Selection of Potential Therapeutic Bacteriophages that Lyse a CTX-M-15 Extended Spectrum β-Lactamase Producing Salmonella enterica Serovar Typhi Strain from the Democratic Republic of the Congo
Abstract
:Author Contributions
Conflicts of Interest
Funding
References
- Karkey, A.; Thwaites, G.E.; Baker, S. The evolution of antimicrobial resistance in Salmonella Typhi. Curr. Opin. Gastroenterol. 2018, 34, 25–30. [Google Scholar] [CrossRef] [PubMed]
- Marks, F.; von Kalckreuth, V.; Aaby, P.; Adu-Sarkodie, Y.; El Tayeb, M.A.; Ali, M.; Aseffa, A.; Baker, S.; Biggs, H.M.; Bjerregaard-Andersen, M.; et al. Incidence of invasive Salmonella disease in sub-Saharan Africa: A multicentre population-based surveillance study. Lancet Glob. Health 2017, 5, e310–e323. [Google Scholar] [CrossRef]
- Tacconelli, E.; Carrara, E.; Savoldi, A.; Harbarth, S.; Mendelson, M.; Monnet, D.L.; Pulcini, C.; Kahlmeter, G.; Kluytmans, J.; Carmeli, Y.; et al. Discovery, research, and development of new antibiotics: The WHO priority list of antibiotic-resistant bacteria and tuberculosis. Lancet Infect. Dis. 2017, 18, 234–236. [Google Scholar] [CrossRef]
- Tackling Drug-Resistant Infections Globally: Final Report and Recommendations. The Review on Antimicrobial Resistance. 2016. Available online: https://amr-review.org/sites/default/files/160525_Final paper_with cover.pdf (accessed on 27 January 2018).
- United Nations. Draft Political Declaration of the High-Level Meeting of the General Assembly on Antimicrobial Resistance (16-16108 (E)). Available online: http://www.un.org/pga/71/wp-content/uploads/sites/40/2016/09/DGACM_GAEAD_ESCAB-AMR-Draft-Political-Declaration-1616108E.pdf (accessed on 17 December 2017).
- Watts, G. Phage therapy: Revival of the bygone antimicrobial. Lancet 2017, 390, 2539–2540. [Google Scholar] [CrossRef]
- Chanishvili, N. Bacteriophages as Therapeutic and Prophylactic Means: Summary of the Soviet and Post Soviet Experiences. Curr. Drug Deliv. 2016, 13, 309–323. [Google Scholar] [CrossRef] [PubMed]
- Nagel, T.E.; Chan, B.K.; de Vos, D.; El-Shibiny, A.; Kang’ethe, E.K.; Makumi, A.; Pirnay, J.P. The Developing World Urgently Needs Phages to Combat Pathogenic Bacteria. Front. Microbiol. 2016, 7, 882. [Google Scholar] [CrossRef] [PubMed]
- Phoba, M.F.; Barbé, B.; Lunguya, O.; Masendu, L.; Lulengwa, D.; Dougan, G.; Wong, V.K.; Bertrand, S.; Ceyssens, P.J.; Jacobs, J.; et al. Salmonella enterica serovar Typhi Producing CTX-M-15 Extended Spectrum β-Lactamase in the Democratic Republic of the Congo. Clin. Infect. Dis. 2017, 65, 1229–1231. [Google Scholar] [CrossRef] [PubMed]
- Bonnet, R. Growing group of extended-spectrum β-lactamases: The CTX-M enzymes. Antimicrob. Agents Chemother. 2004, 48, 1–14. [Google Scholar] [CrossRef] [PubMed]
- Ho, T.D.; Figueroa-Bossi, N.; Wang, M.; Uzzau, S.; Bossi, L.; Slauch, J.M. Identification of GtgE, a novel virulence factor encoded on the Gifsy-2 bacteriophage of Salmonella enterica serovar Typhimurium. J. Bacteriol. 2002, 184, 5234–5239. [Google Scholar] [CrossRef] [PubMed]
