The Combination of Salmonella Phage ST-3 and Antibiotics to Prevent Salmonella Typhimurium In Vitro.


Journal

Current microbiology
ISSN: 1432-0991
Titre abrégé: Curr Microbiol
Pays: United States
ID NLM: 7808448

Informations de publication

Date de publication:
21 Oct 2022
Historique:
received: 13 01 2021
accepted: 03 10 2022
entrez: 21 10 2022
pubmed: 22 10 2022
medline: 26 10 2022
Statut: epublish

Résumé

The novel phage ST-3, capable of infecting the foodborne pathogen Salmonella Typhimurium, was isolated from wastewater. The Biological characters and genome information of ST-3 were analyzed. In the in vitro assay, the phage ST-3 with a MOI of 10 effectively inhibited the growth of Salmonella Typhimurium CGMCC 1.1174 in 6 h. The inhibitory effect of combination phage ST-3 and antibiotics was also studied, the removal rate of planktonic host exposed to ST-3 and levofloxacin hydrochloride at the same time, or to ciprofloxacin followed by ST-3, is higher than that exposed to antibiotic dosing group alone and antibiotic + phage dosing group. The phage ST-3 combined with 0.5 µg/mL levofloxacin hydrochloride resulted in the largest decrease in biofilm biomass at 54%. The phage ST-3 could be a potential agent to control Salmonella Typhimurium growth and provide instruction for use it and antibiotics together.

Identifiants

pubmed: 36269452
doi: 10.1007/s00284-022-03073-3
pii: 10.1007/s00284-022-03073-3
doi:

Substances chimiques

Anti-Bacterial Agents 0
Levofloxacin 6GNT3Y5LMF
Waste Water 0
Ciprofloxacin 5E8K9I0O4U

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

371

Subventions

Organisme : Fundamental Research Funds for Central Universities of the Central South University
ID : E1E40506
Organisme : National Key Laboratory of Science, Technology on Advanced Composites in Special Environments, HIT
ID : GYY-DTFZ-2022-008

Informations de copyright

© 2022. The Author(s), under exclusive licence to Springer Science+Business Media, LLC, part of Springer Nature.

