Comprehensive Metagenomic Analysis of Veterinary Probiotics in Broiler Chickens
Open accessAbstract
Probiotics are widely used in broiler chickens to support the gut microbiome, gut health, and to reduce the amount of antibiotics used. Despite their benefits, there is concern over their ability to carry and spread antimicrobial resistance genes (ARGs), posing a significant public health risk. This study utilized next-generation sequencing to investigate ARGs in probiotics approved for poultry, focusing on their potential to be transferred via mobile genetic elements such as plasmids and phages. We examined the gut microbiome and resistome changes in 60 broiler chickens over their rearing period, correlating these changes with different probiotic treatments. Specific resistance mechanisms against critically important antibiotics were identified, including genes related to fluoroquinolone resistance and peptide antibiotic resistance. We also found genes with significant relevance to public health (aadK, AAC(6′)-Ii) and multiple drug-resistance genes (vmlR, ykkC, ykkD, msrC, clbA, eatAv). Only one phage-encoded gene (dfrA43) was detected, with no evidence of plasmid or mobile genetic element transmission. Additionally, metagenomic analysis of fecal samples showed no significant changes corresponding to time or diet across groups. Our findings highlight the potential risks associated with the use of probiotics in poultry, particularly regarding the carriage of ARGs. It is crucial to conduct further research into the molecular genetics of probiotics to develop strategies that mitigate the risk of resistance gene transfer in agriculture, ensuring the safe and effective use of probiotics in animal husbandry.
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Probiotic products and probiotic-associated taxa may carry detectable ARGs, but public-health relevance depends on taxon identity, gene function, genomic context and mobility potential rather than on ARG counts alone.
“previous studies have shown that probiotic products and probiotic-associated taxa may carry detectable ARGs, but that public-health relevance depends on taxon identity, gene function, genomic context and mobility potential rather than on ARG counts alone [15,16,17,18,22,23].”
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Cites
The rise of the Enterococcus: beyond vancomycin resistance
Arias, C. A., & Murray, B. E. (2012) · Nature Reviews Microbiology · doi:10.1038/nrmicro2761 · Cited by 1,776 · see citing works
(FEEDAP), E. P. O. A. A. P. O. S. U. I. A. F. (2012) · EFSA Journal · doi:10.2903/j.efsa.2012.2740 · Cited by 904 · see citing works
Charteris, Kelly, Morelli, & Collins (1998) · Journal of Applied Microbiology · doi:10.1046/j.1365-2672.1998.00407.x · Cited by 774 · see citing works
Saccharomyces cerevisiae Fungemia: An Emerging Infectious Disease
Munoz, P., Bouza, E., Cuenca-Estrella, M., Eiros, J. M., Perez, M. J., Sanchez-Somolinos, M., Rincon, C., Hortal, J., & Pelaez, T. (2005) · Clinical Infectious Diseases · doi:10.1086/429916 · Cited by 462 · see citing works
Role of commercial probiotic strains against human pathogen adhesion to intestinal mucus
Collado, M. C., Meriluoto, J., & Salminen, S. (2007) · Letters in Applied Microbiology · doi:10.1111/j.1472-765x.2007.02212.x · Cited by 303 · see citing works