- Deamer, D.W.; Akeson, M. Nanopores and nucleic acids: Prospects for ultrarapid sequencing. Trends Biotechnol. 2000, 18, 147–150. [Google Scholar] [CrossRef]
- Koren, S.; Walenz, B.P.; Berlin, K.; Miller, J.R.; Bergman, N.H.; Phillippy, A.M. Canu: Scalable and accurate long-read assembly via adaptive K-mer weighting and repeat separation. Genome Res. 2017, 27, 722–736. [Google Scholar] [CrossRef] [PubMed]
- Vaser, R.; Sović, I.; Nagarajan, N.; Šikić, M. Fast and accurate de novo genome assembly from long uncorrected reads. Genome Res. 2017, 27, 737–746. [Google Scholar] [CrossRef] [PubMed]
- Coordinators, N.R. Database resources of the national center for biotechnology information. Nucleic Acids Res. 2016, 44, D7. [Google Scholar]
- Ondov, B.D.; Treangen, T.J.; Melsted, P.; Mallonee, A.B.; Bergman, N.H.; Koren, S.; Phillippy, A.M. Mash: Fast genome and metagenome distance estimation using MinHash. Genome Biol. 2016, 17, 132. [Google Scholar] [CrossRef] [PubMed]
- R Core Team. R: A Language and Environment for Statistical Computing; R Foundation for Statistical Computing: Vienna, Austria, 2015; Available online: https://www.R-project.org/ (accessed on 24 March 2018).
- Ackermann, H.W. Basic phage electron microscopy. In Bacteriophages: Methods and Protocols, 1st ed.; Clokie, M.R.J., Kropinski, A., Eds.; Humana Press: New York, NY, USA, 2009; Volume 1, pp. 113–126. ISBN 978-1-58829-682-5. [Google Scholar]
- Kutter, E. Phage host range and efficiency of plating. In Bacteriophages: Methods and Protocols, 1st ed.; Clokie, M.R.J., Kropinski, A., Eds.; Humana Press: New York, NY, USA, 2009; Volume 1, pp. 141–149. ISBN 978-1-58829-682-5. [Google Scholar]
- Matsuzaki, S.; Uchiyama, J.; Takemura-Uchiyama, I.; Ujihara, T.; Daibata, M. Isolation of Bacteriophages for Fastidious Bacteria. In Bacteriophage Therapy, 1st ed.; Azeredo, J., Sillankorva, S., Eds.; Humana Press: New York, NY, USA, 2018; pp. 3–10. ISBN 978-1-4939-7394-1. [Google Scholar]
- Gratia, A. Des relations numeriques entre bacteries lysogenes et particules de bacteriophage. Ann. Inst. Pasteur 1936, 57, 652–676. [Google Scholar]
- Appelmans, R. Le dosage du bactériophage. C. R. Seances Soc. Biol. 1921, 85, 1098. [Google Scholar]
- Labrie, S.J.; Samson, J.E.; Moineau, S. Bacteriophage resistance mechanisms. Nat. Rev. Microbiol. 2010, 8, 317–327. [Google Scholar] [CrossRef] [PubMed]
- Hall, A.R.; de Vos, D.; Friman, V.P.; Pirnay, J.P.; Buckling, A. Effects of sequential and simultaneous applications of bacteriophages on populations of Pseudomonas aeruginosa in vitro and in wax moth larvae. Appl. Environ. Microbiol. 2012, 78, 5646–5652. [Google Scholar] [CrossRef] [PubMed]
- Kamal, F.; Dennis, J.J. Burkholderia cepacia complex Phage-Antibiotic Synergy (PAS): Antibiotics stimulate lytic phage activity. Appl. Environ. Microbiol. 2015, 81, 1132–1138. [Google Scholar] [CrossRef] [PubMed]
