Alg8 and Alg44 in alginate polymerization. Microbiology 154:1605-1615.
13. Keiski CL, Harwich M, Jain S, Neculai AM, Yip P, Robinson H, Whitney JC, Riley L, Burrows LL, Ohman DE, Howell PL. 2010. AlgK is a TPR-containing protein and the periplasmic component of a novel exopolysaccharide secretin. Structure 18:265-273.
14. Hay ID, Schmidt O, Filitcheva J, Rehm BH. 2012. Identification of a periplasmic AlgK-AlgX-MucD multiprotein complex in Pseudomonas aeruginosa involved in biosynthesis and regulation of alginate. Appl. Microbiol. Biotechnol. 93:215-227.
15. Gutsche J, Remminghorst U, Rehm BH. 2006. Biochemical analysis of alginate biosynthesis protein AlgX from Pseudomonas aeruginosa: purification of an AlgX-MucD (AlgY) protein complex. Biochimie 88:245-251.
16. Hay ID, Rehman ZU, Rehm BH. 2010. Membrane topology of outer membrane protein AlgE, which is required for alginate production in Pseudomonas aeruginosa. Appl. Environ. Microbiol. 76:1806 -1812.
17. Jain S, Ohman DE. 1998. Deletion of algK in mucoid Pseudomonas aeruginosa blocks alginate polymer formation and results in uronic acid secretion. J. Bacteriol. 180:634-641.
18. Monday SR, Schiller NL. 1996. Alginate synthesis in Pseudomonas aeruginosa: the role of AlgL (alginate lyase) and AlgX. J. Bacteriol. 178:625- 632.
19. Robles-Price A, Wong TY, Sletta H, Valla S, Schiller NL. 2004. AlgX is a periplasmic protein required for alginate biosynthesis in Pseudomonas aeruginosa. J. Bacteriol. 186:7369 -7377.
20. Albrecht MT, Schiller NL. 2005. Alginate lyase (AlgL) activity is required for alginate biosynthesis in Pseudomonas aeruginosa. J. Bacteriol.187: 3869-3872.
21. Jain S, Ohman DE. 2005. Role of an alginate lyase for alginate transport in mucoid Pseudomonas aeruginosa. Infect. Immun. 73:6429-6436.
22. Franklin MJ, Chitnis CE, Gacesa P, Sonesson A, White DC, Ohman DE. 1994. Pseudomonas aeruginosa AlgG is a polymer level alginate C5- mannuronan epimerase. J. Bacteriol. 176:1821-1830.
23. Franklin MJ, Ohman DE. 2002. Mutant analysis and cellular localization of the AlgI, AlgJ, and AlgF proteins required forOacetylation of alginate in Pseudomonas aeruginosa. J. Bacteriol. 184:3000 -3007.
24. Whitney JC, Hay ID, Li C, Eckford PD, Robinson H, Amaya MF, Wood LF, Ohman DE, Bear CE, Rehm BH, Howell PL. 2011. Structural basisfor alginate secretion across the bacterial outer membrane. Proc. Natl. Acad. Sci. U. S. A. 108:13083-13088.
25. Chiu J, Tillett D, Dawes IW, March PE. 2008. Site-directed, ligaseindependent mutagenesis (SLIM) for highly efficient mutagenesis of plasmids greater than 8kb. J. Microbiol. Methods 73:195-198.
26. Blumenkrantz N, Asboe-Hansen G. 1973. New method for quantitative determination of uronic acids. Anal. Biochem. 54:484-489.
27. Hoang TT, Kutchma AJ, Becher A, Schweizer HP. 2000. Integrationproficient plasmids for Pseudomonas aeruginosa: site-specific integration and use for engineering of reporter and expression strains. Plasmid ;43:59 -72.
28. Schlegel HG, Kaltwasser H, Gottschalk G. 1961. A submersion method for culture of hydrogen-oxidizing bacteria: growth physiological studies. Arch. Mikrobiol. ;38:209 -222.
29. du Plessis DJ, Nouwen N, Driessen AJ. 2011. The Sec translocase. Biochim. Biophys. Acta ;1808:851- 865.
30. Knowles TJ, Scott-Tucker A, Overduin M, Henderson IR. 2009. Membrane protein architects: the role of the BAM complex in outer membrane protein assembly. Nat. Rev. Microbiol. 7:206 -214.
31. Eren E, Vijayaraghavan J, Liu J, Cheneke BR, Touw DS, Lepore BW, Indic M, Movileanu L, van den Berg B. 2012. Substrate specificity within a family of outer membrane carboxylate channels. PLoS Biol. 10: e1001242. doi:10.1371/journal.pbio.1001242.
32. Hancock RE, Brinkman FS. 2002. Function of Pseudomonas porins in uptake and efflux. Annu. Rev. Microbiol. 56:17-38.
33. Denker K, Orlik F, Schiffler B, Benz R. 2005. Site-directed mutagenesis of the greasy slide aromatic residues within the LamB (maltoporin) channel of Escherichia coli: effect on ion and maltopentaose transport. J. Mol. Biol. 352:534 -550.
34. Hentzer M, Teitzel GM, Balzer GJ, Heydorn A, Molin S, Givskov M, Parsek MR. 2001. Alginate overproduction affects Pseudomonas aeruginosa biofilm structure and function. J. Bacteriol. 183:5395-5401.
35. Struyve M, Moons M, Tommassen J. 1991. Carboxy-terminal phenylalanine is essential for the correct assembly of a bacterial outer membrane protein. J. Mol. Biol. 218:141-148.
36. Abu Khweek A, Fetherston JD, Perry RD. 2010. Analysis of HmsH and its role in plague biofilm formation. Microbiology 156:1424 -1438.
37. Cuthbertson L, Mainprize IL, Naismith JH, Whitfield C. 2009. Pivotal roles of the outer membrane polysaccharide export and polysaccharide copolymerase protein families in export of extracellular polysaccharides in Gram-negative bacteria. Microbiol. Mol. Biol. Rev. 73:155-177.