Assessing the Risk of Probiotic Dietary Supplements in the Context of Antibiotic Resistance
Zheng, M., Zhang, R., Tian, X., Zhou, X., Pan, X., & Wong, A. (2017) · Frontiers in Microbiology · doi:10.3389/fmicb.2017.00908 · Cited by 218 · see citing works
Flagged first, then by citations
Research works printed but not linked: 84
- [1]Hill C. Guarner F. Reid G. Gibson G.R. Merenstein D.J. Pot B. Morelli L. Canani R.B. Flint H.J. Salminen S. The International Scientific Association for Probiotics and Prebiotics Consensus Statement on the Scope and Appropriate Use of the Term Probiotic Nat. Rev. Gastroenterol. Hepatol. 2014 11 506 514 10.1038/nrgastro.2014.66 24912386 · DOI
- [2]Macpherson A.J. Uhr T. Induction of Protective IgA by Intestinal Dendritic Cells Carrying Commensal Bacteria Science 2004 303 1662 1665 10.1126/science.1091334 15016999 · DOI · Paper page
- [3]Matsuo K. Ota H. Akamatsu T. Sugiyama A. Katsuyama T. Histochemistry of the Surface Mucous Gel Layer of the Human Colon Gut 1997 40 782 789 10.1136/gut.40.6.782 9245933 PMC1027204 · DOI
- [5]Mack D.R. Extracellular MUC3 Mucin Secretion Follows Adherence of Lactobacillus Strains to Intestinal Epithelial Cells in Vitro Gut 2003 52 827 833 10.1136/gut.52.6.827 12740338 PMC1773687 · DOI
- [6]Asahara T. Shimizu K. Nomoto K. Hamabata T. Ozawa A. Takeda Y. Probiotic Bifidobacteria Protect Mice from Lethal Infection with Shiga Toxin-Producing Escherichia Coli O157:H7 Infect. Immun. 2004 72 2240 2247 10.1128/IAI.72.4.2240-2247.2004 15039348 PMC375161 · DOI
- [7]Maqueda M. Sánchez-Hidalgo M. Fernández M. Montalbán-López M. Valdivia E. Martínez-Bueno M. Genetic Features of Circular Bacteriocins Produced by Gram-Positive Bacteria FEMS Microbiol. Rev. 2008 32 2 22 10.1111/j.1574-6976.2007.00087.x 18034824 · DOI
- [13]Kerek Á. Csanády P. Tuska-Szalay B. Kovács L. Jerzsele Á. In Vitro Efficacy of Hungarian Propolis against Bacteria, Yeast, and Trichomonas Gallinae Isolated from Pigeons—A Possible Antibiotic Alternative? Resources 2023 12 101 10.3390/resources12090101 · DOI
- [14]Fredenucci I. Chomarat M. Boucaud C. Flandrois J.P. Saccharomyces Boulardii Fungemia in a Patient Receiving Ultra-Levure Therapy Clin. Infect. Dis. 1998 27 222 223 10.1086/517685 9675488 · DOI
- [15]Henry S. D’Hondt L. André M. Holemans X. Canon J.L. Saccharomyces Cerevisiae Fungemia in a Head and Neck Cancer Patient: A Case Report and Review of the Literature Acta Clin. Belg. 2004 59 220 222 10.1179/acb.2004.032 15597729 · DOI
- [16]Lolis N. Veldekis D. Moraitou H. Kanavaki S. Velegraki A. Triandafyllidis C. Tasioudis C. Pefanis A. Pneumatikos I. Saccharomyces Boulardii Fungaemia in an Intensive Care Unit Patient Treated with Caspofungin Crit. Care 2008 12 414 10.1186/cc6843 18423057 PMC2447580 · DOI
- [18]Niault M. Thomas F. Prost J. Ansari F.H. Kalfon P. Fungemia Due to Saccharomyces Species in a Patient Treated with Enteral Saccharomyces Boulardii Clin. Infect. Dis. 1999 28 930 10.1086/517255 10825077 · DOI
- [19]Land M.H. Rouster-Stevens K. Woods C.R. Cannon M.L. Cnota J. Shetty A.K. Lactobacillus Sepsis Associated with Probiotic Therapy Pediatrics 2005 115 178 181 10.1542/peds.2004-2137 15629999 · DOI · Paper page
- [20]Oggioni M.R. Pozzi G. Valensin P.E. Galieni P. Bigazzi C. Recurrent Septicemia in an Immunocompromised Patient Due to Probiotic Strains of Bacillus Subtilis J. Clin. Microbiol. 1998 36 325 326 10.1128/JCM.36.1.325-326.1998 9431982 PMC124869 · DOI
