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Whole Genome Sequence Analysis of Burkholderia contaminans FFH2055 Strain Reveals the Presence of Putative β-Lactamases

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Abstract

Burkholderia contaminans is a member of the Burkholderia cepacia complex (Bcc), a pathogen with increasing prevalence among cystic fibrosis (CF) patients and the cause of numerous outbreaks due to the use of contaminated commercial products. The antibiotic resistance determinants, particularly β-lactamases, have been poorly studied in this species. In this work, we explored the whole genome sequence (WGS) of a B. contaminans isolate (FFH 2055) and detected four putative β-lactamase-encoding genes. In general, these genes have more than 93% identity with β-lactamase genes found in other Bcc species. Two β-lactamases, a class A (Pen-like, suggested name PenO) and a class D (OXA-like), were further analyzed and characterized. Amino acid sequence comparison showed that Pen-like has 82% and 67% identity with B. multivorans PenA and B. pseudomallei PenI, respectively, while OXA-like displayed strong homology with class D enzymes within the Bcc, but only 22–44% identity with available structures from the OXA family. PCR reactions designed to study the presence of these two genes revealed a heterogeneous distribution among clinical and industrial B. contaminans isolates. Lastly, blaPenO gene was cloned and expressed into E. coli to investigate the antibiotic resistance profile and confers an extended-spectrum β-lactamase (ESBL) phenotype. These results provide insight into the presence of β-lactamases in B. contaminans, suggesting they play a role in antibiotic resistance of these bacteria.

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References

  1. Kelly J (2017) Environmental scan of cystic fibrosis research worldwide. J Cyst Fibros 16(3):367–370. https://doi.org/10.1016/j.jcf.2016.11.002

    Article  PubMed  Google Scholar 

  2. Gilligan PH (2014) Infections in patients with cystic fibrosis: diagnostic microbiology update. Clin Lab Med 34(2):197–217. https://doi.org/10.1016/j.cll.2014.02.001

    Article  PubMed  PubMed Central  Google Scholar 

  3. Sherrard LJ, Tunney MM, Elborn JS (2014) Antimicrobial resistance in the respiratory microbiota of people with cystic fibrosis. Lancet 384(9944):703–713. https://doi.org/10.1016/S0140-6736(14)61137-5

    Article  CAS  PubMed  Google Scholar 

  4. Mahenthiralingam E, Baldwin A, Dowson CG (2008) Burkholderia cepacia complex bacteria: opportunistic pathogens with important natural biology. J Appl Microbiol 104(6):1539–1551. https://doi.org/10.1111/j.1365-2672.2007.03706.x

    Article  CAS  PubMed  Google Scholar 

  5. De Smet B, Mayo M, Peeters C, Zlosnik JE, Spilker T, Hird TJ, LiPuma JJ, Kidd TJ, Kaestli M, Ginther JL, Wagner DM, Keim P, Bell SC, Jacobs JA, Currie BJ, Vandamme P (2015) Burkholderia stagnalis sp. nov. and Burkholderia territorii sp. nov., two novel Burkholderia cepacia complex species from environmental and human sources. Int J Syst Evol Microbiol 65(7):2265–2271. https://doi.org/10.1099/ijs.0.000251

    Article  CAS  PubMed  Google Scholar 

  6. Isles A, Maclusky I, Corey M, Gold R, Prober C, Fleming P, Levison H (1984) Pseudomonas cepacia infection in cystic fibrosis: an emerging problem. J Pediatr 104(2):206–210

    Article  CAS  PubMed  Google Scholar 

  7. Zhou J, Chen Y, Tabibi S, Alba L, Garber E, Saiman L (2007) Antimicrobial susceptibility and synergy studies of Burkholderia cepacia complex isolated from patients with cystic fibrosis. Antimicrob Agents Chemother 51(3):1085–1088. https://doi.org/10.1128/AAC.00954-06

    Article  CAS  PubMed  Google Scholar 

  8. Song JE, Kwak YG, Um TH, Cho CR, Kim S, Park IS, Hwang JH, Kim N, Oh GB (2017) Outbreak of Burkholderia cepacia pseudobacteraemia caused by intrinsically contaminated commercial 0.5% chlorhexidine solution in neonatal intensive care units. J Hosp Infect. https://doi.org/10.1016/j.jhin.2017.09.012

