Sialic acid catabolism in Staphylococcus aureus

Journal of Bacteriology

Volumn 195, Issue 8, 2013, Pages 1779-1788

  Olson, Michael E ^a   King, Jessica M ^a   Yahr, Timothy L ^a   Horswill, Alexander R ^a  

^a UNIVERSITY OF IOWA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

N ACETYLNEURAMINIC ACID; SIALIC ACID;

ARTICLE; BACTERIAL GROWTH; CARBON SOURCE; CATABOLISM; CHROMOSOME; CONTROLLED STUDY; DELETION MUTANT; ELECTROPHORETIC MOBILITY; FUSION GENE; GENE CLUSTER; GENE DELETION; GENE EXPRESSION; GENE LOCUS; GENETIC TRANSCRIPTION; GROWTH INHIBITION; HOST; NONHUMAN; NORTHERN BLOTTING; NUCLEOTIDE SEQUENCE; PHENOTYPE; PRIORITY JOURNAL; PROMOTER REGION; STAPHYLOCOCCUS AUREUS; SURVIVAL;

BACTERIAL PROTEINS; BLOTTING, NORTHERN; CARBON; DNA, BACTERIAL; GENE DELETION; GENE EXPRESSION REGULATION, BACTERIAL; MULTIGENE FAMILY; N-ACETYLNEURAMINIC ACID; PHOSPHOTRANSFERASES (ALCOHOL GROUP ACCEPTOR); PLASMIDS; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; RNA, BACTERIAL; STAPHYLOCOCCUS AUREUS; TRANSCRIPTION INITIATION SITE;

BACTERIA (MICROORGANISMS); STAPHYLOCOCCUS AUREUS;

EID: 84876088524     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.02294-12     Document Type: Article

References (62)

