1887

Abstract

We have identified in , which encodes a bifunctional amylopullulanase with conserved -amylase and pullulanase substrate-binding domains and catalytic motifs. ApuA exhibited properties typical of a Gram-positive surface protein, with a putative signal sequence and LPKTGE cell-wall-anchoring motif. A recombinant protein containing the predicted N-terminal -amylase domain of ApuA was shown to have -(1,4) glycosidic activity. Additionally, an mutant of lacked the pullulanase -(1,6) glycosidic activity detected in a cell-surface protein extract of wild-type . ApuA was required for normal growth in complex medium containing pullulan as the major carbon source, suggesting that this enzyme plays a role in nutrient acquisition via the degradation of glycogen and food-derived starch in the nasopharyngeal and oral cavities. ApuA was shown to promote adhesion to porcine epithelium and mucus , highlighting a link between carbohydrate utilization and the ability of to colonize and infect the host.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.037960-0
2010-09-01
2020-10-26
Loading full text...

Full text loading...

/deliver/fulltext/micro/156/9/2818.html?itemId=/content/journal/micro/10.1099/mic.0.037960-0&mimeType=html&fmt=ahah

References

  1. Arends J. P., Hartwig N., Rudolphy M., Zanen H. C.. 1984; Carrier rate of Streptococcus suis capsular type 2 in palatine tonsils of slaughtered pigs. J Clin Microbiol20:945–947
    [Google Scholar]
  2. Baums C. G., Valentin-Weigand P.. 2009; Surface-associated and secreted factors of Streptococcus suis in epidemiology, pathogenesis and vaccine development. Anim Health Res Rev10:65–83
    [Google Scholar]
  3. Beineke A., Bennecke K., Neis C., Schroder C., Waldmann K. H., Baumgartner W., Valentin-Weigand P., Baums C. G.. 2008; Comparative evaluation of virulence and pathology of Streptococcus suis serotypes 2 and 9 in experimentally infected growers. Vet Microbiol128:423–430
    [Google Scholar]
  4. Benga L., Goethe R., Rohde M., Valentin-Weigand P.. 2004; Non-encapsulated strains reveal novel insights in invasion and survival of Streptococcus suis in epithelial cells. Cell Microbiol6:867–881
    [Google Scholar]
  5. Biswas I., Gruss A., Ehrlich S. D., Maguin E.. 1993; High-efficiency gene inactivation and replacement system for gram-positive bacteria. J Bacteriol175:3628–3635
    [Google Scholar]
  6. Bongaerts R. J., Heinz H. P., Hadding U., Zysk G.. 2000; Antigenicity, expression, and molecular characterization of surface-located pullulanase of Streptococcus pneumoniae. Infect Immun68:7141–7143
    [Google Scholar]
  7. Chen C., Tang J., Dong W., Wang C., Feng Y., Wang J., Zheng F., Pan X., Liu D.. other authors 2007; A glimpse of streptococcal toxic shock syndrome from comparative genomics of S. suis 2 Chinese isolates. PLoS One2:e315
    [Google Scholar]
  8. Cheng Immergluck L., Kanungo S., Schwartz A., McIntyre A., Schreckenberger P. C., Diaz P. S.. 2004; Prevalence of Streptococcus pneumoniae and Staphylococcus aureus nasopharyngeal colonization in healthy children in the United States. Epidemiol Infect132:159–166
    [Google Scholar]
  9. Cloutier G., D'Allaire S., Martinez G., Surprenant C., Lacouture S., Gottschalk M.. 2003; Epidemiology of Streptococcus suis serotype 5 infection in a pig herd with and without clinical disease. Vet Microbiol97:135–151
    [Google Scholar]
  10. Doman-Pytka M., Bardowski J.. 2004; Pullulan degrading enzymes of bacterial origin. Crit Rev Microbiol30:107–121
    [Google Scholar]