    Article  PubMed  Google Scholar 

  9. Torbeck L, Raccasi D, Guilfoyle DE, Friedman RL, Hussong D (2011) Burkholderia cepacia: this decision is overdue. PDA J Pharm Sci Technol 65(5):535–543. https://doi.org/10.5731/pdajpst.2011.00793

    Article  PubMed  Google Scholar 

  10. Vonberg RP, Gastmeier P (2007) Hospital-acquired infections related to contaminated substances. J Hosp Infect 65(1):15–23. https://doi.org/10.1016/j.jhin.2006.09.018

    Article  PubMed  Google Scholar 

  11. Baldwin A, Mahenthiralingam E, Drevinek P, Pope C, Waine DJ, Henry DA, Speert DP, Carter P, Vandamme P, LiPuma JJ, Dowson CG (2008) Elucidating global epidemiology of Burkholderia multivorans in cases of cystic fibrosis by multilocus sequence typing. J Clin Microbiol 46(1):290–295. https://doi.org/10.1128/JCM.01818-07

    Article  CAS  PubMed  Google Scholar 

  12. Lipuma JJ (2010) The changing microbial epidemiology in cystic fibrosis. Clin Microbiol Rev 23(2):299–323. https://doi.org/10.1128/CMR.00068-09

    Article  PubMed  PubMed Central  Google Scholar 

  13. Zlosnik JE, Zhou G, Brant R, Henry DA, Hird TJ, Mahenthiralingam E, Chilvers MA, Wilcox P, Speert DP (2015) Burkholderia species infections in patients with cystic fibrosis in British Columbia, Canada. 30 years’ experience. Ann Am Thorac Soc 12(1):70–78. https://doi.org/10.1513/AnnalsATS.201408-395OC

    Article  PubMed  Google Scholar 

  14. Vanlaere E, Baldwin A, Gevers D, Henry D, De Brandt E, LiPuma JJ, Mahenthiralingam E, Speert DP, Dowson C, Vandamme P (2009) Taxon K, a complex within the Burkholderia cepacia complex, comprises at least two novel species, Burkholderia contaminans sp. nov. and Burkholderia lata sp. nov. Int J Syst Evol Microbiol 59(Pt 1):102–111. https://doi.org/10.1099/ijs.0.001123-0

    Article  CAS  PubMed  Google Scholar 

  15. Coutinho CP, Barreto C, Pereira L, Lito L, Melo Cristino J, Sa-Correia I (2015) Incidence of Burkholderia contaminans at a cystic fibrosis centre with an unusually high representation of Burkholderia cepacia during 15 years of epidemiological surveillance. J Med Microbiol 64(8):927–935. https://doi.org/10.1099/jmm.0.000094

    Article  CAS  PubMed  Google Scholar 

  16. Martin M, Christiansen B, Caspari G, Hogardt M, von Thomsen AJ, Ott E, Mattner F (2011) Hospital-wide outbreak of Burkholderia contaminans caused by prefabricated moist washcloths. J Hosp Infect 77(3):267–270. https://doi.org/10.1016/j.jhin.2010.10.004

    Article  CAS  PubMed  Google Scholar 

  17. Martina P, Bettiol M, Vescina C, Montanaro P, Mannino MC, Prieto CI, Vay C, Naumann D, Schmitt J, Yantorno O, Lagares A, Bosch A (2013) Genetic diversity of Burkholderia contaminans isolates from cystic fibrosis patients in Argentina. J Clin Microbiol 51(1):339–344. https://doi.org/10.1128/JCM.02500-12

    Article  PubMed  PubMed Central  Google Scholar 

  18. Medina-Pascual MJ, Valdezate S, Carrasco G, Villalon P, Garrido N, Saez-Nieto JA (2015) Increase in isolation of Burkholderia contaminans from Spanish patients with cystic fibrosis. Clin Microbiol Infect 21(2):150–156. https://doi.org/10.1016/j.cmi.2014.07.014