1. Lowy FD. 1998. Staphylococcus aureus infections. N. Engl. J. Med. 339: 520-532.
2. Chambers HF, Deleo FR. 2009. Waves of resistance: Staphylococcus aureus in the antibiotic era. Nat. Rev. Microbiol. 7:629-641.
3. DeLeo FR, Chambers HF. 2009. Reemergence of antibiotic-resistant Staphylococcus aureus in the genomics era. J. Clin. Invest. 119:2464-2474.
4. Andrews JI, Fleener DK, Messer SA, Kroeger JS, Diekema DJ. 2009. Screening for Staphylococcus aureus carriage in pregnancy: usefulness of novel sampling and culture strategies. Am. J. Obstet. Gynecol. 201:396.e1-396.e5. doi:10.1016/j.ajog.2009.06.062.
5. Tenover FC, McAllister S, Fosheim G, McDougal LK, Carey RB, Limbago B, Lonsway D, Patel JB, Kuehnert MJ, Gorwitz R. 2008. Characterization of Staphylococcus aureus isolates from nasal cultures collected from individuals in the United States in 2001 to 2004. J. Clin. Microbiol. 46:2837-2841.
6. Holtfreter S, Grumann D, Schmudde M, Nguyen HT, Eichler P, Strommenger B, Kopron K, Kolata J, Giedrys-Kalemba S, Steinmetz I, Witte W, Broker BM. 2007. Clonal distribution of superantigen genes in clinical Staphylococcus aureus isolates. J. Clin. Microbiol. 45:2669-2680.
7. von Eiff C, Becker K, Machka K, Stammer H, Peters G. 2001. Nasal carriage as a source of Staphylococcus aureus bacteremia. N. Engl. J. Med. 344:11-16.
8. Bode LG, Kluytmans JA, Wertheim HF, Bogaers D, Vandenbroucke- Grauls CM, Roosendaal R, Troelstra A, Box AT, Voss A, van der Tweel I, van Belkum A, Verbrugh HA, Vos MC. 2010. Preventing surgical-site infections in nasal carriers of Staphylococcus aureus. N. Engl. J. Med. 362: 9-17.
9. Weinstein HJ. 1959. Control of nasal staphylococcal-carrier states. N. Engl. J. Med. 260:1308-1310.
10. Wertheim HF, Vos MC, Ott A, van Belkum A, Voss A, Kluytmans JA, van Keulen PH, Vandenbroucke-Grauls CM, Meester MH, Verbrugh HA. 2004. Risk and outcome of nosocomial Staphylococcus aureus bacteraemia in nasal carriers versus non-carriers. Lancet 364:703-705.
11. Kluytmans JA, Mouton JW, Ijzerman EP, Vandenbroucke-Grauls CM, Maat AW, Wagenvoort JH, Verbrugh HA. 1995. Nasal carriage of Staphylococcus aureus as a major risk factor for wound infections after cardiac surgery. J. Infect. Dis. 171:216-219.
12. Burian M, Wolz C, Goerke C. 2010. Regulatory adaptation of Staphylococcus aureus during nasal colonization of humans. PLoS One 5:e10040.
13. Burian M, Rautenberg M, Kohler T, Fritz M, Krismer B, Unger C, Hoffmann WH, Peschel A, Wolz C, Goerke C. 2010. Temporal expression of adhesion factors and activity of global regulators during establishment of Staphylococcus aureus nasal colonization. J. Infect. Dis. 201: 1414-1421.
14. Vimr ER, Kalivoda KA, Deszo EL, Steenbergen SM. 2004. Diversity of microbial sialic acid metabolism. Microbiol. Mol. Biol. Rev. 68:132-153.
15. Schauer R. 2000. Achievements and challenges of sialic acid research. Glycoconj. J. 17:485-499.
16. Varki NM, Varki A. 2007. Diversity in cell surface sialic acid presentations: implications for biology and disease. Lab. Invest. 87:851-857.
17. Sillanaukee P, Ponnio M, Jaaskelainen IP. 1999. Occurrence of sialic acids in healthy humans and different disorders. Eur. J. Clin. Invest. 29: 413-425.
18. Burnaugh AM, Frantz LJ, King SJ. 2008. Growth of Streptococcus pneumoniae on human glycoconjugates is dependent upon the sequential activity of bacterial exoglycosidases. J. Bacteriol. 190:221-230.
19. Vimr E, Lichtensteiger C. 2002. To sialylate, or not to sialylate: that is the question. Trends Microbiol. 10:254-257.
20. Chang DE, Smalley DJ, Tucker DL, Leatham MP, Norris WE, Stevenson SJ, Anderson AB, Grissom JE, Laux DC, Cohen PS, Conway T. 2004. Carbon nutrition of Escherichia coli in the mouse intestine. Proc. Natl. Acad. Sci. U. S. A. 101:7427-7432.
21. Almagro-Moreno S, Boyd EF. 2009. Sialic acid catabolism confers a competitive advantage to pathogenic Vibrio cholerae in the mouse intestine. Infect. Immun. 77:3807-3816.
22. Manco S, Hernon F, Yesilkaya H, Paton JC, Andrew PW, Kadioglu A. 2006. Pneumococcal neuraminidases A and B both have essential roles during infection of the respiratory tract and sepsis. Infect. Immun. 74: 4014-4020.
23. Vimr E, Steenbergen S, Cieslewicz M. 1995. Biosynthesis of the polysialic acid capsule in Escherichia coli K1. J. Ind. Microbiol. 15:352-360.
