Antibiotic Susceptibility, Resistance Gene Determinants and Corresponding Genomic Regions in Lactobacillus amylovorus Isolates Derived from Wild Boars and Domestic Pigs

. 2022 Dec 30 ; 11 (1) : . [epub] 20221230

Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid36677394

Grantová podpora
QK1910351 Ministry of Agriculture of the Czech Republic
MZE-RO0518 Ministry of Agriculture of the Czech Republic
MZE-RO0318 Ministry of Agriculture of the Czech Republic

Odkazy

PubMed 36677394
PubMed Central PMC9863647
DOI 10.3390/microorganisms11010103
PII: microorganisms11010103
Knihovny.cz E-zdroje

Restrictions on the use of antibiotics in pigs lead to the continuous search for new probiotics serving as an alternative to antibiotics. One of the key parameters for probiotic bacteria selection is the absence of horizontally transmissible resistance genes. The aim of our study was to determine antibiotic susceptibility profiles in 28 Lactobacillus amylovorus isolates derived from the digestive tract of wild boars and farm pigs by means of the broth microdilution method and whole genome sequencing (WGS). We revealed genetic resistance determinants and examined sequences flanking resistance genes in these strains. Our findings indicate that L. amylovorus strains from domestic pigs are predominantly resistant to tetracycline, erythromycin and ampicillin. WGS analysis of horizontally transmissible genes revealed only three genetic determinants (tetW, ermB and aadE) of which all tetW and ermB genes were present only in strains derived from domestic pigs. Sequence analysis of coding sequences (CDS) in the neighborhood of the tetW gene revealed the presence of site-specific recombinase (xerC/D), site-specific DNA recombinase (spoIVCA) or DNA-binding transcriptional regulator (xre), usually directly downstream of the tetW gene. In the case of ermB, CDS for omega transcriptional repressor or mobilization protein were detected upstream of the ermB gene.

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ECDC. EFSA. EMA Third Joint Inter-agency Report on Integrated Analysis of Consumption of Antimicrobial Agents and Occurrence of Antimicrobial Resistance in Bacteria from Humans and Food-producing Animals in the EU/EEA. EFSA J. 2021;19:e06712. doi: 10.2903/j.efsa.2021.6712. PubMed DOI PMC

Lekagul A., Tangcharoensathien V., Yeung S. Patterns of Antibiotic Use in Global Pig Production: A Systematic Review. Vet. Anim. Sci. 2019;7:100058. doi: 10.1016/j.vas.2019.100058. PubMed DOI PMC

Van Gompel L., Luiken R.E.C., Sarrazin S., Munk P., Knudsen B.E., Hansen R.B., Bossers A., Aarestrup F.M., Dewulf J., Wagenaar J.A., et al. The Antimicrobial Resistome in Relation to Antimicrobial Use and Biosecurity in Pig Farming, a Metagenome-Wide Association Study in Nine European Countries. J. Antimicrob. Chemother. 2019;74:865–876. doi: 10.1093/jac/dky518. PubMed DOI

Gerzova L., Babak V., Sedlar K., Faldynova M., Videnska P., Cejkova D., Jensen A.N., Denis M., Kerouanton A., Ricci A., et al. Characterization of Antibiotic Resistance Gene Abundance and Microbiota Composition in Feces of Organic and Conventional Pigs from Four EU Countries. PLoS ONE. 2015;10:e0132892. doi: 10.1371/journal.pone.0132892. PubMed DOI PMC

Dowarah R., Verma A.K., Agarwal N., Singh P., Singh B.R. Selection and Characterization of Probiotic Lactic Acid Bacteria and Its Impact on Growth, Nutrient Digestibility, Health and Antioxidant Status in Weaned Piglets. PLoS ONE. 2018;13:e0192978. doi: 10.1371/journal.pone.0192978. PubMed DOI PMC

Rychen G., Aquilina G., Azimonti G., Bampidis V., Bastos M.D.L., Bories G., Chesson A., Cocconcelli P.S., Flachowsky G., Gropp J., et al. Guidance on the Characterisation of Microorganisms Used as Feed Additives or as Production Organisms. EFSA J. 2018;16:e05206. doi: 10.2903/J.EFSA.2018.5206. PubMed DOI PMC