  11. Faden H.. 1998; Monthly prevalence of group A, B and G Streptococcus, Haemophilus influenzae types E and F and Pseudomonas aeruginosa nasopharyngeal colonization in the first two years of life. Pediatr Infect Dis J17:255–256
    [Google Scholar]
  12. Ferrari M., Losio M. N., Bernori E., Lingeri R.. 1993; Established thyroid cell line of newborn pig (NPTh. New Microbiol16:381–384
    [Google Scholar]
  13. Ferrari M., Scalvini A., Losio M. N., Corradi A., Soncini M., Bignotti E., Milanesi E., Ajmone-Marsan P., Barlati S.. other authors 2003; Establishment and characterization of two new pig cell lines for use in virological diagnostic laboratories. J Virol Methods107:205–212
    [Google Scholar]
  14. Gottschalk M., Segura M.. 2000; The pathogenesis of the meningitis caused by Streptococcus suis: the unresolved questions. Vet Microbiol76:259–272
    [Google Scholar]
  15. Gottschalk M., Petitbois S., Higgins R., Jacques M.. 1991; Adherence of Streptococcus suis capsular type 2 to porcine lung sections. Can J Vet Res55:302–304
    [Google Scholar]
  16. Gourlay L. J., Santi I., Pezzicoli A., Grandi G., Soriani M., Bolognesi M.. 2009; Group B Streptococcus pullulanase crystal structures in the context of a novel strategy for vaccine development. J Bacteriol191:3544–3552
    [Google Scholar]
  17. Gregoire A. T., Kandil O., Ledger W. J.. 1971; The glycogen content of human vaginal epithelial tissue. Fertil Steril22:64–68
    [Google Scholar]
  18. Hatada Y., Igarashi K., Ozaki K., Ara K., Hitomi J., Kobayashi T., Kawai S., Watabe T., Ito S.. 1996; Amino acid sequence and molecular structure of an alkaline amylopullulanase from Bacillus that hydrolyzes α-1,4 and α-1,6 linkages in polysaccharides at different active sites. J Biol Chem271:24075–24083
    [Google Scholar]
  19. Hava D. L., Camilli A.. 2002; Large-scale identification of serotype 4 Streptococcus pneumoniae virulence factors. Mol Microbiol45:1389–1406
    [Google Scholar]
  20. Hytönen J., Haataja S., Finne J.. 2003; Streptococcus pyogenes glycoprotein-binding strepadhesin activity is mediated by a surface-associated carbohydrate-degrading enzyme, pullulanase. Infect Immun71:784–793
    [Google Scholar]
  21. Hytönen J., Haataja S., Finne J.. 2006; Use of flow cytometry for the adhesion analysis of Streptococcus pyogenes mutant strains to epithelial cells: investigation of the possible role of surface pullulanase and cysteine protease, and the transcriptional regulator Rgg. BMC Microbiol6:18
    [Google Scholar]
  22. Janulczyk R., Rasmussen M.. 2001; Improved pattern for genome-based screening identifies novel cell wall-attached proteins in gram-positive bacteria. Infect Immun69:4019–4026
    [Google Scholar]
  23. Kanno M., Tomimura E.. 1985; Plate culture method for the simultaneous detection of bacteria producing pullulan- and/or starch-hydrolyzing enzymes. Agric Biol Chem49:1529–1530
    [Google Scholar]
  24. Konings R. N., Verhoeven E. J., Peeters B. P.. 1987; pKUN, vectors for the separate production of both DNA strands of recombinant plasmids. Methods Enzymol153:12–34
    [Google Scholar]
  25. Kuriki T., Imanaka T.. 1999; The concept of the alpha-amylase family: structural similarity and common catalytic mechanism. J Biosci Bioeng87:557–565
    [Google Scholar]
  26. Lai C. C., Illias R. M., Hassan H., Kamaruddin K., Aziz S. A., Salleh M. M., Zain W. S. W. M.. 2005; Cloning of pullulanase gene from local isolated bacteria. In Proceedings of 27th Symposium of the Malaysian Society for Microbiology, 24–27 November 2005 Penang, Malaysia. Langkawi: Pulau Pinang;
