Skip to main content
SpringerLink
Log in

Biochemical detection of a metallo-β-lactamase in carbapenem resistant strain ofStreptomyces sp. CN229 isolated from soil

  • Ecological and Environmental Microbiology
  • Original Articles
  • Published:
Annals of Microbiology Aims and scope Submit manuscript

Abstract

Streptomyces sp. CN229 was isolated from Tunisia soil. This strain displayed antimicrobial activity against Gram positive and Gram negative bacteria. In addition it is resistant to most β-lactam antibiotics including imipenem and meropenem (MIC imipenem >70 μg/ml). Metallo-β-lactamase (MβL) production was confirmed by either imipenem MIC decrease in the presence of ethylene diamine tetraactic acid (EDTA) or the inhibition zone enhancement around EDTA-impregnated imipenem, or meropenem discs. Isolectric focusing analysis demonstrated the production of β-lactamase with pI of 5.8 that is inhibited by EDTA.Streptomyces sp. CN229 was screened for the imipenem resistance genes,bla VIM andbla IMP previously identified inPseudomonas aeruginosa. The presence of these genes was not confirmed by specific PCR analysis. We concluded that carbapenem resistance inStreptomyces sp. CN229 strain is mainly due to production of a novel carbapenemase. Our data show for the first time that MβL is produced byStreptomyces sp. MβL-mediated imipenem and meropenem resistance inStreptomyces is a cause for concern in the study of resistance evolution and antibiotic cluster biosynthetic genes.

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

  • Arakawa Y., Shibata N., Shibayama K., Hiroshi Kurokawa H., Yagi T., Fujiwara H., Goto M. (2000). Convenient test for screening metallo-β-lactamase-producing Gram-negative bacteria by using thiol compounds. J. Clin. Microbiol., 38: 40–43.

    CAS  PubMed  Google Scholar 

  • Barthelemy M., Guionie M., Labia R. (1978). β-lactamase: determination of their isoelectric points. Antimicrob. Agents Chemother., 13: 695–698.

    CAS  PubMed  Google Scholar 

  • Boudemagh A., Kitouni M., Boughachiche F., Hamdiken H., Oulmi L., Reghioua S., Zerizer M., Couble A., Mouniee D., Boulahrouf A., Boiron P. (2005). Isolation and molecular identification of actinomycete microflora, of some saharian soils of south east Algeria (Biskra, El-oued and Ourgla) study of antifungal activity of isolated strains. J. Mycol. med., 15: 39–44.

    Google Scholar 

  • Bradford M. M. (1976). A rapid and sensitive method for the quantitation of microorganism quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem., 72: 248–257.

    Article  CAS  PubMed  Google Scholar 

  • Bush K. (1989). Classification of β-lactamases: groups 2c, 2d, 2e, 3 and 4. Antimicrob. Agents Chemother., 33: 271–276.

    CAS  PubMed  Google Scholar 

  • Bush K., Mobashery S. (1998). How β-lactamases have driven pharmaceutical drug discovery. From mechanistic knowledge to clinical circumvention. Adv. Exp. Med. Biol., 456: 71–98.

    CAS  PubMed  Google Scholar 

  • Castaheira M., Toleman M., Jones R., Schmidt F., Walsh T. (2004). Molecular characterization of a β-lactamase gene,bla GIM-1, encoding a new subclass of metallo-β-lactamase. Antimicrob. Agents Chemother., 48: 4654–4661.

    Article  Google Scholar 

  • Chu Y., Afzal-Shah M., Houang E., Palepou M., Lyon D., Woodford N., Livermore D. (2001). IMP-4, a novel metallo-β-lactamase from nosocomialAcinetobacter spp. collected in Hong Kong between 1994 and 1998. Antimicrob. Agents Chemother., 45: 710–714.

    Article  CAS  PubMed  Google Scholar 

  • D’Costa V.M., McGrann K.M., Hughes D.W., Wright G.D. (2006). Sampling the antibiotic resistome. Science, 311: 374–377.

    Article  PubMed  Google Scholar 

  • Doly A., Verdet C., Gautier V., Decre D., Ronco E., Hammami A., Philippon A., Arlet G. (2006). Genetic environment of acquiredbla ACC-1 β-lactamase gene inEnterobacteriaceae isolates. Antimicrob. Agents Chemother., 50: 4177–4181.

    Article  Google Scholar 

  • Furushita M., Okamoto A., Maeda T., Ohta M., Shiba T. (2005). Isolation of multidrug-resistantStenotrophomonas maltophilia from cultured yellowtail (Seriola quinqueradiata) from a marine fish farm. Appl. Environ. Microbiol., 71: 5598–5600.

    Article  CAS  PubMed  Google Scholar 

  • Gong-Xiang C., Rong Z., Hong-Wei Z. (2006). Heterogeneity of metallo-β-lactamases in clinical isolates ofChryseobacterium meningosepticum from Hangzhou, China. J. Antimicrob. Chemother., 27: 750–752.