Références

Laxminarayan R, Duse A, Wattal C, Zaidi AKM, Wertheim HFL, Sumpradit N et al (2013) Antibiotic resistance—the need for global solutions. Lancet Infect Dis 13:1057–1098. https://doi.org/10.1016/S1473-3099(13)70318-9
doi: 10.1016/S1473-3099(13)70318-9 pubmed: 24252483
Rohwer F (2003) Global phage diversity. Cell 113:141. https://doi.org/10.1016/s0092-8674(03)00276-9
doi: 10.1016/s0092-8674(03)00276-9 pubmed: 12705861
Liu H, Xiong Y, Liu X, Li J (2018) Complete genome sequence of a novel virulent phage ST31 infecting Escherichia coli H21. Arch Virol. https://doi.org/10.1007/s00705-018-3812-z
doi: 10.1007/s00705-018-3812-z pubmed: 30564896 pmcid: 6394704
Schooley RT, Biswas B, Gill JJ, Hernandez-Morales A, Lancaster J, Lessor L et al (2018) Development and use of personalized bacteriophage-based therapeutic cocktails to treat a patient with a disseminated resistant Acinetobacter baumannii infection. Antimicrob Agents Chemother. https://doi.org/10.1128/AAC.00954-17
doi: 10.1128/AAC.00954-17 pubmed: 30478181 pmcid: 6256779
Dedrick RM, Guerrero-Bustamante CA, Garlena RA, Russell DA, Ford K, Harris K et al (2019) Engineered bacteriophages for treatment of a patient with a disseminated drug-resistant Mycobacterium abscessus. Nat Med 25:730–733. https://doi.org/10.1038/s41591-019-0437-z
doi: 10.1038/s41591-019-0437-z pubmed: 31068712 pmcid: 6557439
Sulakvelidze A (2013) Using lytic bacteriophages to eliminate or significantly reduce contamination of food by foodborne bacterial pathogens. J Sci Food Agric 93:3137–3146. https://doi.org/10.1002/jsfa.6222
doi: 10.1002/jsfa.6222 pubmed: 23670852
Guenther S, Huwyler D, Richard S, Loessner MJ (2009) Virulent bacteriophage for efficient biocontrol of Listeria monocytogenes in ready-to-eat foods. Appl Environ Microbiol 75:93–100. https://doi.org/10.1128/AEM.01711-08
doi: 10.1128/AEM.01711-08 pubmed: 19011076
Jo A, Ding T, Ahn J (2016) Synergistic antimicrobial activity of bacteriophages and antibiotics against Staphylococcus aureus. Food Sci Biotechnol 25:935–940. https://doi.org/10.1007/s10068-016-0153-0
doi: 10.1007/s10068-016-0153-0 pubmed: 30263357 pmcid: 6049171
Easwaran M, Paudel S, De Zoysa M, Shin HJ (2015) Functional characterization of a novel lytic phage EcSw isolated from Sus scrofa domesticus and its potential for phage therapy. Mol Cell Probes. https://doi.org/10.1016/j.mcp.2015.03.004
doi: 10.1016/j.mcp.2015.03.004 pubmed: 25805216
Oechslin F, Piccardi P, Mancini S, Gabard J, Moreillon P, Entenza JM et al (2016) Synergistic interaction between phage therapy and antibiotics clears pseudomonas aeruginosa infection in endocarditis and reduces virulence. J Infect Dis. https://doi.org/10.1093/infdis/jiw632
doi: 10.1093/infdis/jiw632 pmcid: 5388299
Adzitey F, Huda N, Ali GRR (2012) Prevalence and antibiotic resistance of Campylobacter, Salmonella, and L. monocytogenes in ducks: a review. Foodborne Pathog Dis 9(6):498–505. https://doi.org/10.1089/fpd.2011.1109
doi: 10.1089/fpd.2011.1109 pubmed: 22571641
Espié E, De Valk H, Vaillant V, Quelquejeu N, Le Querrec F et al (2004) An outbreak of multidrug-resistant salmonella enterica serotype newport infections linked to the consumption of imported horse meat in France. Epidemiol Infect. https://doi.org/10.1017/s0950268804003449
doi: 10.1017/s0950268804003449
Voetsch AC, Van GTJ, Angulo FJ, Farley MM, Sue S, Ruthanne M et al (2004) Foodnet estimate of the burden of illness caused by nontyphoidal Salmonella infections in the United States. Clin Infect Dis 38(Supplement_3):S127. https://doi.org/10.1086/381578
doi: 10.1086/381578 pubmed: 15095181
Merino L, Procura F, Trejo FM, Bueno DJ, Golowczyc MA (2019) Biofilm formation by Salmonella sp. in the poultry industry: detection, control and eradication strategies. Food Res Int 119:530–540. https://doi.org/10.1016/j.foodres.2017.11.024
doi: 10.1016/j.foodres.2017.11.024 pubmed: 30884686
Fauvart M, De Grootet VN, Michiels JV (2011) Role of persister cells in chronic infections: clinical relevance and perspectives on anti-persister therapies. J Med Microbiol 60:699–709. https://doi.org/10.1099/jmm.0.030932-0
doi: 10.1099/jmm.0.030932-0 pubmed: 21459912
Clavijo V, Baquero D, Hernandez S, Farfan JC, Vives-Flores M (2019) Phage cocktail Salmofree® reduces Salmonella on a commercial broiler farm. Poul Sci. https://doi.org/10.3382/ps/pez251
doi: 10.3382/ps/pez251
Sambrook J, Russell DW (2006) Purification of RNA from cells and tissues by acid phenol–guanidinium thiocyanate–chloroform extraction. Cold Sring Harb Protoc. 2006(1):149–150. https://doi.org/10.1101/pdb.prot4045
