A whole-cell hypersensitive biosensor for beta-lactams based on the AmpR-AmpC regulatory circuit from the Antarctic Pseudomonas sp. IB20.
Journal
Microbial biotechnology
ISSN: 1751-7915
Titre abrégé: Microb Biotechnol
Pays: United States
ID NLM: 101316335
Informations de publication
Date de publication:
10 Jan 2024
10 Jan 2024
Historique:
revised:
25
10
2023
received:
11
08
2023
accepted:
26
11
2023
medline:
10
1
2024
pubmed:
10
1
2024
entrez:
10
1
2024
Statut:
aheadofprint
Résumé
Detecting antibiotic residues is vital to minimize their impact. Yet, existing methods are complex and costly. Biosensors offer an alternative. While many biosensors detect various antibiotics, specific ones for beta-lactams are lacking. To address this gap, a biosensor based on the AmpC beta-lactamase regulation system (ampR-ampC) from Pseudomonas sp. IB20, an Antarctic isolate, was developed in this study. The AmpR-AmpC system is well-conserved in the genus Pseudomonas and has been extensively studied for its involvement in peptidoglycan recycling and beta-lactam resistance. To create the biosensor, the ampC coding sequence was replaced with the mCherry fluorescent protein as a reporter, resulting in a transcriptional fusion. This construct was then inserted into Escherichia coli SN0301, a beta-lactam hypersensitive strain, generating a whole-cell biosensor. The biosensor demonstrated dose-dependent detection of penicillins, cephalosporins and carbapenems. However, the most interesting aspect of this work is the high sensitivity presented by the biosensor in the detection of carbapenems, as it was able to detect 8 pg/mL of meropenem and 40 pg/mL of imipenem and reach levels of 1-10 ng/mL for penicillins and cephalosporins. This makes the biosensor a powerful tool for the detection of beta-lactam antibiotics, specifically carbapenems, in different matrices.
Identifiants
pubmed: 38197486
doi: 10.1111/1751-7915.14385
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : Agencia Nacional de Investigación y Desarrollo
ID : REDES190148
Organisme : Fondo de Financiamiento de Centros de Investigación en Áreas Prioritarias
ID : MICROB-R
Organisme : Fondo de Financiamiento de Centros de Investigación en Áreas Prioritarias
ID : NCN17-08
Organisme : Universidad de Valparaíso
ID : DIUV-CIDI 4/2016
Organisme : ANID Millenium Science Initiative
ID : NCN17-08
Organisme : ANID REDES
ID : 190148
Organisme : DIUV-CIDI
ID : 4/2016
Informations de copyright
© 2023 The Authors. Microbial Biotechnology published by Applied Microbiology International and John Wiley & Sons Ltd.
Références
Alnassrallah, M.N., Alzoman, N.Z. & Almomen, A. (2022) Qualitative immunoassay for the determination of tetracycline antibiotic residues in milk samples followed by a quantitative improved HPLC-DAD method. Scientific Reports, 12, 14502.
Andresen, M., Araos, J., Wong, K.Y., Leung, Y.C., So, L.Y., Wong, W.T. et al. (2018) Evaluation of meropenem pharmacokinetics in an experimental acute respiratory distress syndrome (ARDS) model during extracorporeal membrane oxygenation (ECMO) by using a PenP β-lactamase biosensor. Sensors, 18, 1424.
Arce-Rodríguez, A., Benedetti, I., Borrero-De Acuña, J.M., Silva-Rocha, R. & de Lorenzo, V. (2023) Standardization of inducer-activated broad host range expression modules: debugging and refactoring an alkane-responsive AlkS/PalkB device. Synthetic Biology, 8, 1-11.
Au, H.W., Tsang, M.W., Chen, Y.W., So, P.K., Wong, K.Y. & Leung, Y.C. (2020) BADAN-conjugated β-lactamases as biosensors for β-lactam antibiotic detection. PLoS One, 15, e0241594.
Balasubramanian, D., Kumari, H. & Mathee, K. (2015) Pseudomonas aeruginosa AmpR: an acute-chronic switch regulator. Pathogens and Disease, 73, 1.