    Google Scholar 

  • Hemalatha V., Sekar U., Kamat V. (2005). Detection of metall-β-lactamase producingPseudomonas aeruginosa in hospitalized patients. Indian J. Med. Res., 122: 148–152.

    CAS  PubMed  Google Scholar 

  • Henriques I., Moura A., Alves A., Saavedra M. (2004). Molecular characterization of a carbapenem-hydrolyzing class A β-lactamase, SFC-1, fromSerratia fonticola UTAD54. Antimicrob. Agents Chemother., 48: 2321–2324.

    Article  CAS  PubMed  Google Scholar 

  • Hopwood D. (2007). How do antibiotic-producing bacteria ensure their self-resistance before antibiotic biosynthesis incapacitates them? Mol. Microb., 63: 937–940.

    Article  CAS  Google Scholar 

  • Kieser T., Bibb M., Buttner M., Chater K., Hopwood D. (2000). PracticalStreptomyces Genetics. The John Innes Foundation, Norwich, United Kingdom.

    Google Scholar 

  • Kim I., Ki C., Kim S., Oh W., Peck K., Song J., Lee K., Lee N. (2007). Diversity of ampicillin resistance genes and antimicrobial susceptibility patterns inHaemophilus influenzae strains isolated in Korea. Antimicrob. Agents Chemother., 51: 453–460.

    Article  CAS  PubMed  Google Scholar 

  • Kitouni M., Boudemagh A., Oulmi L., Reghioua S., Boughachiche F., Zerizer H., Hamdiken H., Couble A., Mouniee D., Boulahrouf A., Boiron P. (2005). Isolation of actinomycetes producing bioactive substances from water, soil and tree bark samples of the north-east of Algeria. J. Med. Mycol., 15: 45–51.

    Google Scholar 

  • Lee K., Lim J., Yum J., Yong D., Chong Y., Kim J., Livermore D. (2002).bla VIM-2 cassette-containing novel integrons in metallo-β-lactamase producingPseudomonas aeruginosa spp. andPseudomonas putida isolates disseminated in a Korean hospital. Antimicrob. Agents Chemother., 46: 1053–1058.

    Article  CAS  PubMed  Google Scholar 

  • Lee K., Lim Y., Yong D., Yum J., Chong Y. (2003). Evaluation of the Hodge test and the imipenem-EDTA double-disk synergy test for differentiating metallo-β-lactamase producing isolates ofPseudomonas spp. andAcinetobacter spp. J. Clin. Microbiol., 41: 4623–4629.

    Article  CAS  PubMed  Google Scholar 

  • Locci R., Ed. (1989). Streptomycetes and Related Genera. In: Bergey’s Manual of Systematic Bacteriology, Vol. 4, Williams and Wilkins, Baltimore, USA

    Google Scholar 

  • Manchanda V., Singh N. (2003). Occurrence and detection of AmpC β-lactamase among Gram-negative clinical isolates using a modified three-dimensional test at Guru Tegh Bahadur hospital, Delhi, India. J. Antimicrob. Chemother., 51: 415–418.

    Article  CAS  PubMed  Google Scholar 

  • Massov I., Mobashry S. (1998). Kinship and diversification of bacterial pencillin-binding protein and β-lactamases. Antimicrob. Agents Chmother., 42: 1–17.

    Google Scholar 

  • Migliavacca R., Docquier J., Mugnaioli C., Amicosante G., Daturi R., Lee K., Rossolini G., Pagani L. (2002). Simple microdilution test for detection of metallo-β-lactamase production inPseudomonas aeruginosa. J. Clin. Microbiol., 40: 4388–4390.

    Article  CAS  PubMed  Google Scholar 

  • NCCLS—National Committee for Clinical Laboratory Standards (2003) Performance standards for antimicrobial disk susceptibility testing. Approved standard. NCCLS Document M24-A. National Committee for Clinical Laboratory Standards, Wayne, Pa.

    Google Scholar 

  • Nomura Y., Ishino Y., Kimizuka F., Kato I. (1995). A novelStreptomyces restriction endonuclease,Sse18251, cleaving at 5′-GG/GWCCC-3′. Gene, 157: 323–324.

    Article  CAS  PubMed  Google Scholar 

  • Nordmann P., Poirel L. (2002). Emerging carbapenemases in Gram negative aerobes. Clin. Microbiol. Infect., 8: 321–331.

    Article  CAS  PubMed  Google Scholar 

  • Poirel L., Nass T., Guibert M., Chaibi E., Labia R., Nordmann P. (1999). Molecular and biochemical characterization of VEB-1, a novel class a extended-spectrum β-lactamase encoded by anEscherichia coli integron gene. Antimicrob. Agents Chemother., 43: 573–581.