    Article  CAS  PubMed  Google Scholar 

  19. Moehring RW, Lewis SS, Isaacs PJ, Schell WA, Thomann WR, Althaus MM, Hazen KC, Dicks KV, Lipuma JJ, Chen LF, Sexton DJ (2014) Outbreak of bacteremia due to Burkholderia contaminans linked to intravenous fentanyl from an institutional compounding pharmacy. JAMA Intern Med 174(4):606–612. https://doi.org/10.1001/jamainternmed.2013.13768

    Article  CAS  PubMed  Google Scholar 

  20. Peterson AE, Chitnis AS, Xiang N, Scaletta JM, Geist R, Schwartz J, Dement J, Lawlor E, Lipuma JJ, O’Connell H, Noble-Wang J, Kallen AJ, Hunt DC (2013) Clonally related Burkholderia contaminans among ventilated patients without cystic fibrosis. Am J Infect Control 41(12):1298–1300. https://doi.org/10.1016/j.ajic.2013.05.015

    Article  PubMed  PubMed Central  Google Scholar 

  21. Nunvar J, Kalferstova L, Bloodworth RA, Kolar M, Degrossi J, Lubovich S, Cardona ST, Drevinek P (2016) Understanding the pathogenicity of Burkholderia contaminans, an emerging pathogen in cystic fibrosis. PLoS ONE 11(8):e0160975. https://doi.org/10.1371/journal.pone.0160975

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Deng P, Wang X, Baird SM, Showmaker KC, Smith L, Peterson DG, Lu S (2016) Comparative genome-wide analysis reveals that Burkholderia contaminans MS14 possesses multiple antimicrobial biosynthesis genes but not major genetic loci required for pathogenesis. MicrobiologyOpen 5(3):353–369. https://doi.org/10.1002/mbo3.333

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Haim MS, Mollerach M, Van Domselaar G, Teves SA, Degrossi J, Cardona ST (2016) Draft genome sequences of Burkholderia contaminans FFI-28, a strain isolated from a contaminated pharmaceutical solution. Genome Announcements. https://doi.org/10.1128/genomeA.01177-16

    Article  PubMed  PubMed Central  Google Scholar 

  24. Jung JY, Ahn Y, Kweon O, LiPuma JJ, Hussong D, Marasa BS, Cerniglia CE (2017) Improved high-quality draft genome sequence and annotation of Burkholderia contaminans LMG 23361(T). Genome Announcements. https://doi.org/10.1128/genomeA.00245-17

    Article  PubMed  PubMed Central  Google Scholar 

  25. Burns J (2006) Antibiotic resistance of Burkholderia spp. In: Coenye PVT (ed) Burkholderia: molecular microbiology and genomics. Horizon Bioscience, Norfolk, pp 81–91

    Google Scholar 

  26. Drevinek P, Mahenthiralingam E (2010) Burkholderia cenocepacia in cystic fibrosis: epidemiology and molecular mechanisms of virulence. Clin Microbiol Infect 16(7):821–830. https://doi.org/10.1111/j.1469-0691.2010.03237.x

    Article  CAS  PubMed  Google Scholar 

  27. Ramirez MS, Vargas LJ, Cagnoni V, Tokumoto M, Centron D (2005) Class 2 integron with a novel cassette array in a Burkholderia cenocepacia isolate. Antimicrob Agents Chemother 49(10):4418–4420. https://doi.org/10.1128/AAC.49.10.4418-4420.2005

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Trepanier S, Prince A, Huletsky A (1997) Characterization of the penA and penR genes of Burkholderia cepacia 249 which encode the chromosomal class A penicillinase and its LysR-type transcriptional regulator. Antimicrob Agents Chemother 41(11):2399–2405

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Poirel L, Rodriguez-Martinez JM, Plesiat P, Nordmann P (2009) Naturally occurring Class A ss-lactamases from the Burkholderia cepacia complex. Antimicrob Agents Chemother 53(3):876–882. https://doi.org/10.1128/AAC.00946-08

    Article  CAS  PubMed  Google Scholar 

  30. Papp-Wallace KM, Taracila MA, Gatta JA, Ohuchi N, Bonomo RA, Nukaga M (2013) Insights into beta-lactamases from Burkholderia species, two phylogenetically related yet distinct resistance determinants. J Biol Chem 288(26):19090–19102. https://doi.org/10.1074/jbc.M113.458315