24. Vimr E, Lichtensteiger C, Steenbergen S. 2000. Sialic acid metabolism's dual function in Haemophilus influenzae. Mol. Microbiol. 36:1113-1123.
25. Schenk S, Laddaga RA. 1992. Improved method for electroporation of Staphylococcus aureus. FEMS Microbiol. Lett. 73:133-138.
26. Novick RP. 1991. Genetic systems in staphylococci. Methods Enzymol. 204:587-636.
27. Bae T, Schneewind O. 2006. Allelic replacement in Staphylococcus aureus with inducible counter-selection. Plasmid 55:58-63.
28. Scotto-Lavino E, Du G, Frohman MA. 2006. 5= end cDNA amplification using classic RACE. Nat. Protoc. 1:2555-2562.
29. Brutinel ED, Vakulskas CA, Brady KM, Yahr TL. 2008. Characterization of ExsA and of ExsA-dependent promoters required for expression of the Pseudomonas aeruginosa type III secretion system. Mol. Microbiol. 68: 657-671.
30. Ringenberg MA, Steenbergen SM, Vimr ER. 2003. The first committed step in the biosynthesis of sialic acid by Escherichia coli K1 does not involve a phosphorylated N-acetylmannosamine intermediate. Mol. Microbiol. 50:961-975.
31. Almagro-Moreno S, Boyd EF. 2009. Insights into the evolution of sialic acid catabolism among bacteria. BMC Evol. Biol. 9:118. doi:10.1186/1471 -2148-9-118.
32. Diep BA, Gill SR, Chang RF, Phan TH, Chen JH, Davidson MG, Lin F, Lin J, Carleton HA, Mongodin EF, Sensabaugh GF, Perdreau- Remington F. 2006. Complete genome sequence of USA300, an epidemic clone of community-acquired meticillin-resistant Staphylococcus aureus. Lancet 367:731-739.
33. Johnston JW, Zaleski A, Allen S, Mootz JM, Armbruster D, Gibson BW, Apicella MA, Munson RS, Jr. 2007. Regulation of sialic acid transport and catabolism in Haemophilus influenzae. Mol. Microbiol. 66:26-39.
34. Komatsuzawa H, Fujiwara T, Nishi H, Yamada S, Ohara M, McCallum N, Berger-Bachi B, Sugai M. 2004. The gate controlling cell wall synthesis in Staphylococcus aureus. Mol. Microbiol. 53:1221-1231.
35. Kennedy AD, Otto M, Braughton KR, Whitney AR, Chen L, Mathema B, Mediavilla JR, Byrne KA, Parkins LD, Tenover FC, Kreiswirth BN, Musser JM, DeLeo FR. 2008. Epidemic community-associated methicillin- resistant Staphylococcus aureus: recent clonal expansion and diversification. Proc. Natl. Acad. Sci. U. S. A. 105:1327-1332.
36. Kelley LA, Sternberg MJ. 2009. Protein structure prediction on the Web: a case study using the Phyre server. Nat. Protoc. 4:363-371.
37. Sørensen KI, Hove-Jensen B. 1996. Ribose catabolism of Escherichia coli: characterization of the rpiB gene encoding ribose phosphate isomerase B and of the rpiR gene, which is involved in regulation of rpiB expression. J. Bacteriol. 178:1003-1011.
38. Byers HL, Homer KA, Beighton D. 1996. Utilization of sialic acid by viridans streptococci. J. Dent. Res. 75:1564-1571.
39. Byers HL, Homer KA, Tarelli E, Beighton D. 1999. N-acetylneuraminic acid transport by Streptococcus oralis strain AR3. J. Med. Microbiol. 48: 375-381.
40. Severi E, Randle G, Kivlin P, Whitfield K, Young R, Moxon R, Kelly D, Hood D, Thomas GH. 2005. Sialic acid transport in Haemophilus influenzae is essential for lipopolysaccharide sialylation and serum resistance and is dependent on a novel tripartite ATP-independent periplasmic transporter. Mol. Microbiol. 58:1173-1185.
41. Ward RE, Ninonuevo M, Mills DA, Lebrilla CB, German JB. 2007. In vitro fermentability of human milk oligosaccharides by several strains of bifidobacteria. Mol. Nutr. Food Res. 51:1398-1405.
42. Frank DN, Feazel LM, Bessesen MT, Price CS, Janoff EN, Pace NR. 2010. The human nasal microbiota and Staphylococcus aureus carriage. PLoS One 5:e10598. doi:10.1371/journal.pone.0010598.
43. Macintosh RL, Brittan JL, Bhattacharya R, Jenkinson HF, Derrick J, Upton M, Handley PS. 2009. The terminal A domain of the fibrillar accumulation-associated protein (Aap) of Staphylococcus epidermidis mediates adhesion to human corneocytes. J. Bacteriol. 191:7007-7016.
44. Varki A, Schauer R. 2009. Chapter 14, Sialic acids. In Varki A, Cummings RD, Esko JD, Freeze HH, Stanley P, Bertozzi CR, Hart GW, Etzler ME (ed), Essentials of glycobiology,2nded. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY. http://www.ncbi.nlm.nih.gov/books/NBK1920/.
45. Schauer R. 2009. Sialic acids as regulators of molecular and cellular interactions. Curr. Opin. Struct. Biol. 19:507-514.
46. Vimr ER, Troy FA. 1985. Identification of an inducible catabolic system for sialic acids (nan) in Escherichia coli. J. Bacteriol. 164:845-853.