Lebeer S., Bron P.A., Marco M.L., van Pijkeren J.P., O’Connell Motherway M., Hill C., Pot B., Roos S., Klaenhammer T. Identification of Probiotic Effector Molecules: Present State and Future Perspectives. Curr. Opin. Biotechnol. 2018;49:217–223. doi: 10.1016/j.copbio.2017.10.007. PubMed DOI

Campedelli I., Mathur H., Salvetti E., Clarke S., Rea M.C., Torriani S., Ross R.P., Hill C., O’Toole P.W. Genus-Wide Assessment of Antibiotic Resistance in Lactobacillus spp. Appl. Environ. Microbiol. 2019;85:e01738-18. doi: 10.1128/AEM.01738-18. PubMed DOI PMC

Thumu S.C.R., Halami P.M. Conjugal Transfer of Erm(B) and Multiple Tet Genes from Lactobacillus spp. to Bacterial Pathogens in Animal Gut, in Vitro and during Food Fermentation. Food Res. Int. 2019;116:1066–1075. doi: 10.1016/j.foodres.2018.09.046. PubMed DOI

Dec M., Urban-Chmiel R., Stępień-Pyśniak D., Wernicki A. Assessment of Antibiotic Susceptibility in Lactobacillus Isolates from Chickens. Gut Pathog. 2017;9:54. doi: 10.1186/s13099-017-0203-z. PubMed DOI PMC

Devirgiliis C., Zinno P., Perozzi G., Roberts M.C. Update on Antibiotic Resistance in Foodborne Lactobacillus and Lactococcus Species. Front. Microbiol. 2013;4:301. doi: 10.3389/fmicb.2013.00301. PubMed DOI PMC

Juricova H., Matiasovicova J., Kubasova T., Cejkova D., Rychlik I. The Distribution of Antibiotic Resistance Genes in Chicken Gut Microbiota Commensals. Sci. Rep. 2021;11:3290. doi: 10.1038/s41598-021-82640-3. PubMed DOI PMC

Shen J., Zhang J., Zhao Y., Lin Z., Ji L., Ma X. Tibetan Pig-Derived Probiotic Lactobacillus amylovorus SLZX20-1 Improved Intestinal Function via Producing Enzymes and Regulating Intestinal Microflora. Front. Nutr. 2022;9:846991. doi: 10.3389/fnut.2022.846991. PubMed DOI PMC

Fujisawa T., Benno Y., Yaeshima T., Mitsuoka T. Taxonomic Study of the Lactobacillus acidophilus Group, with Recognition of Lactobacillus gallinarum Sp. Nov. and Lactobacillus johnsonii Sp. Nov. and Synonymy of Lactobacillus acidophilus Group A3 (Johnson et al. 1980) with the Type Strain of Lactobacill. Int. J. Syst. Evol. Microbiol. 1992;42:487–491. doi: 10.1099/00207713-42-3-487. PubMed DOI

Zheng J., Wittouck S., Salvetti E., Franz C.M.A.P., Harris H.M.B., Mattarelli P., O’toole P.W., Pot B., Vandamme P., Walter J., et al. A Taxonomic Note on the Genus Lactobacillus: Description of 23 Novel Genera, Emended Description of the Genus Lactobacillus beijerinck 1901, and Union of Lactobacillaceae and Leuconostocaceae. Int. J. Syst. Evol. Microbiol. 2020;70:2782–2858. doi: 10.1099/ijsem.0.004107. PubMed DOI

Lagacé L., Pitre M., Jacqeus M., Roy D. Identification of the Bacterial Community of Maple Sap by Using Amplified Ribosomal DNA (RDNA) Restriction Analysis and RDNA Sequencing. Appl. Environ. Microbiol. 2004;70:2052–2060. doi: 10.1128/AEM.70.4.2052-2060.2004. PubMed DOI PMC

Ewels P., Magnusson M., Lundin S., Käller M. MultiQC: Summarize Analysis Results for Multiple Tools and Samples in a Single Report. Bioinformatics. 2016;32:3047–3048. doi: 10.1093/bioinformatics/btw354. PubMed DOI PMC