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Papp-Wallace KM, Becka SA, Taracila MA, Zeiser ET, Gatta JA, LiPuma JJ, Bonomo RA (2017) Exploring the role of the Omega-loop in the evolution of Ceftazidime resistance in the PenA beta-lactamase from Burkholderia multivorans, an important cystic fibrosis pathogen. Antimicrob Agents Chemother. https://doi.org/10.1128/AAC.01941-16

    Article  PubMed  PubMed Central  Google Scholar 

  32. Everaert A, Coenye T (2016) Effect of beta-Lactamase inhibitors on in vitro activity of beta-Lactam antibiotics against Burkholderia cepacia complex species. Antimicrob Resist Infect Control 5:44. https://doi.org/10.1186/s13756-016-0142-3

    Article  PubMed  PubMed Central  Google Scholar 

  33. Holden MT, Seth-Smith HM, Crossman LC, Sebaihia M, Bentley SD, Cerdeno-Tarraga AM, Thomson NR, Bason N, Quail MA, Sharp S, Cherevach I, Churcher C, Goodhead I, Hauser H, Holroyd N, Mungall K, Scott P, Walker D, White B, Rose H, Iversen P, Mil-Homens D, Rocha EP, Fialho AM, Baldwin A, Dowson C, Barrell BG, Govan JR, Vandamme P, Hart CA, Mahenthiralingam E, Parkhill J (2009) The genome of Burkholderia cenocepacia J2315, an epidemic pathogen of cystic fibrosis patients. J Bacteriol 191(1):261–277. https://doi.org/10.1128/JB.01230-08

    Article  CAS  PubMed  Google Scholar 

  34. Bloodworth RA, Selin C, Lopez De Volder MA, Drevinek P, Galanternik L, Degrossi J, Cardona ST (2015) Draft genome sequences of Burkholderia contaminans, a Burkholderia cepacia complex species that is increasingly recovered from cystic fibrosis patients. Genome Announcements. https://doi.org/10.1128/genomeA.00766-15

    Article  PubMed  PubMed Central  Google Scholar 

  35. Becka SA, Zeiser ET, Marshall SH, Gatta JA, Nguyen K, Singh I, Greco C, Sutton GG, Fouts DE, LiPuma JJ, Papp-Wallace KM (2018) Sequence heterogeneity of the PenA carbapenemase in clinical isolates of Burkholderia multivorans. Diagn Microbiol Infect Dis 92(3):253–258. https://doi.org/10.1016/j.diagmicrobio.2018.06.005

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Aziz RK, Bartels D, Best AA, DeJongh M, Disz T, Edwards RA, Formsma K, Gerdes S, Glass EM, Kubal M, Meyer F, Olsen GJ, Olson R, Osterman AL, Overbeek RA, McNeil LK, Paarmann D, Paczian T, Parrello B, Pusch GD, Reich C, Stevens R, Vassieva O, Vonstein V, Wilke A, Zagnitko O (2008) The RAST server: rapid annotations using subsystems technology. BMC Genomics 9:75. https://doi.org/10.1186/1471-2164-9-75

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Overbeek R, Olson R, Pusch GD, Olsen GJ, Davis JJ, Disz T, Edwards RA, Gerdes S, Parrello B, Shukla M, Vonstein V, Wattam AR, Xia F, Stevens R (2014) The SEED and the rapid annotation of microbial genomes using subsystems technology (RAST). Nucleic Acids Res 42(Database issue):D206–D214. https://doi.org/10.1093/nar/gkt1226

    Article  CAS  PubMed  Google Scholar 

  38. Winsor GL, Khaira B, Van Rossum T, Lo R, Whiteside MD, Brinkman FS (2008) The Burkholderia genome database: facilitating flexible queries and comparative analyses. Bioinformatics 24(23):2803–2804. https://doi.org/10.1093/bioinformatics/btn524

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Gouet P, Robert X, Courcelle E (2003) ESPript/ENDscript: extracting and rendering sequence and 3D information from atomic structures of proteins. Nucleic Acids Res 31(13):3320–3323

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Notredame C, Higgins DG, Heringa J (2000) T-Coffee: a novel method for fast and accurate multiple sequence alignment. J Mol Biol 302(1):205–217. https://doi.org/10.1006/jmbi.2000.4042

