Skip to main content

Advertisement

SpringerLink
Log in

Association of tannase-producing Staphylococcus lugdunensis with colon cancer and characterization of a novel tannase gene

  • Alimentary Tract
  • Published:
Journal of Gastroenterology Aims and scope Submit manuscript

Abstract

Background

The relationship between Streptococcus (St.) bovis endocarditis and colon cancer is well known. In St. bovis, the biotype I strain (formerly, St. gallolyticus) produces tannase that degrades tannins. The aim of this study was to investigate the association of tannase-producing bacteria with colon cancer, and to identify the major tannase-producing bacteria and the gene involved.

Methods

Tannase-producing bacteria were isolated in tannic acid-treated selective agar medium from feces and rectal swabs of 357 patients who underwent colon endoscopy from 1999 to 2004.

Results

Tannase-producing bacteria were isolated more frequently from the colon cancer group (24.3%) than from the adenoma or normal groups (14.4%; P < 0.05). S. gallolyticus, Staphylococcus (S.) lugdunensis, Lactobacillus (L.) plantarum, and L. pentosus were all identified as tannase-producing bacteria. Of these, S. lugdunensis was significantly isolated from the advanced-stage cancer group (22.2%; P < 0.001) more than from the early-stage cancer (8.6%) or adenoma (4.9%) groups. The gene (tanA) for tannase in S. lugdunensis was cloned and sequenced. The tanA gene was associated with all S. lugdunensis but not with other bacteria by Southern blotting and polymerase chain reaction.

Conclusions

Tannase-producing S. lugdunensis is associated with advanced-stage colon cancer, and the tanA gene is a useful marker for the detection of S. lugdunensis.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. JL Beebe EW Koneman (1995) ArticleTitleRecovery of uncommon bacteria from blood: association with neoplastic disease Clin Microbiol Rev 8 336–56 Occurrence Handle7553569 Occurrence Handle1:STN:280:DyaK28%2FgvFaisA%3D%3D

    PubMed  CAS  Google Scholar 

  2. S Ellmerich M Scholler B Duranton F Gosse M Galluser JP Klein et al. (2000) ArticleTitlePromotion of intestinal carcinogenesis by Streptococcus bovis Carcinogenesis 21 753–6 Occurrence Handle10753212 Occurrence Handle10.1093/carcin/21.4.753 Occurrence Handle1:CAS:528:DC%2BD3cXivFKkur0%3D

    Article  PubMed  CAS  Google Scholar 

  3. IA Herrero MS Rouse KE Piper SA Alyaseen JM Steckelberg R Patel (2002) ArticleTitleReevaluation of Streptococcus bovis endocarditis cases from 1975 to 1985 by 16S ribosomal DNA sequence analysis J Clin Microbiol 40 3848–50 Occurrence Handle12354897 Occurrence Handle10.1128/JCM.40.10.3848-3850.2002 Occurrence Handle1:CAS:528:DC%2BD38Xot1Gnurk%3D

    Article  PubMed  CAS  Google Scholar 

  4. RS Klein RA Recco MT Catalano SC Edberg JI Casey NH Steigbigel (1977) ArticleTitleAssociation of Streptococcus bovis with carcinoma of the colon N Engl J Med 297 800–2 Occurrence Handle408687 Occurrence Handle1:STN:280:DyaE2s3lsV2muw%3D%3D Occurrence Handle10.1056/NEJM197710132971503

    Article  PubMed  CAS  Google Scholar 

  5. JE Clarridge Suffix3rd SM Attorri Q Zhang J Bartell (2001) ArticleTitle16S ribosomal DNA sequence analysis distinguishes biotypes of Streptococcus bovis: Streptococcus bovis Biotype II/2 is a separate genospecies and the predominant clinical isolate in adult males J Clin Microbiol 39 1549–52 Occurrence Handle11283085 Occurrence Handle10.1128/JCM.39.4.1549-1552.2001

    Article  PubMed  Google Scholar 

  6. R Facklam (2002) ArticleTitleWhat happened to the streptococci? Overview of taxonomic and nomenclature changes Clin Microbiol Rev 15 613–30 Occurrence Handle12364372 Occurrence Handle10.1128/CMR.15.4.613-630.2002