Wick R.R., Judd L.M., Gorrie C.L., Holt K.E. Unicycler: Resolving Bacterial Genome Assemblies from Short and Long Sequencing Reads. PLoS Comput. Biol. 2017;13:e1005595. doi: 10.1371/journal.pcbi.1005595. PubMed DOI PMC

Nurk S., Meleshko D., Korobeynikov A., Pevzner P.A. MetaSPAdes: A New Versatile Metagenomic Assembler. Genome Res. 2017;27:824–834. doi: 10.1101/gr.213959.116. PubMed DOI PMC

Jain C., Rodriguez-R L.M., Phillippy A.M., Konstantinidis K.T., Aluru S. High Throughput ANI Analysis of 90K Prokaryotic Genomes Reveals Clear Species Boundaries. Nat. Commun. 2018;9:5114. doi: 10.1038/s41467-018-07641-9. PubMed DOI PMC

Seemann T. Prokka: Rapid Prokaryotic Genome Annotation. Bioinformatics. 2014;30:2068–2069. doi: 10.1093/bioinformatics/btu153. PubMed DOI

Huerta-Cepas J., Szklarczyk D., Heller D., Hernández-Plaza A., Forslund S.K., Cook H., Mende D.R., Letunic I., Rattei T., Jensen L.J., et al. EggNOG 5.0: A Hierarchical, Functionally and Phylogenetically Annotated Orthology Resource Based on 5090 Organisms and 2502 Viruses. Nucleic Acids Res. 2019;47:D309–D314. doi: 10.1093/nar/gky1085. PubMed DOI PMC

Buchfink B., Reuter K., Drost H.G. Sensitive Protein Alignments at Tree-of-Life Scale Using DIAMOND. Nat. Methods. 2021;18:366–368. doi: 10.1038/s41592-021-01101-x. PubMed DOI PMC

Page A.J., Cummins C.A., Hunt M., Wong V.K., Reuter S., Holden M.T.G., Fookes M., Falush D., Keane J.A., Parkhill J. Roary: Rapid Large-Scale Prokaryote Pan Genome Analysis. Bioinformatics. 2015;31:3691–3693. doi: 10.1093/bioinformatics/btv421. PubMed DOI PMC

Jia B., Raphenya A.R., Alcock B., Waglechner N., Guo P., Tsang K.K., Lago B.A., Dave B.M., Pereira S., Sharma A.N., et al. CARD 2017: Expansion and Model-Centric Curation of the Comprehensive Antibiotic Resistance Database. Nucleic Acids Res. 2017;45:D566–D573. doi: 10.1093/nar/gkw1004. PubMed DOI PMC

Zankari E., Hasman H., Cosentino S., Vestergaard M., Rasmussen S., Lund O., Aarestrup F.M., Larsen M.V. Identification of Acquired Antimicrobial Resistance Genes. J. Antimicrob. Chemother. 2012;67:2640–2644. doi: 10.1093/jac/dks261. PubMed DOI PMC

Gupta S.K., Padmanabhan B.R., Diene S.M., Lopez-Rojas R., Kempf M., Landraud L., Rolain J.M. ARG-Annot, a New Bioinformatic Tool to Discover Antibiotic Resistance Genes in Bacterial Genomes. Antimicrob. Agents Chemother. 2014;58:212–220. doi: 10.1128/AAC.01310-13. PubMed DOI PMC

Doster E., Lakin S.M., Dean C.J., Wolfe C., Young J.G., Boucher C., Belk K.E., Noyes N.R., Morley P.S. MEGARes 2.0: A Database for Classification of Antimicrobial Drug, Biocide and Metal Resistance Determinants in Metagenomic Sequence Data. Nucleic Acids Res. 2020;48:D561–D569. doi: 10.1093/nar/gkz1010. PubMed DOI PMC

Feldgarden M., Brover V., Haft D.H., Prasad A.B., Slotta D.J., Tolstoy I., Tyson G.H., Zhao S., Hsu C.H., McDermott P.F., et al. Validating the AMRFINder Tool and Resistance Gene Database by Using Antimicrobial Resistance Genotype-Phenotype Correlations in a Collection of Isolates. Antimicrob. Agents Chemother. 2019;63:e00483-19. doi: 10.1128/AAC.00483-19. PubMed DOI PMC