- [21]Ohishi A. Takahashi S. Ito Y. Ohishi Y. Tsukamoto K. Nanba Y. Ito N. Kakiuchi S. Saitoh A. Morotomi M. Bifidobacterium Septicemia Associated with Postoperative Probiotic Therapy in a Neonate with Omphalocele J. Pediatr. 2010 156 679 681 10.1016/j.jpeds.2009.11.041 20303445 · DOI
- [22]Zein E.F. Karaa S. Chemaly A. Saidi I. Daou-Chahine W. Rohban R. Lactobacillus rhamnosus septicemia in a diabetic patient associated with probiotic use: A case report Ann. Biol. Clin. 2008 66 195 198 10.1684/abc.2008.0210 18390430 · DOI
- [23]Vaarala O. Immunological Effects of Probiotics with Special Reference to Lactobacilli Clin. Exp. Allergy 2003 33 1634 1640 10.1111/j.1365-2222.2003.01835.x 14656348 · DOI
- [24]Veckman V. Miettinen M. Pirhonen J. Sirén J. Matikainen S. Julkunen I. Streptococcus Pyogenes and Lactobacillus Rhamnosus Differentially Induce Maturation and Production of Th1-Type Cytokines and Chemokines in Human Monocyte-Derived Dendritic Cells J. Leukoc. Biol. 2004 75 764 771 10.1189/jlb.1003461 14966192 · DOI
- [25]Rijkers G.T. de Vos W.M. Brummer R.-J. Morelli L. Corthier G. Marteau P. Health Benefits and Health Claims of Probiotics: Bridging Science and Marketing Br. J. Nutr. 2011 106 1291 1296 10.1017/S000711451100287X 21861940 · DOI
- [26]Sniffen J.C. McFarland L.V. Evans C.T. Goldstein E.J.C. Choosing an Appropriate Probiotic Product for Your Patient: An Evidence-Based Practical Guide PLoS ONE 2018 13 e0209205 10.1371/journal.pone.0209205 30586435 PMC6306248 · DOI · Paper page
- [27]Hempel S. Newberry S. Ruelaz A. Wang Z. Miles J.N.V. Suttorp M.J. Johnsen B. Shanman R. Slusser W. Fu N. Safety of Probiotics Used to Reduce Risk and Prevent or Treat Disease Evid. Rep. Technol. Assess. (Full Rep.) 2011 200 1 645 PMC4780970 23126627
- [28]Harbarth S. Balkhy H.H. Goossens H. Jarlier V. Kluytmans J. Laxminarayan R. Saam M. Van Belkum A. Pittet D. for the World Healthcare-Associated Infections Resistance Forum participants Antimicrobial Resistance: One World, One Fight! Antimicrob. Resist. Infect. Control 2015 4 49 10.1186/s13756-015-0091-2 · DOI
- [29]Baquero F. Threats of Antibiotic Resistance: An Obliged Reappraisal Int. Microbiol. 2021 24 499 506 10.1007/s10123-021-00184-y 34028624 PMC8141826 · DOI
- [30]Van Boeckel T.P. Gandra S. Ashok A. Caudron Q. Grenfell B.T. Levin S.A. Laxminarayan R. Global Antibiotic Consumption 2000 to 2010: An Analysis of National Pharmaceutical Sales Data Lancet Infect Dis 2014 14 742 750 10.1016/S1473-3099(14)70780-7 25022435 · DOI
- [32]Sanders M.E. Akkermans L.M.A. Haller D. Hammerman C. Heimbach J. Hörmannsperger G. Huys G. Levy D.D. Lutgendorff F. Mack D. Safety Assessment of Probiotics for Human Use Gut Microbes 2010 1 164 185 10.4161/gmic.1.3.12127 21327023 PMC3023597 · DOI · Paper page
- [33]Vankerckhoven V. Huys G. Vancanneyt M. Vael C. Klare I. Romond M.-B. Entenza J.M. Moreillon P. Wind R.D. Knol J. Biosafety Assessment of Probiotics Used for Human Consumption: Recommendations from the EU-PROSAFE Project Trends Food Sci. Technol. 2008 19 102 114 10.1016/j.tifs.2007.07.013 · DOI
- [34]Kastner S. Perreten V. Bleuler H. Hugenschmidt G. Lacroix C. Meile L. Antibiotic Susceptibility Patterns and Resistance Genes of Starter Cultures and Probiotic Bacteria Used in Food Syst. Appl. Microbiol. 2006 29 145 155 10.1016/j.syapm.2005.07.009 16464696 · DOI