- Merabishvili, M.; Vervaet, C.; Pirnay, J.P.; De Vos, D.; Verbeken, G.; Mast, J.; Chanishvili, N.; Vaneechoutte, M. Stability of Staphylococcus aureus phage ISP after freeze-drying (lyophilization). PLoS ONE 2013, 8, e68797. [Google Scholar] [CrossRef] [PubMed] [Green Version]
Nr | Name | GenBank Accession Numbers | Source | Isolation Year | Host Strain | Family | Homology to Other Phages | Host Range (%) *All Serovars/S. Enteritidis/S. Typhimurium/S. Dublin (Total Number of Tested Isolates) | Lytic Activity on the Typhi 10040_15_DRC_2015 Isolate | |||||||
---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
Streak Method | Spot Test | Gratia’s Method | Appelmans’ Method | |||||||||||||
Titer (pfu/mL) | Dilution | 6 h | 18 h | 24 h | ||||||||||||
001 | GE_vB_N3 | ND | Mtkvari river water | 2013 | S. Enteritidis 3 | Siphoviridae | ND | 78/98/73/87 (239) | + | + | + | 109 | −1 | − | − | + |
108 | −2 | − | − | + | ||||||||||||
107 | −3 | − | + | + | ||||||||||||
002 | GE_vB_N5 | MG969412 | Mtkvari river water | 2013 | S. Enteritidis 3 | Siphoviridae | E. coli T5 strain ATCC 11303-B5 | 45/80/25/74 (239) | + | + | + | 108 | −1 | − | + | + |
107 | −2 | − | + | + | ||||||||||||
106 | −3 | − | + | + | ||||||||||||
003 | GE_vB_N8 | MG969413 | Mtkvari river water | 2013 | S. Enteritidis 3 | Siphoviridae | phage SPC35 | 65/84/67/78 (239) | + | + | − | 109 | −1 | − | − | + |
108 | −2 | − | − | + | ||||||||||||
107 | −3 | − | + | + | ||||||||||||
004 | GE_vB_MG | MG969411 | Tbilisi sewage water | 2013 | S. Enteritidis 3 | Myoviridae | S. phage PVP-SE1 | 47/49/59/43 (239) | − | − | + | 109 | −1 | − | − | − |
108 | −2 | − | − | − | ||||||||||||
107 | −3 | − | − | − | ||||||||||||
005 | GE_vB_BS | MG969407 | Black Sea water | 2013 | S. Typhimurium 4 | Myoviridae | S SPT-1, partial genome | 81/96/93/83 (239) | + | + | + | 1010 | −1 | + | − | − |
109 | −2 | + | − | − | ||||||||||||
108 | −3 | + | − | − | ||||||||||||
006 | GE_vB_B1 | MG969405 | Mtkvari river water | 2013 | S. Typhimurium 6 | Myoviridae | S. phage Mushroom | 80/93/83/87 (239) | + | + | + | 109 | −1 | + | − | − |
108 | −2 | + | − | − | ||||||||||||
107 | −3 | + | − | − | ||||||||||||
007 | GE_vB_B3 | MG969406 | Mtkvari river water | 2013 | S. Typhimurium 6 | Myoviridae | S. phage Mushroom | 81/98/73/87 (239) | + | + | + | 109 | −1 | + | − | − |
108 | −2 | + | − | − | ||||||||||||
107 | −3 | + | − | − | ||||||||||||
008 | GE_vB_NS7 | MG969414 | Raw cow milk | 2015 | S. Typhimurium 6 | Myoviridae | S. phage Mushroom | 75/91/81/78 (239) | + | + | + | 109 | −1 | + | − | − |
108 | −2 | − | + | − | ||||||||||||
107 | −3 | − | + | + | ||||||||||||
009 | GE_vB_M4 | MG969409 | Black Sea water | 2016 | S. Enteritidis 232 | Siphoviridae | S. phage vB_SenS-Ent3 | 23/64/18/22 (218) | + | + | + | 1010 | −1 | + | − | − |
109 | −2 | + | − | − | ||||||||||||
108 | −3 | − | − | − | ||||||||||||
010 | GE_vB_M5 | MG969410 | Black Sea water | 2016 | S. Enteritidis 407 | Siphoviridae | S. phage vB_SenS-Ent3 | 33/66/26/61 (218) | + | + | + | 108 | −1 | + | − | − |