    Article  PubMed  Google Scholar 

  7. L Schlegel F Grimont E Ageron PA Grimont A Bouvet (2003) ArticleTitleReappraisal of the taxonomy of the Streptococcus bovis/Streptococcus equinus complex and related species: description of Streptococcus gallolyticus subsp. gallolyticus subsp. nov., S. gallolyticus subsp. macedonicus subsp. nov. and S. gallolyticus subsp. pasteurianus subsp. nov Int J Syst Evol Microbiol 53 631–45 Occurrence Handle12807180 Occurrence Handle10.1099/ijs.0.02361-0 Occurrence Handle1:CAS:528:DC%2BD3sXkvFOjur4%3D

    Article  PubMed  CAS  Google Scholar 

  8. LI Sly MM Cahill R Osawa T Fujisawa (1997) ArticleTitleThe tannin-degrading species Streptococcus gallolyticus and Streptococcus caprinus are subjective synonyms Int J Syst Bacteriol 47 893–4 Occurrence Handle9226925 Occurrence Handle1:STN:280:DyaK2szntVKiuw%3D%3D

    PubMed  CAS  Google Scholar 

  9. R Osawa (1990) ArticleTitleFormation of a clear zone on tannin-treated brain heart infusion agar by a Streptococcus sp. isolated from feces of koalas Appl Environ Microbiol 56 829–31 Occurrence Handle2180375 Occurrence Handle1:STN:280:DyaK3c7pslajsg%3D%3D

    PubMed  CAS  Google Scholar 

  10. R Osawa T Fujisawa LI Sly (1995) ArticleTitleStreptococcus gallolyticus sp. nov.; gallate degrading organisms formerly assigned to Streptococcus bovis Syst Appl Microbiol 18 74–8

    Google Scholar 

  11. K Hirota R Osawa K Nemoto T Ono Y Miyake (1996) ArticleTitleHighly expressed human sialyl Lewis antigen on cell surface of Streptococcus gallolyticus Lancet 347 760 Occurrence Handle8602016 Occurrence Handle10.1016/S0140-6736(96)90109-9 Occurrence Handle1:STN:280:DyaK287otFWntg%3D%3D

    Article  PubMed  CAS  Google Scholar 

  12. R Osawa (1996) Tannin degrading bacteria Streptococcus gallolyticus isolated from Koala's feces. Presented at Riken Symposium Classification and ecology of lactic acid bacteria 1996 Riken Saitama 36–45

    Google Scholar 

  13. A Scalbert (1991) ArticleTitleAntimicrobial properties of tannins Phytochemistry 30 3875–83 Occurrence Handle10.1016/0031-9422(91)83426-L Occurrence Handle1:CAS:528:DyaK38XnvF2ksg%3D%3D

    Article  CAS  Google Scholar 

  14. P Vohra FH Kratzer MA Joslyn (1966) ArticleTitleThe growth depressing and toxic effects of tannins to chicks Poult Sci 45 135–42 Occurrence Handle5905856 Occurrence Handle1:CAS:528:DyaF28XmtFOrtg%3D%3D

    PubMed  CAS  Google Scholar 

  15. TK Bhat B Singh OP Sharma (1998) ArticleTitleMicrobial degradation of tannins—a current perspective Biodegradation 9 343–57 Occurrence Handle10192896 Occurrence Handle10.1023/A:1008397506963 Occurrence Handle1:CAS:528:DyaK1MXisVKhsbk%3D

    Article  PubMed  CAS  Google Scholar 

  16. S Iibuchi Y Minoda K Yamada (1968) ArticleTitleStudies on tannin acryl hydrolase of microorganisms, part III. Purification of the enzyme and some properties of it Agric Biol Chem 32 803–9 Occurrence Handle1:CAS:528:DyaF1cXkslCjtLs%3D

    CAS  Google Scholar 

  17. C Barthomeuf F Regerat H Pourrat (1994) ArticleTitleProduction, purification and characterization of a tannase from Aspergillus niger LCF8 J Ferment Bioeng 77 320–3 Occurrence Handle10.1016/0922-338X(94)90242-9 Occurrence Handle1:CAS:528:DyaK2cXksFarsr4%3D

    Article  CAS  Google Scholar 

  18. R Osawa (1992) ArticleTitleTannin–protein complex-degrading enterobacteria isolated from the alimentary tracts of koalas and a selective medium for their enumeration Appl Environ Microbiol 58 1754–9 Occurrence Handle1622248 Occurrence Handle1:CAS:528:DyaK38XktVCjsrY%3D