- [35]Huys G. D’Haene K. Swings J. Genetic Basis of Tetracycline and Minocycline Resistance in Potentially Probiotic Lactobacillus Plantarum Strain CCUG 43738 Antimicrob. Agents Chemother. 2006 50 1550 1551 10.1128/AAC.50.4.1550-1551.2006 16569881 PMC1426919 · DOI
- [36]Xing S.-C. Chen J.-Y. Cai Y.-F. Huang C.-B. Liao X.-D. Mi J.-D. Bacillus Coagulans R11 Consumption Influenced the Abundances of Cecum Antibiotic Resistance Genes in Lead-Exposed Laying Hens Environ. Pollut. 2021 274 116562 10.1016/j.envpol.2021.116562 33545525 · DOI
- [37]Zavišić G. Popović M. Stojkov S. Medić D. Gusman V. Jovanović Lješković N. Jovanović Galović A. Antibiotic Resistance and Probiotics: Knowledge Gaps, Market Overview and Preliminary Screening Antibiotics 2023 12 1281 10.3390/antibiotics12081281 37627701 PMC10451169 · DOI
- [38]Merenstein D. Pot B. Leyer G. Ouwehand A.C. Preidis G.A. Elkins C.A. Hill C. Lewis Z.T. Shane A.L. Zmora N. Emerging Issues in Probiotic Safety: 2023 Perspectives Gut Microbes 2023 15 2185034 10.1080/19490976.2023.2185034 36919522 PMC10026873 · DOI · Paper page
- [39]Gareau M.G. Sherman P.M. Walker W.A. Probiotics and the Gut Microbiota in Intestinal Health and Disease Nat. Rev. Gastroenterol. Hepatol. 2010 7 503 514 10.1038/nrgastro.2010.117 20664519 PMC4748966 · DOI · Paper page
- [41]Arias C.A. Contreras G.A. Murray B.E. Management of Multidrug-Resistant Enterococcal Infections Clin. Microbiol. Infect. 2010 16 555 562 10.1111/j.1469-0691.2010.03214.x 20569266 PMC3686902 · DOI
- [43]Gao W. Howden B.P. Stinear T.P. Evolution of Virulence in Enterococcus Faecium, a Hospital-Adapted Opportunistic Pathogen Curr. Opin. Microbiol. 2018 41 76 82 10.1016/j.mib.2017.11.030 29227922 · DOI
- [44]Doron S. Snydman D.R. Risk and Safety of Probiotics Clin. Infect. Dis. 2015 60 S129 S134 10.1093/cid/civ085 25922398 PMC4490230 · DOI · Paper page
- [45]Huang Y.-F. Liu P.-Y. Chen Y.-Y. Nong B.-R. Huang I.-F. Hsieh K.-S. Chen K.-T. Three-Combination Probiotics Therapy in Children With Salmonella and Rotavirus Gastroenteritis J. Clin. Gastroenterol. 2014 48 37 42 10.1097/MCG.0b013e31828f1c6e 23632352 · DOI
- [46]Poloni V. Salvato L. Pereyra C. Oliveira A. Rosa C. Cavaglieri L. Keller K.M. Bakery By-Products Based Feeds Borne-Saccharomyces Cerevisiae Strains with Probiotic and Antimycotoxin Effects plus Antibiotic Resistance Properties for Use in Animal Production Food Chem. Toxicol. 2017 107 630 636 10.1016/j.fct.2017.02.040 28259658 · DOI
- [48]Charteris W.P. Kelly P.M. Morelli L. Collins J.K. Gradient Diffusion Antibiotic Susceptibility Testing of Potentially Probiotic Lactobacilli J. Food Prot. 2001 64 2007 2014 10.4315/0362-028X-64.12.2007 11770631 · DOI
- [49]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 10.1007/s00284-010-9856-2 21212956 · DOI · Paper page
- [50]Belletti N. Gatti M. Bottari B. Neviani E. Tabanelli G. Gardini F. Antibiotic Resistance of Lactobacilli Isolated from Two Italian Hard Cheeses J. Food Prot. 2009 72 2162 2169 10.4315/0362-028X-72.10.2162 19833040 · DOI
- [51]Chen Y.-C. Yu Y.-H. Bacillus Licheniformis-Fermented Products and Enramycin Differentially Modulate Microbiota and Antibiotic Resistome in the Cecal Digesta of Broilers Poult. Sci. 2022 101 102010 10.1016/j.psj.2022.102010 35841645 PMC9293667 · DOI