doi: 10.1101/pdb.prot4045
Zrelovs N, Cernooka E, Dislers A, Kazaks A (2019) Isolation and characterization of the novel Virgibacillus-infecting bacteriophage Mimir87. Arch Virol. https://doi.org/10.1007/s00705-019-04516-2
doi: 10.1007/s00705-019-04516-2 pubmed: 31875246
Moineau S, Pandian S, Klaenhammer TR (1994) Evolution of a lytic bacteriophage via DNA acquistition from the Lactococcus-Lactis chromosome. Appl Environ Microbiol 60:1832–1841. https://doi.org/10.1128/aem.60.6.1832-1841.1994
doi: 10.1128/aem.60.6.1832-1841.1994 pubmed: 16349277 pmcid: 201570
Casey E, Mahony J, Neve H, Noben J-P, Dal Bello F, van Sinderen D (2015) Novel phage group infecting Lactobacillus delbrueckii subsp lactis, as revealed by genomic and proteomic analysis of bacteriophage Ldl1. Appl Environ Microbiol 81:1319–1326. https://doi.org/10.1128/AEM.03413-14
doi: 10.1128/AEM.03413-14 pubmed: 25501478 pmcid: 4309708
Arndt D, Grant JR, Marcu A, Sajed T, Pon A, Liang Y et al (2016) PHASTER: a better, faster version of the PHAST phage search tool. Nucleic Acids Res 44:W16–W21. https://doi.org/10.1093/nar/gkw387
doi: 10.1093/nar/gkw387 pubmed: 27141966 pmcid: 4987931
Gasteiger E, Gattiker A, Hoogland C, Ivanyi I, Appel RD, Bairoch A (2003) ExPASy: the proteomics server for in-depth protein knowledge and analysis. Nucleic Acids Res 31:3784–3788. https://doi.org/10.1093/nar/gkg563
doi: 10.1093/nar/gkg563 pubmed: 12824418 pmcid: 168970
Liu B, Zheng D, Jin Q, Chen L, Yang J (2019) VFDB 2019: a comparative pathogenomic platform with an interactive web interface. Nucleic Acids Res 47:D687–D692. https://doi.org/10.1093/nar/gky1080
doi: 10.1093/nar/gky1080 pubmed: 30395255
Zankari E, Hasman H, Cosentino S, Vestergaard M, Rasmussen S, Lund O et al (2012) Identification of acquired antimicrobial resistance genes. J Antimicrob Chemother 67:2640–2644. https://doi.org/10.1093/jac/dks261
doi: 10.1093/jac/dks261 pubmed: 22782487 pmcid: 3468078
Lowe TM, Chan PP (2016) tRNAscan-SE On-line: integrating search and context for analysis of transfer RNA genes. Nucleic Acids Res 44:W54–W57. https://doi.org/10.1093/jac/dks261
doi: 10.1093/jac/dks261 pubmed: 27174935 pmcid: 4987944
Adzhubei IA, Schmidt S, Peshkin L, Ramensky VE, Gerasimova A, Bork P et al (2010) A method and server for predicting damaging missense mutations. Nat Methods 7:248–249. https://doi.org/10.1038/nmeth0410-248
doi: 10.1038/nmeth0410-248 pubmed: 20354512 pmcid: 2855889
Darling AE, Mau B, Perna NT (2010) progressiveMauve: multiple genome alignment with gene gain, loss and rearrangement. PLoS ONE. https://doi.org/10.1371/journal.pone.0011147
doi: 10.1371/journal.pone.0011147 pubmed: 20593022 pmcid: 2892488
Clinical and Laboratory Standards Institute (2006) Methods for dilution antimicrobial susceptibility tests for bacteria that grow aerobically, 7th edn. Clinical and Laboratory Standards Institute, Wayne
Bailly-Bechet M, Vergassola M, Rocha E (2007) Causes for the intriguing presence of tRNAs in phages. Genome Res 17:1486–1495. https://doi.org/10.1101/gr.6649807
doi: 10.1101/gr.6649807 pubmed: 17785533 pmcid: 1987346
Lehman SM, Kropinski AM, Castle AJ, Svircev AM (2009) Complete genome of the broad-host-range Erwinia amylovora phage phiEa21-4 and its relationship to Salmonella phage felix O1. Appl Environ Microbiol 75:2139–2147. https://doi.org/10.1128/AEM.02352-08
doi: 10.1128/AEM.02352-08 pubmed: 19181832 pmcid: 2663227
Fong K, Tremblay DM, Delaquis P, Goodridge L, Levesque RC, Moineau S et al (2019) Diversity and host specificity revealed by biological characterization and whole genome sequencing of bacteriophages infecting Salmonella enterica. Viruses-Basel. https://doi.org/10.3390/v11090854
doi: 10.3390/v11090854
Lu M, Liu H, Lu H, Liu R, Liu X (2020) Characterization and genome analysis of a novel Salmonella phage vB_SenS_SE1. Curr Microbiol. https://doi.org/10.1007/s00284-020-01879-7
doi: 10.1007/s00284-020-01879-7 pubmed: 32970172 pmcid: 7485193
Kang HW, Kim JW, Jung TS, Woo GJ (2013) wksl3, a new biocontrol agent for Salmonella enterica Serovars Enteritidis and Typhimurium in foods: characterization, application, sequence analysis, and oral acute toxicity study. Appl Environ Microbiol 79:1956–1968. https://doi.org/10.1128/AEM.02793-12
doi: 10.1128/AEM.02793-12 pubmed: 23335772 pmcid: 3592225