    PubMed  CAS  Google Scholar 

  19. R Osawa K Kuroiso S Goto A Shimizu (2000) ArticleTitleIsolation of tannin-degrading lactobacilli from humans and fermented foods Appl Environ Microbiol 66 3093–7 Occurrence Handle10877812 Occurrence Handle10.1128/AEM.66.7.3093-3097.2000 Occurrence Handle1:CAS:528:DC%2BD3cXkslKltLs%3D

    Article  PubMed  CAS  Google Scholar 

  20. M Dorsch E Stackebrandt (1992) ArticleTitleSome modification in the procedure of direct sequence of PCR amplified 16S rDNA J Microbiol Methods 16 271–9 Occurrence Handle10.1016/0167-7012(92)90017-X

    Article  Google Scholar 

  21. BL Maidak JR Cole CT Parker SuffixJr GM Garrity N Larsen B Li et al. (1999) ArticleTitleA new version of the RDP (Ribosomal Database Project) Nucleic Acids Res 27 171–3 Occurrence Handle9847171 Occurrence Handle10.1093/nar/27.1.171 Occurrence Handle1:CAS:528:DyaK1MXpsVKjsw%3D%3D

    Article  PubMed  CAS  Google Scholar 

  22. J Freney Y Brun M Bes H Meugnier F Grimont PAD Grimont et al. (1988) ArticleTitleStaphylococcus lugdunensis sp. nov. and Staphylococcus schleiferi sp. nov., two species from human clinical specimens Int J Syst Bacteriol 38 168–72 Occurrence Handle10.1099/00207713-38-2-168

    Article  Google Scholar 

  23. N Noguchi K Takada J Katayama A Emura M Sasatsu (2000) ArticleTitleRegulation of transcription of the mph(A) gene for macrolide 2′-phosphotransferase I in Escherichia coli: characterization of the regulatory gene mphR(A) J Bacteriol 182 5052–8 Occurrence Handle10960087 Occurrence Handle10.1128/JB.182.18.5052-5058.2000 Occurrence Handle1:CAS:528:DC%2BD3cXmsVOqtb0%3D

    Article  PubMed  CAS  Google Scholar 

  24. T Ezaki Y Hashimoto N Takeuchi H Yamamoto SL Liu H Miura et al. (1988) ArticleTitleSimple genetic method to identify viridans group streptococci by colorimetric dot hybridization and fluorometric hybridization in microdilution wells J Clin Microbiol 26 1708–13 Occurrence Handle3183018 Occurrence Handle1:STN:280:DyaL1M%2FjsVOlsw%3D%3D

    PubMed  CAS  Google Scholar 

  25. K Shishido N Noguchi C Kim T Ando (1983) ArticleTitleIsolation of a tetracycline-resistance plasmid excised from a chromosomal DNA sequence in Bacillus subtilis Plasmid 10 224–34 Occurrence Handle6318246 Occurrence Handle10.1016/0147-619X(83)90036-7 Occurrence Handle1:CAS:528:DyaL2cXhvVGgtw%3D%3D

    Article  PubMed  CAS  Google Scholar 

  26. N Noguchi J Suwa K Narui M Sasatsu T Ito K Hiramatsu et al. (2005) ArticleTitleSusceptibilities to antiseptic agents and distribution of antiseptic-resistance genes qacA/B and smr of methicillin-resistant Staphylococcus aureus isolated in Asia during 1998 and 1999 J Med Microbiol 54 557–65 Occurrence Handle15888465 Occurrence Handle10.1099/jmm.0.45902-0 Occurrence Handle1:CAS:528:DC%2BD2MXlvVGisrw%3D

    Article  PubMed  CAS  Google Scholar 

  27. P Glaser L Frangeul C Buchrieser C Rusniok A Amend F Baquero et al. (2001) ArticleTitleComparative genomics of Listeria species Science 294 849–52 Occurrence Handle11679669 Occurrence Handle1:CAS:528:DC%2BD3MXotVChtL0%3D

    PubMed  CAS  Google Scholar 

  28. SR Gill DE Fouts GL Archer EF Mongodin RT Deboy J Ravel et al. (2005) ArticleTitleInsights on evolution of virulence and resistance from the complete genome analysis of an early methicillin-resistant Staphylococcus aureus strain and a biofilm-producing methicillin-resistant Staphylococcus epidermidis strain J Bacteriol 187 2426–38 Occurrence Handle15774886 Occurrence Handle10.1128/JB.187.7.2426-2438.2005 Occurrence Handle1:CAS:528:DC%2BD2MXjt1Kqs7s%3D