    [Google Scholar]
  27. Lalonde M., Segura M., Lacouture S., Gottschalk M.. 2000; Interactions between Streptococcus suis serotype 2 and different epithelial cell lines. Microbiology146:1913–1921
    [Google Scholar]
  28. Law B. A.. 1978; Peptide utilization by group N streptococci. J Gen Microbiol105:113–118
    [Google Scholar]
  29. Levitt M. D., Hirsh P., Fetzer C. A., Sheahan M., Levine A. S.. 1987; H2 excretion after ingestion of complex carbohydrates. Gastroenterology92:383–389
    [Google Scholar]
  30. Lun Z. R., Wang Q. P., Chen X. G., Li A. X., Zhu X. Q.. 2007; Streptococcus suis: an emerging zoonotic pathogen. Lancet Infect Dis7:201–209
    [Google Scholar]
  31. Madsen L. W., Svensmark B., Elvestad K., Aalbaek B., Jensen H. E.. 2002; Streptococcus suis serotype 2 infection in pigs: new diagnostic and pathogenetic aspects. J Comp Pathol126:57–65
    [Google Scholar]
  32. Maguin E., Prevost H., Ehrlich S. D., Gruss A.. 1996; Efficient insertional mutagenesis in lactococci and other gram-positive bacteria. J Bacteriol178:931–935
    [Google Scholar]
  33. Mai N. T., Hoa N. T., Nga T. V., Linh le D., Chau T. T., Sinh D. X., Phu N. H., Chuong L. V., Diep T. S.. other authors 2008; Streptococcus suis meningitis in adults in Vietnam. Clin Infect Dis46:659–667
    [Google Scholar]
  34. Melles D. C., Bogaert D., Gorkink R. F., Peeters J. K., Moorhouse M. J., Ott A., van Leeuwen W. B., Simons G., Verbrugh H. A.. other authors 2007; Nasopharyngeal co-colonization with Staphylococcus aureus and Streptococcus pneumoniae in children is bacterial genotype independent. Microbiology153:686–692
    [Google Scholar]
  35. Mora D., Maguin E., Masiero M., Parini C., Ricci G., Manachini P. L., Daffonchio D.. 2004; Characterization of urease genes cluster of Streptococcus thermophilus. J Appl Microbiol96:209–219
    [Google Scholar]
  36. Morgan F. J., Adams K. R., Priest F. G.. 1979; A cultural method for the detection of pullulan-degrading enzymes in bacteria and its application to the genus Bacillus. J Appl Bacteriol46:291–294
    [Google Scholar]
  37. Mormann J. E., Muhlemann H. R.. 1981; Oral starch degradation and its influence on acid production in human dental plaque. Caries Res15:166–175
    [Google Scholar]
  38. Orru G., Marini M. F., Ciusa M. L., Isola D., Cotti M., Baldoni M., Piras V., Pisano E., Montaldo C.. 2006; Usefulness of real time PCR for the differentiation and quantification of 652 and JP2 Actinobacillus actinomycetemcomitans genotypes in dental plaque and saliva. BMC Infect Dis6:98
    [Google Scholar]
  39. Pouliot J. M., Walton I., Nolen-Parkhouse M., Abu-Lail L. I., Camesano T. A.. 2005; Adhesion of Aureobasidium pullulans is controlled by uronic acid based polymers and pullulan. Biomacromolecules6:1122–1131
    [Google Scholar]
  40. Rollenhagen C., Bumann D.. 2006; Salmonella enterica highly expressed genes are disease specific. Infect Immun74:1649–1660
    [Google Scholar]
  41. Ryan P. A., Pancholi V., Fischetti V. A.. 2001; Group A streptococci bind to mucin and human pharyngeal cells through sialic acid-containing receptors. Infect Immun69:7402–7412
    [Google Scholar]
  42. Santi I., Pezzicoli A., Bosello M., Berti F., Mariani M., Telford J. L., Grandi G., Soriani M.. 2008; Functional characterization of a newly identified group B Streptococcus pullulanase eliciting antibodies able to prevent alpha-glucans degradation. PLoS One3:e3787
    [Google Scholar]