    Article  CAS  PubMed  Google Scholar 

  42. Muñoz V, Serrano L (1997) Development of the multiple sequence approximation within the AGADIR model of alpha-helix formation: comparison with Zimm-Bragg and Lifson-Roig formalisms. Biopolymers 41(5):495–509

    Article  PubMed  Google Scholar 

  43. Krieger E, Darden T, Nabuurs SB, Finkelstein A, Vriend G (2004) Making optimal use of empirical energy functions: force-field parameterization in crystal space. Proteins 57(4):678–683. https://doi.org/10.1002/prot.20251

    Article  CAS  PubMed  Google Scholar 

  44. Schrödinger L The PyMOL molecular Graphics System., 1.5.0.4 edn.

  45. Koressaar T, Remm M (2007) Enhancements and modifications of primer design program Primer3. Bioinformatics 23(10):1289–1291. https://doi.org/10.1093/bioinformatics/btm091

    Article  CAS  PubMed  Google Scholar 

  46. Untergasser A, Cutcutache I, Koressaar T, Ye J, Faircloth BC, Remm M, Rozen SG (2012) Primer3–new capabilities and interfaces. Nucleic Acids Res 40(15):e115. https://doi.org/10.1093/nar/gks596

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Clinical and Laboratory Standards Institute (2017) Performance standards for antimicrobial susceptibility testing; twenty-sixth informational supplement M100-S27, vol 37. vol 1. Clinical and Laboratory Standards Institute, Wayne

    Google Scholar 

  48. Bret L, Chaibi EB, Chanal-Claris C, Sirot D, Labia R, Sirot J (1997) Inhibitor-resistant TEM (IRT) b-lactamases with different substitutions at position 244. Antimicrob Agents Chemother 41(11):2547–2549

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Perez-Llarena FJ, Cartelle M, Mallo S, Beceiro A, Perez A, Villanueva R, Romero A, Bonnet R, Bou G (2008) Structure-function studies of arginine at position 276 in CTX-M b-lactamases. J Antimicrob Chemother 61(4):792–797. https://doi.org/10.1093/jac/dkn031

    Article  CAS  PubMed  Google Scholar 

  50. Ruggiero M, Kerff F, Herman R, Sapunaric F, Galleni M, Gutkind G, Charlier P, Sauvage E, Power P (2014) Crystal structure of the extended-spectrum beta-lactamase PER-2 and insights into the role of specific residues in the interaction with beta-lactams and beta-lactamase inhibitors. Antimicrob Agents Chemother. https://doi.org/10.1128/AAC.00089-14

    Article  PubMed  PubMed Central  Google Scholar 

  51. Ruggiero M, Curto L, Brunetti F, Sauvage E, Galleni M, Power P, Gutkind G (2017) Impact of mutations at Arg220 and Thr237 in PER-2 beta-lactamase on conformation, activity, and susceptibility to inhibitors. Antimicrob Agents Chemother. https://doi.org/10.1128/AAC.02193-16

    Article  PubMed  PubMed Central  Google Scholar 

  52. Chen Y, Delmas J, Sirot J, Shoichet B, Bonnet R (2005) Atomic resolution structures of CTX-M beta-lactamases: extended spectrum activities from increased mobility and decreased stability. J Mol Biol 348(2):349–362. https://doi.org/10.1016/j.jmb.2005.02.010

    Article  CAS  PubMed  Google Scholar 

  53. Delmas J, Chen Y, Prati F, Robin F, Shoichet BK, Bonnet R (2008) Structure and dynamics of CTX-M enzymes reveal insights into substrate accommodation by extended-spectrum beta-lactamases. J Mol Biol 375(1):192–201. https://doi.org/10.1016/j.jmb.2007.10.026

    Article  CAS  PubMed  Google Scholar 

  54. Toleman MA, Rolston K, Jones RN, Walsh TR (2003) Molecular and biochemical characterization of OXA-45, an extended-spectrum class 2d’ beta-lactamase in Pseudomonas aeruginosa. Antimicrob Agents Chemother 47(9):2859–2863

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Stojanoski V, Chow DC, Fryszczyn B, Hu L, Nordmann P, Poirel L, Sankaran B, Prasad BV, Palzkill T (2015) Structural basis for different substrate profiles of two closely related class d beta-lactamases and their inhibition by halogens. Biochemistry 54(21):3370–3380. https://doi.org/10.1021/acs.biochem.5b00298