- [52]Wang Y. Hu Y. Liu F. Cao J. Lv N. Zhu B. Zhang G. Gao G.F. Integrated Metagenomic and Metatranscriptomic Profiling Reveals Differentially Expressed Resistomes in Human, Chicken, and Pig Gut Microbiomes Environ. Int. 2020 138 105649 10.1016/j.envint.2020.105649 32200314 · DOI
- [56]Sahin-Tóth J. Kovács E. Tóthpál A. Juhász J. Forró B. Bányai K. Havril K. Horváth A. Ghidán Á. Dobay O. Whole Genome Sequencing of Coagulase Positive Staphylococci from a Dog-and-Owner Screening Survey PLoS ONE 2021 16 e0245351 10.1371/journal.pone.0245351 33428679 PMC7799803 · DOI
- [57]Modi A. Vai S. Caramelli D. Lari M. The Illumina Sequencing Protocol and the NovaSeq 6000 System Methods Mol. Biol. 2021 2242 15 42 10.1007/978-1-0716-1099-2_2 33961215 · DOI
- [58]Muzzey D. Evans E.A. Lieber C. Understanding the Basics of NGS: From Mechanism to Variant Calling Curr. Genet. Med. Rep. 2015 3 158 165 10.1007/s40142-015-0076-8 26566462 PMC4633438 · DOI
- [59]Mihály Z. Győrffy B. Következő generációs szekvenálási technológiák kifejlődése és alkalmazásai = Next generation sequencing technologies (NGST) development and applications Orvosi Hetil. 2011 152 55 62 10.1556/OH.2011.29007 21177232 · DOI
- [61]Chen S. Zhou Y. Chen Y. Gu J. Fastp: An Ultra-Fast All-in-One FASTQ Preprocessor Bioinformatics 2018 34 i884 i890 10.1093/bioinformatics/bty560 30423086 PMC6129281 · DOI
- [62]Benoit G. Lavenier D. Lemaitre C. Rizk G. Bloocoo, a Memory Efficient Read Corrector Proceedings of the European Conference on Computational Biology (ECCB) Strasbourg, France 7 September 2014
- [64]Dinghua MEGAHIT: An Ultra-Fast Single-Node Solution for Large and Complex Metagenomics Assembly via Succinct de Bruijn Graph. Bioinformatics. Oxford Academic Available online: https://academic.oup.com/bioinformatics/article/31/10/1674/177884 (accessed on 25 April 2022) 25609793
- [65]Vicedomini R. Vezzi F. Scalabrin S. Arvestad L. Policriti A. GAM-NGS: Genomic Assemblies Merger for next Generation Sequencing BMC Bioinform. 2013 14 (Suppl. S7) S6 10.1186/1471-2105-14-S7-S6 PMC3633056 23815503 · DOI
- [66]Gurevich A. Saveliev V. Vyahhi N. Tesler G. QUAST: Quality Assessment Tool for Genome Assemblies Bioinformatics 2013 29 1072 1075 10.1093/bioinformatics/btt086 23422339 PMC3624806 · DOI · Paper page
- [67]Langmead B. Salzberg S.L. Fast Gapped-Read Alignment with Bowtie 2 Nat. Methods 2012 9 357 359 10.1038/nmeth.1923 22388286 PMC3322381 · DOI · Paper page
- [68]Wood D.E. Lu J. Langmead B. Improved Metagenomic Analysis with Kraken 2 Genome Biol. 2019 20 257 10.1186/s13059-019-1891-0 31779668 PMC6883579 · DOI
- [69]Pruitt K.D. Tatusova T. Maglott D.R. NCBI Reference Sequences (RefSeq): A Curated Non-Redundant Sequence Database of Genomes, Transcripts and Proteins Nucleic Acids Res. 2007 35 D61 D65 10.1093/nar/gkl842 17130148 PMC1716718 · DOI
- [70]McMurdie P.J. Holmes S. Phyloseq: An R Package for Reproducible Interactive Analysis and Graphics of Microbiome Census Data PLoS ONE 2013 8 e61217 10.1371/journal.pone.0061217 23630581 PMC3632530 · DOI
- [72]Nurk S. Meleshko D. Korobeynikov A. Pevzner P.A. MetaSPAdes: A New Versatile Metagenomic Assembler Genome Res. 2017 27 824 834 10.1101/gr.213959.116 28298430 PMC5411777 · DOI · Paper page
- [73]Hyatt D. Chen G.-L. Locascio P.F. Land M.L. Larimer F.W. Hauser L.J. Prodigal: Prokaryotic Gene Recognition and Translation Initiation Site Identification BMC Bioinform. 2010 11 119 10.1186/1471-2105-11-119 20211023 PMC2848648 · DOI