Bartowsky, E. & Normark, S. (1993) Interactions of wild-type and mutant AmpR of Citrobacter freundii with target DNA. Molecular Microbiology, 10, 555-565.
Bengtsson-Palme, J., Kristiansson, E. & Larsson, D.G.J. (2018) Environmental factors influencing the development and spread of antibiotic resistance. FEMS Microbiology Reviews, 42, 68-80.
Bengtsson-Palme, J. & Larsson, D.G.J. (2015) Antibiotic resistance genes in the environment: prioritizing risks. Nature Reviews. Microbiology, 13, 396.
Caille, O., Zincke, D., Merighi, M., Balasubramanian, D., Kumari, H., Kong, K.F. et al. (2014) Structural and functional characterization of Pseudomonas aeruginosa global regulator AmpR. Journal of Bacteriology, 196, 3890-3902.
Chambers, H.F. & Miick, C. (1992) Characterization of penicillin-binding protein 2 of Staphylococcus aureus: deacylation reaction and identification of two penicillin-binding peptides. Antimicrobial Agents and Chemotherapy, 36, 656-661.
Chinnappan, R., Eissa, S., Alotaibi, A., Siddiqua, A., Alsager, O.A. & Zourob, M. (2020) In vitro selection of DNA aptamers and their integration in a competitive voltammetric biosensor for azlocillin determination in wastewater. Analytica Chimica Acta, 1101, 149-156.
CLSI. (2018) Performance standards for antimicrobial susceptibility testing. Wyne, PA, USA: Clinical and Laboratory Standards Institute.
Codjoe, F.S. & Donkor, E.S. (2017) Carbapenem resistance: a review. Medical Science, 6, 1.
Coque, T.M., Cantón, R., Pérez-Cobas, A.E., Fernández-de-Bobadilla, M.D. & Baquero, F. (2023) Antimicrobial resistance in the global health network: known unknowns and challenges for efficient responses in the 21st century. Microorganisms, 11, 1050.
Davies, T.A., Page, M.G.P., Shang, W., Andrew, T., Kania, M. & Bush, K. (2007) Binding of ceftobiprole and comparators to the penicillin-binding proteins of Escherichia coli, Pseudomonas aeruginosa, Staphylococcus aureus, and Streptococcus pneumoniae. Antimicrobial Agents and Chemotherapy, 51, 2621-2624.
Dietz, H., Pfeifle, D. & Wiedemann, B. (1996) Location of N-acetylmuramyl-L-alanyl-D-glutamylmesodiaminopimelic acid, presumed signal molecule for β-lactamase induction, in the bacterial cell. Antimicrobial Agents and Chemotherapy, 40, 2173-2177.
Dik, D.A., Kim, C., Madukoma, C.S., Fisher, J.F., Shrout, J.D. & Mobashery, S. (2020) Fluorescence assessment of the ampR-signaling network of Pseudomonas aeruginosa to exposure to β-lactam antibiotics. ACS Chemical Biology, 15, 1184-1194.
Feng, G., Huang, H. & Chen, Y. (2021) Effects of emerging pollutants on the occurrence and transfer of antibiotic resistance genes: a review. Journal of Hazardous Materials, 420, 126602.
Fontana, R., Cornaglia, G., Ligozzi, M. & Mazzariol, A. (2000) The final goal: penicillin-binding proteins and the target of cephalosporins. Clinical Microbiology and Infection, 6, 34-40.
Gaudin, V. (2017) Advances in biosensor development for the screening of antibiotic residues in food products of animal origin: a comprehensive review. Biosensors & Bioelectronics, 90, 363-377.
Griboff, J., Carrizo, J.C., Bonansea, R.I., Valdés, M.E., Wunderlin, D.A. & Amé, M.V. (2020) Multiantibiotic residues in commercial fish from Argentina. The presence of mixtures of antibiotics in edible fish, a challenge to health risk assessment. Food Chemistry, 332, 127380.
Gutmann, L., Vincent, S., Billot-Klein, D., Acar, J.F., Mrèna, E. & Williamson, R. (1986) Involvement of penicillin-binding protein 2 with other penicillin-binding proteins in lysis of Escherichia coli by some β-lactam antibiotics alone and in synergistic lytic effect of amdinocillin (mecillinam). Antimicrobial Agents and Chemotherapy, 30, 906-912.
