Skip to main content

Advertisement

Log in

Characterization of Antibiotic-Resistant Stenotrophomonas Isolates from Painted Turtles Living in the Wild

  • Short Communication
  • Published:
Current Microbiology Aims and scope Submit manuscript

Abstract

Stenotrophomonas maltophilia is a ubiquitous multidrug-resistant opportunistic pathogen commonly associated with nosocomial infections. The purpose of this study was to isolate and characterize extended-spectrum beta-lactamase (ESBL) producing bacteria from painted turtles (Chrysemys picta) living in the wild and captured in southeastern Wisconsin. Fecal samples from ten turtles were examined for ESBL producing bacteria after incubation on HardyCHROM™ ESBL agar. Two isolates were cultivated and identified by 16S rRNA gene sequencing and whole genome sequencing (WGS) as Stenotrophomonas sp. 9A and S. maltophilia 15A. They were multidrug-resistant, as determined by antibiotic susceptibility testing. Stenotrophomonas sp. 9A was found to produce an extended spectrum beta-lactamase (ESBL) and both isolates were found to be carbapenem-resistant. EDTA-modified carbapenem inactivation method (eCIM) and the modified carbapenem inactivation method (mCIM) tests were used to examine the carbapenemase production and the test results were negative. Through WGS several antimicrobial resistance genes were identified in S. maltophilia 15A. For example a chromosomal L1 β-lactamase gene, which is known to hydrolyze carbapenems, a L2 β-lactamase gene, genes for the efflux systems smeABC and smeDEF and the aminoglycosides resistance genes aac(6′)-lz and aph(3′)-llc were found. An L2 β-lactamase gene in Stenotrophomonas sp. 9A was identified through WGS.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1

Data Availability

The 16S rRNA gene sequences have been deposited in the GenBank nucleotide database under the accession numbers ON624157 and ON624158. This Whole Genome Shotgun project has been deposited at DDBJ/ENA/GenBank under the accessions JAMOKY000000000 and JAMOKZ000000000.

Code Availability

Not applicable.

References

  1. Brooke JS (2021) Advances in the microbiology of Stenotrophomonas maltophilia. Clin Microbiol Rev 34:e0003019

    Article  PubMed  Google Scholar 

  2. Brooke JS (2012) Stenotrophomonas maltophilia: an emerging global opportunistic pathogen. Clin Microbiol Rev 25:2–41

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Batra P, Mathur P, Misra MC (2017) Clinical characteristics and prognostic factors of patients with Stenotrophomonas maltophilia infections. J Lab Physicians 9:132–135

    Article  PubMed  PubMed Central  Google Scholar 

  4. Bao H, Qiao Y, Liu D, Chen J, Wu X, Hu X, Ma X, Wu D (2020) The clinical impact of Stenotrophomonas maltophilia bacteremia on the 30-day mortality rate in patients with hematologic disorders: a single-institution experience. Infection 48:205–212

    Article  CAS  PubMed  Google Scholar 

  5. Hogg HDJ, Siah WF, Okonkwo A, Narayanan M, Figueiredo FC (2019) Stenotrophomonas maltophilia—a case series of a rare keratitis affecting patients with bandage contact. Eye Contact Lens 45:e1–e4

    Article  PubMed  Google Scholar 

  6. Kucukates E, Gultekin N, Bagdatli Y (2013) Cases of active infective endocarditis in a university hospital during a 10-year period. J Pak Med Assoc 63:1163–1167

    PubMed  Google Scholar 

  7. Kaito S, Sekiya N, Najima Y, Sano N, Horiguchi S, Kakihana K, Hishima T, Ohashi K (2018) Fatal neutropenic enterocolitis caused by Stenotrophomonas maltophilia: a rare and underrecognized entity. Intern Med 57:3667–3671