Hsieh SE, Lo HH, Chen ST, Lee MC, Tseng YH (2011) Wide host range and strong lytic activity of Staphylococcus aureus lytic phage Stau2. Appl Environ Microbiol 77:756–761. https://doi.org/10.1128/AEM.01848-10
doi: 10.1128/AEM.01848-10 pubmed: 21148689
Imklin N, Nasanit R (2020) Characterization of Salmonella bacteriophages and their potential use in dishwashing materials. J Appl Microbiol. https://doi.org/10.1111/jam.14617
doi: 10.1111/jam.14617 pubmed: 32073713
Hall AR, De Vos D, Friman VP, Pirnay JP, Buckling A (2012) Effects of sequential and simultaneous applications of bacteriophages on populations of Pseudomonas aeruginosa in Vitro and in wax moth larvae. Appl Environ Microbiol 78:5646–5652. https://doi.org/10.1128/AEM.00757-12
doi: 10.1128/AEM.00757-12 pubmed: 22660719 pmcid: 3406105
Chan BK, Sistrom M, Wertz JE, Kortright KE, Narayan D, Turner PE (2016) Phage selection restores antibiotic sensitivity in MDR Pseudomonas aeruginosa. Sci Rep. https://doi.org/10.1038/srep26717
doi: 10.1038/srep26717 pubmed: 28442790 pmcid: 5431345
Escobar-Paramo P, Gougat-Barbera C, Hochberg ME (2012) Evolutionary dynamics of separate and combined exposure of Pseudomonas fluorescens SBW25 to antibiotics and bacteriophage. Evol Appl 5:583–592. https://doi.org/10.1111/j.1752-4571.2012.00248.x
doi: 10.1111/j.1752-4571.2012.00248.x pubmed: 23028399 pmcid: 3461141
Torres-Barcelo C, Arias-Sanchez FI, Vasse M, Ramsayer J, Kaltz O, Hochberg ME (2014) A window of opportunity to control the bacterial pathogen Pseudomonas aeruginosa combining antibiotics and phages. PLoS ONE. https://doi.org/10.1371/JOURNAL.PONE.0106628
doi: 10.1371/JOURNAL.PONE.0106628 pubmed: 25259735 pmcid: 4178015
Kim M, Jo Y, Hwang YJ, Hong HW, Hong SS, Park K, Myung H (2018) Phage-antibiotic synergy via delayed lysis. Appl Environ Microbiol. https://doi.org/10.1128/AEM.02085-18
doi: 10.1128/AEM.02085-18 pubmed: 30377199 pmcid: 6275337
Kumaran D, Taha M, Yi Q, Ramirez-Arcos S, Diallo JS, Carli A et al (2018) Does treatment order matter? Investigating the ability of bacteriophage to augment antibiotic activity against Staphylococcus aureus biofilms. Front Microbiol. https://doi.org/10.3389/fmicb.2018.00127
doi: 10.3389/fmicb.2018.00127 pubmed: 29459853 pmcid: 5807357
Pamp SJ, Sternberg C, Tolker-Nielsen T (2009) Insight into the microbial multicellular lifestyle via flow-cell technology and confocal microscopy. Cytom Part A 75A:90–103. https://doi.org/10.1002/cyto.a.20685
doi: 10.1002/cyto.a.20685
Sillankorva S, Azeredo J (2014) The use of bacteriophages and bacteriophage-derived enzymes for clinically relevant biofilm control. Phage Therapy: Current Research and Applications. Caister Academic Press, Wymondham
Garcia KC, de Oliveira Corrêa IM, Pereira LQ, Silva TM, Mioni MD, de Moraes Izidoro AC et al (2017) Bacteriophage use to control Salmonella biofilm on surfaces present in chicken slaughterhouses. Poult Sci 96:3392–3398. https://doi.org/10.3382/ps/pex124
doi: 10.3382/ps/pex124
Andersson S, Dalhammar G, Rajarao GK (2011) Influence of microbial interactions and EPS/polysaccharide composition on nutrient removal activity in biofilms formed by strains found in wastewater treatment systems. Microbiol Res 166:449–457. https://doi.org/10.1016/j.micres.2010.08.005
doi: 10.1016/j.micres.2010.08.005 pubmed: 20869860
Liu B, Lu H, Li Z, Yan P, Liu R, Liu X (2022) Expression and biological activity of lytic proteins HolST-3 and LysST-3 of Salmonella phage ST-3. Microb Pathog 169:105624. https://doi.org/10.1016/j.micpath.2022.105624
doi: 10.1016/j.micpath.2022.105624 pubmed: 35697172

Auteurs

Min Lu (M)

College of Resources and Environment, University of Chinese Academy of Sciences, Beijing, 101408, China.

Bingxin Liu (B)

College of Resources and Environment, University of Chinese Academy of Sciences, Beijing, 101408, China.

Wenbin Xiong (W)

College of Resources and Environment, University of Chinese Academy of Sciences, Beijing, 101408, China.

Xinchun Liu (X)

College of Resources and Environment, University of Chinese Academy of Sciences, Beijing, 101408, China. xcliu@ucas.ac.cn.

Articles similaires

Vancomycin-associated DRESS demonstrates delay in AST abnormalities.

Ahmed Hussein, Kateri L Schoettinger, Jourdan Hydol-Smith et al.
1.00
Humans Drug Hypersensitivity Syndrome Vancomycin Female Male
Humans Arthroplasty, Replacement, Elbow Prosthesis-Related Infections Debridement Anti-Bacterial Agents
Genome, Viral Ralstonia Composting Solanum lycopersicum Bacteriophages
Vancomycin Polyesters Anti-Bacterial Agents Models, Theoretical Drug Liberation

Classifications MeSH