Higuera-Llantén, S., Vásquez-Ponce, F., Núñez-Gallegos, M., Pavlov, M.S., Marshall, S. & Olivares-Pacheco, J. (2018) Phenotypic and genotypic characterization of a novel multi-antibiotic-resistant, alginate hyperproducing strain of Pseudomonas mandelii isolated in Antarctica. Polar Biology, 41, 469-480.
Jacobs, C., Huang, L.J., Bartowsky, E., Normark, S. & Park, J.T. (1994) Bacterial cell wall recycling provides cytosolic muropeptides as effectors for β-lactamase induction. EMBO Journal, 13, 4684-4694.
Juan, C., Torrens, G., González-Nicolau, M. & Oliver, A. (2017) Diversity and regulation of intrinsic β-lactamases from non-fermenting and other gram-negative opportunistic pathogens. FEMS Microbiology Reviews, 41, 781-815.
Kim, C., Ryu, H.D., Chung, E.G., Kim, Y. & Lee, J.k. (2018) A review of analytical procedures for the simultaneous determination of medically important veterinary antibiotics in environmental water: sample preparation, liquid chromatography, and mass spectrometry. Journal of Environmental Management, 217, 629-645.
Kocaoglu, O. & Carlson, E.E. (2015) Profiling of β-lactam selectivity for penicillin-binding proteins in Escherichia coli strain DC2. Antimicrobial Agents and Chemotherapy, 59, 2785-2790.
Lautenschläger, N., Popp, P.F. & Mascher, T. (2020) Development of a novel heterologous β-lactam-specific whole-cell biosensor in Bacillus subtilis. Journal of Biological Engineering, 14, 1-14.
Lindquist, S., Lindberg, F. & Normark, S. (1989) Binding of the Citrobacter freundii ampR regulator to a single DNA site provides both autoregulation and activation of the inducible ampC β-lactamase gene. Journal of Bacteriology, 171, 3746-3753.
Liu, X., Lu, S., Guo, W., Xi, B. & Wang, W. (2018) Antibiotics in the aquatic environments: a review of lakes, China. Science of the Total Environment, 627, 1195-1208.
Livermore, D.M. & Woodford, N. (2006) The beta-lactamase threat in Enterobacteriaceae, Pseudomonas and Acinetobacter. Trends in Microbiology, 14, 413-420.
Mehlhorn, A., Rahimi, P. & Joseph, Y. (2018) Aptamer-based biosensors for antibiotic detection: a review. Biosensors, 8, 54.
Meng, Q., Liu, S., Meng, J., Feng, J., Mecklenburg, M., Zhu, L. et al. (2021) Rapid personalized AMR diagnostics using two-dimensional antibiotic resistance profiling strategy employing a thermometric NDM-1 biosensor. Biosensors & Bioelectronics, 193, 113526.
Morehead, M.S. & Scarbrough, C. (2018) Emergence of global antibiotic resistance. Primary Care, 45, 467-484.
Moya, B., Dötsch, A., Juan, C., Blázquez, J., Zamorano, L., Haussler, S. et al. (2009) β-Lactam resistance response triggered by inactivation of a nonessential penicillin-binding protein. PLoS Pathogens, 5, e1000353.
Naseri, M., Niazi, A., Bagherzadeh, K., Konoz, E. & Samadikhah, H.R. (2023) Modified electrochemical aptasensor for ultrasensitive detection of tetracycline: in silico and in vitro studies. Food Chemistry, 421, 136195.
Parker, S.L., Pandey, S., Sime, F.B., Lipman, J., Roberts, J.A. & Wallis, S.C. (2019) A validated LC-MSMS method for the simultaneous quantification of meropenem and vaborbactam in human plasma and renal replacement therapy effluent and its application to a pharmacokinetic study. Analytical and Bioanalytical Chemistry, 411, 7831-7840.
Pfaffl, M.W. (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Research, 29, e45.