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

Research reported in this publication was supported in part by funds and/or facilities provided by the Cleveland Department of Veterans Affairs, the Veterans Affairs Merit Review Program BX002872 (KMP-W) and BX001974 (RAB) from the United States (U.S.) Department of Veterans Affairs Biomedical Laboratory Research and Development Service, and the Geriatric Research Education and Clinical Center VISN 10 to RAB. The contents do not represent the views of the U.S. Department of Veterans Affairs or the United States Government. This study was partially supported by National Institute of Allergy and Infectious Diseases of the National Institutes of Health under Award Numbers R21AI114508, R01AI100560, R01AI063517, and R01AI072219 to RAB. The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health. We want to thank Dr. Ana P. Meo (Hospital Ramos Mejía) and Dr. Carlos Vay (Hospital de Clínicas General San Martín) for providing the non-CF B. contaminans isolates for this study. Special thanks are offered to Dr. German M. Traglia for his technical help in bioinformatics analysis.

Funding

This work was funded by grants from Agencia Nacional de Promoción Científica y Tecnológica (PICT 2014-0457 to PP). P. Power is a researcher for the Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET, Argentina). JF has a SOAR-ELEVAR Scholar Fellowship from Latina/o Graduate Students from the U.S. Department of Education.

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Authors and Affiliations

  1. Cátedra de Salud Pública e Higiene Ambiental, Facultad de Farmacia y Bioquímica, Universidad de Buenos Aires, Buenos Aires, Argentina

    José J. Degrossi & Nicolás E. Bo

  2. Department of Biological Science, California State University Fullerton, 800 N State College Blvd, Fullerton, CA, 92831, USA

    Cindy Merino, Chelsea Collins, Mariana Papalia, Jennifer S. Fernandez & María S. Ramirez

  3. Servicio de Bacteriología, Hospital de Pediatría Juan P. Garrahan, Buenos Aires, Argentina

    Adela M. Isasmendi & Claudia M. Hernandez

  4. Servicio de Bacteriología, Hospital de Niños Ricardo Gutierrez, Buenos Aires, Argentina

    Lorena M. Ibarra & Miryam S. Vazquez

  5. Cátedra de Microbiología, Laboratorio de Resistencia Bacteriana, Facultad de Farmacia y Bioquímica, Universidad de Buenos Aires, Buenos Aires, Argentina

    Mariana Papalia & Pablo Power

  6. Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Buenos Aires, Argentina

    Pablo Power

  7. Research Service, Louis Stokes Cleveland Department of Veterans Affairs, Cleveland, OH, 44106, USA

    Krisztina M. Papp-Wallace & Robert A. Bonomo

  8. Department of Medicine, Case Western Reserve University, Cleveland, OH, 44106, USA

    Krisztina M. Papp-Wallace & Robert A. Bonomo

  9. Department of Biochemistry, Case Western Reserve University, Cleveland, OH, 44106, USA

    Krisztina M. Papp-Wallace & Robert A. Bonomo

  10. Departments of Microbiology and Molecular Biology, Case Western Reserve University, Cleveland, OH, 44106, USA

    Robert A. Bonomo

  11. Department of Pharmacology, Case Western Reserve University, Cleveland, OH, 44106, USA

    Robert A. Bonomo

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  1. José J. Degrossi
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  2. Cindy Merino
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Correspondence to María S. Ramirez.

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Figure S1

. Burkholderia cepacia complex (Bcc) whole-genome phylogram of representative genomes showing the distribution of class B, C and D β-lactamases using the composition vector method. (JPEG 4616 KB)

Figure S2

. Genetic context of blaPen genes. Arrows represent the direction of transcription. (TIF 251 KB)

Figure S3

. Genetic environment of blaOXA-like. Arrows represent the direction of transcription. (TIF 213 KB)

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Degrossi, J.J., Merino, C., Isasmendi, A.M. et al. Whole Genome Sequence Analysis of Burkholderia contaminans FFH2055 Strain Reveals the Presence of Putative β-Lactamases. Curr Microbiol 76, 485–494 (2019). https://doi.org/10.1007/s00284-019-01653-4

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