    Article  PubMed  PubMed Central  Google Scholar 

  8. Samonis G, Karageorgopoulos DE, Maraki S, Levis P, Dimopoulou D, Spernovasilis NA, Kofteridis DP, Falagas ME (2012) Stenotrophomonas maltophilia infections in a general hospital: patient characteristics, antimicrobial susceptibility, and treatment outcome. PLoS ONE 7:e37375

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Ernst CH, Lovich JE (2009) Turtles of the United States and Canada, 2nd edn. Johns Hopkins University Press, Baltimore, p 840

    Book  Google Scholar 

  10. Fugate HM, Kapfer JM, McLaughlin RW (2020) Analysis of the microbiota in the fecal material of Painted Turtles (Chrysemys picta). Curr Microbiol 77:11–14

    Article  CAS  PubMed  Google Scholar 

  11. Mitchell JC, McAvoy BV (1990) Enteric bacteria in natural populations of freshwater turtles in Virginia. Virginia J Science 41:233–242

    Google Scholar 

  12. Youenou B, Favre-Bonté S, Bodilis J, Brothier E, Dubost A, Muller D, Nazaret S (2015) Comparative genomics of environmental and clinical Stenotrophomonas maltophilia strains with different antibiotic resistance profiles. Genome Biol Evol 7:2484–2505

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M, Kulikov AS, Lesin VM, Nikolenko SI, Pham S, Prjibelski AD, Pyshkin AV, Sirotkin AV, Vyahhi N, Tesler G (2012) SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 19:455–477

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Brettin T, Davis JJ, Disz T, Edwards RA, Gerdes S, Olsen GJ, Olson R, Overbeek R, Parrello B, Pusch GD, Shukla M, Thomason JA 3rd, Stevens R, Vonstein V, Wattam AR, Xia F (2015) RASTtk: a modular and extensible implementation of the RAST algorithm for building custom annotation pipelines and annotating batches of genomes. Sci Rep 5:8365

    Article  PubMed  PubMed Central  Google Scholar 

  15. Rodriguez RLM, Konstantinidis KT (2016) The enveomics collection: a toolbox for specialized analyses of microbial genomes and metagenomes. Peer J Preprints 4:e1900v1

    Google Scholar 

  16. Davis JJ, Wattam AR, Aziz RK, Brettin T, Butler R, Butler RM, Chlenski P, Conrad N, Dickerman A, Dietrich EM, Gabbard JL, Gerdes S, Guard A, Kenyon RW, Machi D, Mao C, Murphy-Olson D, Nguyen M, Nordberg EK, Olsen GJ, Olson RD, Overbeek JC, Overbeek R, Parrello B, Pusch GD, Shukla M, Thomas C, VanOeffelen M, Vonstein V, Warren AS, Xia F, Xie D, Yoo H, Stevens R (2020) The PATRIC bioinformatics resource center: expanding data and analysis capabilities. Nucleic Acids Res 48:D606–D612

    CAS  PubMed  Google Scholar 

  17. Schmartz GP, Hartung A, Hirsch P, Kern F, Fehlmann T, Müller R, Keller A (2022) PLSDB: advancing a comprehensive database of bacterial plasmids. Nucleic Acids Res 50:D273–D278

    Article  CAS  PubMed  Google Scholar 

  18. Antonopoulos DA, Assaf R, Aziz RK, Brettin T, Bun C, Conrad N, Davis JJ, Dietrich EM, Disz T, Gerdes S, Kenyon RW, Machi D, Mao C, Murphy-Olson DE, Nordberg EK, Olsen GJ, Olson R, Overbeek R, Parrello B, Pusch GD, Santerre J, Shukla M, Stevens RL, VanOeffelen M, Vonstein V, Warren AS, Wattam AR, Xia F, Yoo H (2019) PATRIC as a unique resource for studying antimicrobial resistance. Brief Bioinform 20:1094–1102

    Article  CAS  PubMed  Google Scholar 

  19. Clinical and Laboratory Standards Institute (2019) Performance standards for antimicrobial susceptibility testing. 29th ed. CLSI supplement M100. Wayne, PA