Preston, D.A., Wu, C.Y.E., Blaszczak, L.C., Seitz, D.E. & Halligan, N.G. (1990) Biological characterization of a new radioactive labeling reagent for bacterial penicillin-binding proteins. Antimicrobial Agents and Chemotherapy, 34, 718-721.
Rodríguez-González, L., Núñez-Delgado, A., Álvarez-Rodríguez, E., García-Campos, E., Martín, Á., Díaz-Raviña, M. et al. (2022) Effects of ciprofloxacin, trimethoprim, and amoxicillin on microbial structure and growth as emerging pollutants reaching crop soils. Environmental Research, 214, 113916.
Ruppé, É., Woerther, P.L. & Barbier, F. (2015) Mechanisms of antimicrobial resistance in gram-negative bacilli. Annals of Intensive Care, 5, 1-15.
Sanders, C.C., Bradford, P.A., Ehrhardt, A.F., Bush, K., Young, K.D., Henderson, T.A. et al. (1997) Penicillin-binding proteins and induction of AmpC beta-lactamase. Antimicrobial Agents and Chemotherapy, 41, 2013-2015.
Schmidt, H., Korfmann, G., Barth, H. & Martin, H.H. (1995) The signal transducer encoded by ampG is essential for induction of chromosomal AmpC p-lactamase in Escherichia coli by β-lactam antibiotics and “unspecific” inducers. Microbiology, 141, 1085-1092.
Schmidtke, A.J. & Hanson, N.D. (2006) Model system to evaluate the effect of ampD mutations on AmpC-mediated β-lactam resistance. Antimicrobial Agents and Chemotherapy, 50, 2030-2037.
Sharafati-Chaleshtori, R., Mardani, G., Rafieian-Kopaei, M., Sharafati-Chaleshtori, A. & Drees, F. (2013) Residues of oxytetracycline in cultured rainbow trout. Pakistan Journal of Biological Sciences, 16, 1419-1422.
Torrens, G., Hernández, S.B., Ayala, J.A., Moya, B., Juan, C., Cava, F. et al. (2019) Regulation of AmpC-driven β-lactam resistance in Pseudomonas aeruginosa: different pathways, different signaling. mSystems, 4, 10-1128.
Vadlamani, G., Thomas, M.D., Patel, T.R., Donald, L.J., Reeve, T.M., Stetefeld, J. et al. (2015) The β-lactamase gene regulator AmpR is a tetramer that recognizes and binds the D-Ala-D-Ala motif of its repressor UDP-N-acetylmuramic acid (MurNAc)-pentapeptide. The Journal of Biological Chemistry, 290, 2630-2643.
Valtonen, S.J., Kurittu, J.S. & Karp, M.T. (2002) A luminescent Escherichia coli biosensor for the high throughput detection of beta-lactams. Journal of Biomolecular Screening, 7, 127-134.
Vásquez-Ponce, F., Higuera-Llantén, S., Pavlov, M.S., Marshall, S.H. & Olivares-Pacheco, J. (2018) Phylogenetic MLSA and phenotypic analysis identification of three probable novel Pseudomonas species isolated on King George Island, south Shetland, Antarctica. Brazilian Journal of Microbiology, 49, 695-702.
Vásquez-Ponce, F., Higuera-Llantén, S., Pavlov, M.S., Ramírez-Orellana, R., Marshall, S.H. & Olivares-Pacheco, J. (2017) Alginate overproduction and biofilm formation by psychrotolerant Pseudomonas mandelii depend on temperature in Antarctic marine sediments. Electronic Journal of Biotechnology, 28, 27-34.
Vollmer, W. & Höltje, J.V. (2001) Morphogenesis of Escherichia coli. Current Opinion in Microbiology, 4, 625-633.
Xiao, F., Li, G., Wu, Y., Chen, Q., Wu, Z. & Yu, R. (2016) Label-free photonic crystal-based β-lactamase biosensor for β-lactam antibiotic and β-lactamase inhibitor. Analytical Chemistry, 88, 9207-9212.
Yang, S., Li, C., Zhan, H., Liu, R., Chen, W., Wang, X. et al. (2023) A label-free fluorescent biosensor based on specific aptamer-templated silver nanoclusters for the detection of tetracycline. Journal of Nanobiotechnology, 21, 22.