  43. Saul D. J., Williams L. C., Grayling R. A., Chamley L. W., Love D. R., Bergquist P. L.. 1990; celB, a gene coding for a bifunctional cellulase from the extreme thermophile “ Caldocellum saccharolyticum”. Appl Environ Microbiol56:3117–3124
    [Google Scholar]
  44. Shelburne S. A. III, Granville C., Tokuyama M., Sitkiewicz I., Patel P., Musser J. M.. 2005; Growth characteristics of and virulence factor production by group A Streptococcus during cultivation in human saliva. Infect Immun73:4723–4731
    [Google Scholar]
  45. Shelburne S. A. III, Sumby P., Sitkiewicz I., Okorafor N., Granville C., Patel P., Voyich J., Hull R., DeLeo F. R., Musser J. M.. 2006; Maltodextrin utilization plays a key role in the ability of group A Streptococcus to colonize the oropharynx. Infect Immun74:4605–4614
    [Google Scholar]
  46. Shelburne S. A. III, Okorafor N., Sitkiewicz I., Sumby P., Keith D., Patel P., Austin C., Graviss E. A., Musser J. M.. 2007; Regulation of polysaccharide utilization contributes to the persistence of group A Streptococcus in the oropharynx. Infect Immun75:2981–2990
    [Google Scholar]
  47. Shelburne S. A. III, Keith D. B., Davenport M. T., Horstmann N., Brennan R. G., Musser J. M.. 2008a; Molecular characterization of group A Streptococcus maltodextrin catabolism and its role in pharyngitis. Mol Microbiol69:436–452
    [Google Scholar]
  48. Shelburne S. A., Davenport M. T., Keith D. B., Musser J. M.. 2008b; The role of complex carbohydrate catabolism in the pathogenesis of invasive streptococci. Trends Microbiol16:318–325
    [Google Scholar]
  49. Smith H. E., Wisselink H. J., Vecht U., Gielkens A. L., Smits M. A.. 1995; High-efficiency transformation and gene inactivation in Streptococcus suis type 2. Microbiology141:181–188
    [Google Scholar]
  50. Sreenivasan P. K., LeBlanc D. J., Lee L. N., Fives-Taylor P.. 1991; Transformation of Actinobacillus actinomycetemcomitans by electroporation, utilizing constructed shuttle plasmids. Infect Immun59:4621–4627
    [Google Scholar]
  51. Tang J., Wang C., Feng Y., Yang W., Song H., Chen Z., Yu H., Pan X., Zhou X.. other authors 2006; Streptococcal toxic shock syndrome caused by Streptococcus suis serotype 2. PLoS Med3:e151
    [Google Scholar]
  52. van Bueren A. L., Higgins M., Wang D., Burke R. D., Boraston A. B.. 2007; Identification and structural basis of binding to host lung glycogen by streptococcal virulence factors. Nat Struct Mol Biol14:76–84
    [Google Scholar]
  53. Vecht U., Arends J. P., van der Molen E. J., van Leengoed L. A.. 1989; Differences in virulence between two strains of Streptococcus suis type II after experimentally induced infection of newborn germ-free pigs. Am J Vet Res50:1037–1043
    [Google Scholar]
  54. Vecht U., Wisselink H. J., van Dijk J. E., Smith H. E.. 1992; Virulence of Streptococcus suis type 2 strains in newborn germfree pigs depends on phenotype. Infect Immun60:550–556
    [Google Scholar]
  55. Virtaneva K., Porcella S. F., Graham M. R., Ireland R. M., Johnson C. A., Ricklefs S. M., Babar I., Parkins L. D., Romero R. A.. other authors 2005; Longitudinal analysis of the group A Streptococcus transcriptome in experimental pharyngitis in cynomolgus macaques. Proc Natl Acad Sci U S A102:9014–9019
    [Google Scholar]
  56. Wertheim H. F., Nghia H. D., Taylor W., Schultsz C.. 2009; Streptococcus suis: an emerging human pathogen. Clin Infect Dis48:617–625
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.037960-0
Loading
/content/journal/micro/10.1099/mic.0.037960-0
Loading

Data & Media loading...

Most cited this month Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error