107 | −2 | + | − | − | ||||||||||||
106 | −3 | + | − | − | ||||||||||||
011 | GE_vB_TR | MG969415 | Mtkvari river water | 2017 | S. Typhimurium 641 | Podoviridae | S. phage BTP1 | 40/90/28/59 (141) | − | − | + | 109 | −1 | − | − | − |
108 | −2 | − | − | − | ||||||||||||
107 | −3 | − | − | − | ||||||||||||
012 | GE_vB_HIL | MG969408 | Mtkvari river water | 2017 | S. Enteritidis 765 | Siphoviridae | S. phage vB_SenS-Ent3 | 58/81/75/77 (141) | + | + | − | 1010 | −1 | + | − | − |
109 | −2 | − | − | − | ||||||||||||
108 | −3 | − | + | + | ||||||||||||
013 | GE_vB_7A | MG969404 | Mtkvari river water | 2017 | S. Typhimurium 1328 | Myoviridae | S. phage BPS15Q2 | 37/62/28/23 (141) | + | + | + | 108 | −1 | − | − | − |
107 | −2 | − | − | − | ||||||||||||
106 | −3 | − | − | − | ||||||||||||
014 | GE_vB_M1 | ND | Black Sea water | 2016 | S. Enteritidis 104 | Podoviridae | ND | 12/20/19/0 (77) | + | + | − | 109 | −1 | − | − | − |
108 | −2 | − | − | − | ||||||||||||
107 | −3 | − | − | − |
© 2018 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/).
Share and Cite
Kakabadze, E.; Makalatia, K.; Grdzelishvili, N.; Bakuradze, N.; Goderdzishvili, M.; Kusradze, I.; Phoba, M.-F.; Lunguya, O.; Lood, C.; Lavigne, R.; et al. Selection of Potential Therapeutic Bacteriophages that Lyse a CTX-M-15 Extended Spectrum β-Lactamase Producing Salmonella enterica Serovar Typhi Strain from the Democratic Republic of the Congo. Viruses 2018, 10, 172. https://doi.org/10.3390/v10040172
Kakabadze E, Makalatia K, Grdzelishvili N, Bakuradze N, Goderdzishvili M, Kusradze I, Phoba M-F, Lunguya O, Lood C, Lavigne R, et al. Selection of Potential Therapeutic Bacteriophages that Lyse a CTX-M-15 Extended Spectrum β-Lactamase Producing Salmonella enterica Serovar Typhi Strain from the Democratic Republic of the Congo. Viruses. 2018; 10(4):172. https://doi.org/10.3390/v10040172
Chicago/Turabian StyleKakabadze, Elene, Khatuna Makalatia, Nino Grdzelishvili, Nata Bakuradze, Marina Goderdzishvili, Ia Kusradze, Marie-France Phoba, Octavie Lunguya, Cédric Lood, Rob Lavigne, and et al. 2018. "Selection of Potential Therapeutic Bacteriophages that Lyse a CTX-M-15 Extended Spectrum β-Lactamase Producing Salmonella enterica Serovar Typhi Strain from the Democratic Republic of the Congo" Viruses 10, no. 4: 172. https://doi.org/10.3390/v10040172
APA StyleKakabadze, E., Makalatia, K., Grdzelishvili, N., Bakuradze, N., Goderdzishvili, M., Kusradze, I., Phoba, M. -F., Lunguya, O., Lood, C., Lavigne, R., Jacobs, J., Deborggraeve, S., De Block, T., Van Puyvelde, S., Lee, D., Coffey, A., Sedrakyan, A., Soentjens, P., De Vos, D., ... Chanishvili, N. (2018). Selection of Potential Therapeutic Bacteriophages that Lyse a CTX-M-15 Extended Spectrum β-Lactamase Producing Salmonella enterica Serovar Typhi Strain from the Democratic Republic of the Congo. Viruses, 10(4), 172. https://doi.org/10.3390/v10040172