  20. Richter M, Rosselló-Móra R (2009) Shifting the genomic gold standard for the prokaryotic species definition. Proc Natl Acad Sci USA (vol 106, pp. 19126–19131)

  21. Li XZ, Zhang L, Poole K (2002) SmeC, an outer membrane multidrug efflux protein of Stenotrophomonas maltophilia. Antimicrob Agents Chemother 46:333–343

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Zhang L, Li XZ, Poole K (2001) SmeDEF multidrug efflux pump contributes to intrinsic multidrug resistance in Stenotrophomonas maltophilia. Antimicrob Agents Chemother 45:3497–3503

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Okazaki A, Avison MB (2007) Aph(3’)-IIc, an aminoglycoside resistance determinant from Stenotrophomonas maltophilia. Antimicrob Agents Chemother 51:359–360

    Article  CAS  PubMed  Google Scholar 

  24. Lambert T, Ploy MC, Denis F, Courvalin P (1999) Characterization of the chromosomal aac(6’)-Iz gene of Stenotrophomonas maltophilia. Antimicrob Agents Chemother 43:2366–2371

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Rhoads DD (2021) Stenotrophomonas maltophilia susceptibility testing challenges and strategies. J Clin Microbiol 59:e0109421

    Article  PubMed  Google Scholar 

  26. Mojica MF, Rutter JD, Taracila M, Abriata LA, Fouts DE, Papp-Wallace KM, Walsh TJ, LiPuma JJ, Vila AJ, Bonomo RA (2019) Population structure, molecular epidemiology, and β-lactamase diversity among Stenotrophomonas maltophilia isolates in the United States. MBio 10:e00405-e419

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Looney WJ, Narita M, Mühlemann K (2009) Stenotrophomonas maltophilia: an emerging opportunist human pathogen. Lancet Infect Dis 9:312–323

    Article  CAS  PubMed  Google Scholar 

  28. Fluit AC, Bayjanov JR, Aguilar MD, Cantón R, Elborn S, Tunney MM, Scharringa J, Benaissa-Trouw BJ, Ekkelenkamp MB (2022) Taxonomic position, antibiotic resistance and virulence factor production by Stenotrophomonas isolates from patients with cystic fibrosis and other chronic respiratory infections. BMC Microbiol 22:129

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. McLaughlin RW, Cochran PA, Dowd SE (2015) Metagenomic analysis of the gut microbiota of the timber rattlesnake, Crotalus horridus. Mol Biol Rep 42:1187–1195

    Article  CAS  PubMed  Google Scholar 

  30. Torres RT, Cunha MV, Araujo D, Ferreira H, Fonseca C, Palmeira JD (2022) A walk on the wild side: Wild ungulates as potential reservoirs of multi-drug resistant bacteria and genes, including Escherichia coli harbouring CTX-M beta-lactamases. Environ Pollut 306:119367

    Article  CAS  PubMed  Google Scholar 

Download references

Funding

This project was supported by the University of Wisconsin-La Crosse Undergraduate Research and Creativity Committee grant for Noah Grover.

Author information

Authors and Affiliations

Authors

Contributions

RW and XL designed and supervised the project. RW, NR, and XL conducted the experiments. RW prepared the first draft the manuscript. RW and XL finalize the manuscript.

Corresponding author

Correspondence to Xinhui Li.

Ethics declarations

Conflict of interest

The authors declare that that there is no conflict of interest.

Ethical Approval

Samples were collected under the auspices of Institutional Animal Care and Use Committee (IACUC) approved permit K145011020Q.

Consent to Participate

Not applicable.

Consent for Publication

All authors agree to publish.

Declaration of Deposition in Repositories

Not applicable.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 42 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Li, X., McLaughlin, R.W. & Grover, N.A. Characterization of Antibiotic-Resistant Stenotrophomonas Isolates from Painted Turtles Living in the Wild. Curr Microbiol 80, 93 (2023). https://doi.org/10.1007/s00284-023-03193-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00284-023-03193-4

Keywords

Navigation