    CAS  PubMed  Google Scholar 

  • Poirel L., Nass T., Nicolas D., Collet L., Bellais S., Cavallo J., Nordman P. (2000). Characterization of VIM-2, a carbapenem-hydrolyzing metallo-β-lactamace and its plasmid and integron-born gene from aPseudomonas aeruginosa clinical isolate in France. Antimicrob. Agents Chemother., 44: 891–897.

    Article  CAS  PubMed  Google Scholar 

  • Poirel L., Lambert T., Türkoglü S., Ronco E., Gaillard J., Nordmann P. (2001). Characterization of class I integrons fromPseudomonas aeruginosa that contain thebla VIM-2 carbapenem-hydrolyzing β-lactamase gene and of two novel aminoglycoside resistance gene cassettes. Antimicrob. Agents Chemother., 45: 546–552.

    Article  CAS  PubMed  Google Scholar 

  • Poirel L., Leviandier C., Nordmann P. (2006). Prevalence and genetic analysis of plasmid-mediated quinolone resistance determinants QnrA and QnrS inEnterobacteriaceae isolates from a French university hospital. Antimicrob. Agents Chemother., 50: 3992–3997.

    Article  CAS  PubMed  Google Scholar 

  • Poirel L., Cattoir V., Soares A., Soussy C., Nordmann P. (2007). Novel ambler class A β-lactamase LAP-1 and its association with the plasmid-mediated quinolone resistance determinant QnrS1. Antimicrob. Agents Chemother., 51: 631–637.

    Article  CAS  PubMed  Google Scholar 

  • Rintala H., Nevalainen A., Ronka E., Suutari M. (2001). PCR primers targeting the 16S rRNA gene for the specific detection of streptomycetes. Mol. Cell. Probes, 15: 337–347.

    Article  CAS  PubMed  Google Scholar 

  • Rossolini G., Condemi M., Pantanella F., Docquier J., Amicosante G., Thaller M. (2001). Metallo-β-lactamase producers in environmental microbiota: new molecular class B enzyme inJanthinobacterium lividum. Antimicrob. Agents Chemother., 45, 837–844.

    Article  CAS  PubMed  Google Scholar 

  • Shah D., Narang M. (2005). Meropenem. Indian Pediatrics, 42: 443–445.

    PubMed  Google Scholar 

  • Toleman M., Simm A., Murphy T., Gales A., Biedenbach D., Jones R., Walsh T. (2002). Molecular characterization of SPM-1, a novel metallo-β-lacatamase isolated in Latin America: report from the SENTRY antimicrobial surveillance programme. J. Antimicrob. Chemother., 50: 673–679.

    Article  CAS  PubMed  Google Scholar 

  • Toleman M., Biedenbach D., Bennett D., Jones R., Walsh T. (2005). Italian metallo-β-lactamases: a national problem? Report from the SENTRY antimicrobial surveillance programme. J. Antimicrob. Chemother. 55: 61–70.

    Article  CAS  PubMed  Google Scholar 

  • Vera M., Ana K., Marcelo M. (2005). Metallo-β-lactamase producingPseudomonas aeruginosa strains isolated in hospitals in Recife, Brazil. Braz. J. Microbiol., 36: 123–125.

    Google Scholar 

  • Yan J., Hsueh P., Ko W., Luh K., Tsai S., Wu H., Wu J. (2001). Metallo-β-lacatamase in clinicalPseudomonas isolates in Taiwan and identification of VIM-3, a novel variant of the VIM-2 enzyme. Antimicrob. Agents Chemother., 45: 2224–2228.

    Article  CAS  PubMed  Google Scholar 

  • Yong D., Lee K., Yum J., Shin H., Rossolini G., Chong Y. (2002). Imipenem-EDTA disk method for differentiation of metallo-β-lactamase producing clinical isolates ofPseudomonas spp. andAcinetobacter spp. J. Clin. Microbiol. 40: 3798–3801.

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Unité de Microbiologie et Biologie Moléculaire, Centre Nationale des Sciences et Technologies Nucléaires, Technopole de Sidi Thabet, 2020, Tunis, Tunisia

    Hadeer Lazim, Nedra Slama & Insaf Barkallah

  2. Laboratoire de microbiologie, Centre national de Greffe de Moelle osseuse, Bab Saadoun, Tunis, Tunisia

    Abbassi Mohamed Salah & Assia Ben Hassen

  3. Laboratoire des Interactions Légumineuses Microorganismes, Centre de Biotechnologie, Technopole de Borj Cedria, 910-2050, Hammam-Lif, Tunisia

    Ferid Limam

Authors
  1. Hadeer Lazim
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Abbassi Mohamed Salah
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Nedra Slama
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Insaf Barkallah
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Assia Ben Hassen
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Ferid Limam
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Hadeer Lazim.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Lazim, H., Salah, A.M., Slama, N. et al. Biochemical detection of a metallo-β-lactamase in carbapenem resistant strain ofStreptomyces sp. CN229 isolated from soil. Ann. Microbiol. 57, 515–519 (2007). https://doi.org/10.1007/BF03175348

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF03175348

Key words

Search

Navigation