Carver T., Harris S.R., Berriman M., Parkhill J., McQuillan J.A. Artemis: An Integrated Platform for Visualization and Analysis of High-Throughput Sequence-Based Experimental Data. Bioinformatics. 2012;28:464–469. doi: 10.1093/bioinformatics/btr703. PubMed DOI PMC

Sullivan M.J., Petty N.K., Beatson S.A. Easyfig: A Genome Comparison Visualizer. Bioinformatics. 2011;27:1009–1010. doi: 10.1093/bioinformatics/btr039. PubMed DOI PMC

Madeira F., Pearce M., Tivey A.R.N., Basutkar P., Lee J., Edbali O., Madhusoodanan N., Kolesnikov A., Lopez R. Search and Sequence Analysis Tools Services from EMBL-EBI in 2022. Nucleic Acids Res. 2022;50:W276–W279. doi: 10.1093/nar/gkac240. PubMed DOI PMC

Arndt D., Grant J.R., Marcu A., Sajed T., Pon A., Liang Y., Wishart D.S. PHASTER: A Better, Faster Version of the PHAST Phage Search Tool. Nucleic Acids Res. 2016;44:W16–W21. doi: 10.1093/nar/gkw387. PubMed DOI PMC

Kumar S., Stecher G., Li M., Knyaz C., Tamura K. MEGA X: Molecular Evolutionary Genetics Analysis across Computing Platforms. Mol. Biol. Evol. 2018;35:1547–1549. doi: 10.1093/molbev/msy096. PubMed DOI PMC

Camacho C., Coulouris G., Avagyan V., Ma N., Papadopoulos J., Bealer K., Madden T.L. BLAST+: Architecture and Applications. BMC Bioinform. 2009;10:421. doi: 10.1186/1471-2105-10-421. PubMed DOI PMC

Tamura K. Estimation of the Number of Nucleotide Substitutions When There Are Strong Transition-Transversion and G+C-Content Biases. Mol. Biol. Evol. 1992;9:678–687. doi: 10.1093/oxfordjournals.molbev.a040752. PubMed DOI

Carattoli A., Zankari E., Garciá-Fernández A., Larsen M.V., Lund O., Villa L., Aarestrup F.M., Hasman H. In Silico Detection and Typing of Plasmids Using Plasmidfinder and Plasmid Multilocus Sequence Typing. Antimicrob. Agents Chemother. 2014;58:3895–3903. doi: 10.1128/AAC.02412-14. PubMed DOI PMC

Schwengers O., Barth P., Falgenhauer L., Hain T., Chakraborty T., Goesmann A. Platon: Identification and Characterization of Bacterial Plasmid Contigs in Short-Read Draft Assemblies Exploiting Protein Sequence-Based Replicon Distribution Scores. Microb. Genom. 2020;6:mgen000398. doi: 10.1099/mgen.0.000398. PubMed DOI PMC

Wang N., Hang X., Zhang M., Liu X., Yang H. Analysis of Newly Detected Tetracycline Resistance Genes and Their Flanking Sequences in Human Intestinal Bifidobacteria. Sci. Rep. 2017;7:6267. doi: 10.1038/s41598-017-06595-0. PubMed DOI PMC

Skarzynska M., Leekitcharoenphon P., Hendriksen R.S., Aarestrup F.M., Wasyl D. A Metagenomic Glimpse into the Gut of Wild and Domestic Animals: Quantification of Antimicrobial Resistance and More. PLoS ONE. 2020;15:e0242987. doi: 10.1371/journal.pone.0242987. PubMed DOI PMC

Takahashi Y., Nakashima T. Actinomycetes, an Inexhaustible Source of Naturally Occurring Antibiotics. Antibiotics. 2018;7:45. doi: 10.3390/antibiotics7020045. PubMed DOI PMC

European Committee on Antimicrobial Susceptibility Testing Breakpoint Tables for Interpretation of MICs and Zone Diameters. Version 12.0. 2022. [(accessed on 1 October 2022)]. Available online: https://www.eucast.org/clinical_breakpoints.