    Article  PubMed  CAS  Google Scholar 

  29. RP de Vries PA vanKuyk HC Kester J Visser (2002) ArticleTitleThe Aspergillus niger faeB gene encodes a second feruloyl esterase involved in pectin and xylan degradation and is specifically induced in the presence of aromatic compounds Biochem J 363 377–86 Occurrence Handle11931668 Occurrence Handle10.1042/0264-6021:3630377 Occurrence Handle1:CAS:528:DC%2BD38XjsFWmtL0%3D

    Article  PubMed  CAS  Google Scholar 

  30. O Hatamoto T Watarai M Kikuchi K Mizusawa H Sekine (1996) ArticleTitleCloning and sequencing of the gene encoding tannase and a structural study of the tannase subunit from Aspergillus oryzae Gene 175 215–21 Occurrence Handle8917102 Occurrence Handle10.1016/0378-1119(96)00153-9 Occurrence Handle1:CAS:528:DyaK28XmtlehtLg%3D

    Article  PubMed  CAS  Google Scholar 

  31. LA Devriese P Vandamme B Pot M Vanrobaeys K Kersters F Haesebrouck (1998) ArticleTitleDifferentiation between Streptococcus gallolyticus strains of human clinical and veterinary origins and Streptococcus bovis strains from the intestinal tracts of ruminants J Clin Microbiol 36 3520–3 Occurrence Handle9817865 Occurrence Handle1:STN:280:DyaK1M%2Fjs1Omsw%3D%3D

    PubMed  CAS  Google Scholar 

  32. R Bellamy T Barkham (2002) ArticleTitleStaphylococcus lugdunensis infection sites: predominance of abscesses in the pelvic girdle region Clin Infect Dis 35 E32–4 Occurrence Handle12115114 Occurrence Handle10.1086/341304

    Article  PubMed  Google Scholar 

  33. JM Greig MJ Wood (2003) ArticleTitleStaphylococcus lugdunensis vertebral osteomyelitis Clin Microbiol Infect 9 1139–41 Occurrence Handle14616734 Occurrence Handle10.1046/j.1469-0691.2003.00777.x Occurrence Handle1:STN:280:DC%2BD3srjslSrsQ%3D%3D

    Article  PubMed  CAS  Google Scholar 

  34. R Patel KE Piper MS Rouse JR Uhl FR Cockerill Suffix3rd JM Steckelberg (2000) ArticleTitleFrequency of isolation of Staphylococcus lugdunensis among staphylococcal isolates causing endocarditis: a 20-year experience J Clin Microbiol 38 4262–3 Occurrence Handle11060105 Occurrence Handle1:STN:280:DC%2BD3M%2FovFygsA%3D%3D

    PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Microbiology, School of Pharmacy, Tokyo University of Pharmacy and Life Science, 1432-1 Horinouchi, Hachioji, Tokyo, 192-0392, Japan

    Norihisa Noguchi, Takashi Ohashi, Koji Narui & Masanori Sasatsu

  2. Department of Gastroenterology, Hachioji Medical Center of Tokyo Medical University, Tokyo, Japan

    Taisei Shiratori

  3. Department of Gastroenterology, Tokyo Medical University, Tokyo, Japan

    Tadashi Hagiwara, Mari Ko, Takeo Miyahara, Satoru Taira & Fuminori Moriyasu

  4. Hachioji Pharmaceutical Center, Tokyo, Japan

    Kiyoshi Watanabe

Authors
  1. Norihisa Noguchi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Takashi Ohashi
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Taisei Shiratori
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Koji Narui
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Tadashi Hagiwara
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Mari Ko
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Kiyoshi Watanabe
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Takeo Miyahara
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Satoru Taira
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Fuminori Moriyasu
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Masanori Sasatsu
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Noguchi, N., Ohashi, T., Shiratori, T. et al. Association of tannase-producing Staphylococcus lugdunensis with colon cancer and characterization of a novel tannase gene. J Gastroenterol 42, 346–351 (2007). https://doi.org/10.1007/s00535-007-2012-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00535-007-2012-5

Key words

Search

Navigation