47. Larion M, Moore LB, Thompson SM, Miller BG. 2007. Divergent evolution of function in theROKsugar kinase superfamily: role of enzyme loops in substrate specificity. Biochemistry 46:13564-13572.
48. Jaeger T, Mayer C. 2008. The transcriptional factors MurR and catabolite activator protein regulate N-acetylmuramic acid catabolism in Escherichia coli. J. Bacteriol. 190:6598-6608.
49. Raczynska J, Olchowy J, Konariev PV, Svergun DI, Milewski S, Rypniewski W. 2007. The crystal and solution studies of glucosamine-6- phosphate synthase from Candida albicans. J. Mol. Biol. 372:672-688.
50. Boles BR, Thoendel M, Roth AJ, Horswill AR. 2010. Identification of genes involved in polysaccharide-independent Staphylococcus aureus biofilm formation. PLoS One 5:e10146. doi:10.1371/journal.pone.0010146.
51. Gillaspy AF, Hickmon SG, Skinner RA, Thomas JR, Nelson CL, Smeltzer MS. 1995. Role of the accessory gene regulator (agr) in pathogenesis of staphylococcal osteomyelitis. Infect. Immun. 63:3373-3380.
52. Holden MT, Feil EJ, Lindsay JA, Peacock SJ, Day NP, Enright MC, Foster TJ, Moore CE, Hurst L, Atkin R, Barron A, Bason N, Bentley SD, Chillingworth C, Chillingworth T, Churcher C, Clark L, Corton C, Cronin A, Doggett J, Dowd L, Feltwell T, Hance Z, Harris B, Hauser H, Holroyd S, Jagels K, James KD, Lennard N, Line A, Mayes R, Moule S, Mungall K, Ormond D, Quail MA, Rabbinowitsch E, Rutherford K, Sanders M, Sharp S, Simmonds M, Stevens K, Whitehead S, Barrell BG, Spratt BG, Parkhill J. 2004. Complete genomes of two clinical Staphylococcus aureus strains: evidence for the rapid evolution of virulence and drug resistance. Proc. Natl. Acad. Sci. U. S. A. 101:9786-9791.
53. Baba T, Takeuchi F, Kuroda M, Yuzawa H, Aoki K, Oguchi A, Nagai Y, Iwama N, Asano K, Naimi T, Kuroda H, Cui L, Yamamoto K, Hiramatsu K. 2002. Genome and virulence determinants of high virulence community-acquired MRSA. Lancet 359:1819-1827.
54. Gill SR, Fouts DE, Archer GL, Mongodin EF, Deboy RT, Ravel J, Paulsen IT, Kolonay JF, Brinkac L, Beanan M, Dodson RJ, Daugherty SC, Madupu R, Angiuoli SV, Durkin AS, Haft DH, Vamathevan J, Khouri H, Utterback T, Lee C, Dimitrov G, Jiang L, Qin H, Weidman J, Tran K, Kang K, Hance IR, Nelson KE, Fraser CM. 2005. Insights on evolution of virulence and resistance from the complete genome analysis of an early methicillin-resistant Staphylococcus aureus strain and a biofilmproducing methicillin-resistant Staphylococcus epidermidis strain. J. Bacteriol. 187:2426-2438.
55. Baba T, Bae T, Schneewind O, Takeuchi F, Hiramatsu K. 2008. Genome sequence of Staphylococcus aureus strain Newman and comparative analysis of staphylococcal genomes: polymorphism and evolution of two major pathogenicity islands. J. Bacteriol. 190:300-310.
56. Herbert S, Ziebandt AK, Ohlsen K, Schafer T, Hecker M, Albrecht D, Novick R, Gotz F. 2010. Repair of global regulators in Staphylococcus aureus 8325 and comparative analysis with other clinical isolates. Infect. Immun. 78:2877-2889.
57. Mack D, Siemssen N, Laufs R. 1992. Parallel induction by glucose of adherence and a polysaccharide antigen specific for plastic-adherent Staphylococcus epidermidis: evidence for functional relation to intercellular adhesion. Infect. Immun. 60:2048-2057.
58. Zhang YQ, Ren SX, Li HL, Wang YX, Fu G, Yang J, Qin ZQ, Miao YG, Wang WY, Chen RS, Shen Y, Chen Z, Yuan ZH, Zhao GP, Qu D, Danchin A, Wen YM. 2003. Genome-based analysis of virulence genes in a non-biofilm-forming Staphylococcus epidermidis strain (ATCC 12228). Mol. Microbiol. 49:1577-1593.
59. Seeber S, Kessler C, Gotz F. 1990. Cloning, expression and characterization of the Sau3AI restriction and modification genes in Staphylococcus carnosus TM300. Gene 94:37-43.
60. Heilbronner S, Holden MT, van Tonder A, Geoghegan JA, Foster TJ, Parkhill J, Bentley SD. 2011. Genome sequence of Staphylococcus lugdunensis N920143 allows identification of putative colonization and virulence factors. FEMS Microbiol. Lett. 322:60-67.
61. Lauderdale KJ, Malone CL, Boles BR, Morcuende J, Horswill AR. 2010. Biofilm dispersal of community-associated methicillin-resistant Staphylococcus aureus on orthopedic implant material. J. Orthop. Res. 28:55-61.
62. Wörmann ME, Reichmann NT, Malone CL, Horswill AR, Grundling A. 2011. Proteolytic cleavage inactivates the Staphylococcus aureus lipoteichoic acid synthase. J. Bacteriol. 193:5279-5291.