Jiang X., Yu T., Zhou D., Ji S., Zhou C., Shi L., Wang X. Characterization of Quinolone Resistance Mechanisms in Lactic Acid Bacteria Isolated from Yogurts in China. Ann. Microbiol. 2016;66:1249–1256. doi: 10.1007/s13213-016-1214-6. DOI

European Medicines Agency Sales of Veterinary Antimicrobial Agents in 31 European Countries in 2019 and 2020. 2021. [(accessed on 1 October 2022)]. Available online: https://op.europa.eu/en/publication-detail/-/publication/d20a0041-83db-11ec-8c40-01aa75ed71a1/language-en.

WHO . Critically Important Antimicrobials for Human Medicine, 6th Revision. WHO; Geneva, Switzerland: 2019.

Chang Y.C., Tsai C.Y., Lin C.F., Wang Y.C., Wang I.K., Chung T.C. Characterization of Tetracycline Resistance Lactobacilli Isolated from Swine Intestines at Western Area of Taiwan. Anaerobe. 2011;17:239–245. doi: 10.1016/j.anaerobe.2011.08.001. PubMed DOI

Holmer I., Salomonsen C.M., Jorsal S.E., Astrup L.B., Jensen V.F., Høg B.B., Pedersen K. Antibiotic Resistance in Porcine Pathogenic Bacteria and Relation to Antibiotic Usage. BMC Vet. Res. 2019;15:449. doi: 10.1186/s12917-019-2162-8. PubMed DOI PMC

Zou X., Weng M., Ji X., Guo R., Zheng W., Yao W. Comparison of Antibiotic Resistance and Copper Tolerance of Enterococcus spp. and Lactobacillus spp. Isolated from Piglets before and after Weaning. J. Microbiol. 2017;55:703–710. doi: 10.1007/s12275-017-6241-x. PubMed DOI

Villedieu A., Diaz-Torres M.L., Hunt N., McNab R., Spratt D.A., Wilson M., Mullany P. Prevalence of Tetracycline Resistance Genes in Oral Bacteria. Antimicrob. Agents Chemother. 2003;47:878–882. doi: 10.1128/AAC.47.3.878-882.2003. PubMed DOI PMC

Sullivan B.A., Gentry T., Karthikeyan R. Characterization of Tetracycline-Resistant Bacteria in an Urbanizing Subtropical Watershed. J. Appl. Microbiol. 2013;115:774–785. doi: 10.1111/jam.12283. PubMed DOI

Tsuchida S., Maruyama F., Ogura Y., Toyoda A., Hayashi T., Okuma M., Ushida K. Genomic Characteristics of Bifidobacterium thermacidophilum Pig Isolates and Wild Boar Isolates Reveal the Unique Presence of a Putative Mobile Genetic Element with TetW for Pig Farm Isolates. Front. Microbiol. 2017;8:1540. doi: 10.3389/fmicb.2017.01540. PubMed DOI PMC

Wickramage I., Spigaglia P., Sun X. Mechanisms of Antibiotic Resistance of Clostridioides Difficile. J. Antimicrob. Chemother. 2021;76:3077–3090. doi: 10.1093/jac/dkab231. PubMed DOI PMC

Kartalidis P., Skoulakis A., Tsilipounidaki K., Florou Z., Petinaki Ε., Fthenakis G.C. Clostridioides Difficile as a Dynamic Vehicle for the Dissemination of Antimicrobial-Resistance Determinants: Review and in Silico Analysis. Microorganisms. 2021;9:1383. doi: 10.3390/microorganisms9071383. PubMed DOI PMC

Nawaz M., Wang J., Zhou A., Ma C., Wu X., Moore J.E., Cherie Millar B., Xu J. Characterization and Transfer of Antibiotic Resistance in Lactic Acid Bacteria from Fermented Food Products. Curr. Microbiol. 2011;62:1081–1089. doi: 10.1007/s00284-010-9856-2. PubMed DOI

Midonet C., Barre F.-X. Xer Site-Specific Recombination: Promoting Vertical and Horizontal Transmission of Genetic Information. Microbiol. Spectr. 2014;2 doi: 10.1128/microbiolspec.MDNA3-0056-2014. PubMed DOI

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