- [74]Alcock B.P. Raphenya A.R. Lau T.T.Y. Tsang K.K. Bouchard M. Edalatmand A. Huynh W. Nguyen A.-L.V. Cheng A.A. Liu S. CARD 2020: Antibiotic Resistome Surveillance with the Comprehensive Antibiotic Resistance Database Nucleic Acids Res. 2020 48 D517 D525 10.1093/nar/gkz935 31665441 PMC7145624 · DOI · Paper page
- [75]Johansson M.H.K. Bortolaia V. Tansirichaiya S. Aarestrup F.M. Roberts A.P. Petersen T.N. Detection of Mobile Genetic Elements Associated with Antibiotic Resistance in Salmonella Enterica Using a Newly Developed Web Tool: MobileElementFinder J. Antimicrob. Chemother. 2021 76 101 109 10.1093/jac/dkaa390 33009809 PMC7729385 · DOI · Paper page
- [76]Krawczyk P.S. Lipinski L. Dziembowski A. PlasFlow: Predicting Plasmid Sequences in Metagenomic Data Using Genome Signatures Nucleic Acids Res. 2018 46 e35 10.1093/nar/gkx1321 29346586 PMC5887522 · DOI
- [77]Roux S. Enault F. Hurwitz B.L. Sullivan M.B. VirSorter: Mining Viral Signal from Microbial Genomic Data PeerJ 2015 3 e985 10.7717/peerj.985 26038737 PMC4451026 · DOI
- [79]Xu Y. Yu Y. Shen Y. Li Q. Lan J. Wu Y. Zhang R. Cao G. Yang C. Effects of Bacillus Subtilis and Bacillus Licheniformis on Growth Performance, Immunity, Short Chain Fatty Acid Production, Antioxidant Capacity, and Cecal Microflora in Broilers Poult. Sci. 2021 100 101358 10.1016/j.psj.2021.101358 34358955 PMC8350532 · DOI
- [80]Ma Y. Wang W. Zhang H. Wang J. Zhang W. Gao J. Wu S. Qi G. Supplemental Bacillus Subtilis DSM 32315 Manipulates Intestinal Structure and Microbial Composition in Broiler Chickens Sci. Rep. 2018 8 15358 10.1038/s41598-018-33762-8 30337568 PMC6194052 · DOI
- [81]Trela J. Kierończyk B. Hautekiet V. Józefiak D. Combination of Bacillus Licheniformis and Salinomycin: Effect on the Growth Performance and GIT Microbial Populations of Broiler Chickens Animals 2020 10 889 10.3390/ani10050889 32443689 PMC7278455 · DOI
- [82]Wang B. Gong L. Zhou Y. Tang L. Zeng Z. Wang Q. Zou P. Yu D. Li W. Probiotic Paenibacillus Polymyxa 10 and Lactobacillus Plantarum 16 Enhance Growth Performance of Broilers by Improving the Intestinal Health Anim. Nutr. 2021 7 829 840 10.1016/j.aninu.2021.03.008 34466687 PMC8384779 · DOI
- [83]Reuben R.C. Sarkar S.L. Ibnat H. Roy P.C. Jahid I.K. Novel Mono- and Multi-Strain Probiotics Supplementation Modulates Growth, Intestinal Microflora Composition and Haemato-Biochemical Parameters in Broiler Chickens Vet. Med. Sci. 2022 8 668 680 10.1002/vms3.709 35014219 PMC8959300 · DOI
- [84]Wu Y. Zhen W. Geng Y. Wang Z. Guo Y. Effects of Dietary Enterococcus Faecium NCIMB 11181 Supplementation on Growth Performance and Cellular and Humoral Immune Responses in Broiler Chickens Poult. Sci 2019 98 150 163 10.3382/ps/pey368 30137622 · DOI
- [85]Han W. Zhang X.L. Wang D.W. Li L.Y. Liu G.L. Li A.K. Zhao Y.X. Effects of Microencapsulated Enterococcus Fecalis CG1.0007 on Growth Performance, Antioxidation Activity, and Intestinal Microbiota in Broiler Chickens J. Anim. Sci. 2013 91 4374 4382 10.2527/jas.2012-5956 23825327 · DOI
- [86]Gao P. Hou Q. Kwok L.-Y. Huo D. Feng S. Zhang H. Effect of Feeding Lactobacillus Plantarum P-8 on the Faecal Microbiota of Broiler Chickens Exposed to Lincomycin Sci. Bull. 2017 62 105 113 10.1016/j.scib.2017.01.001 36659481 · DOI
- [87]Sureshkumar S. Jung S.K. Kim D. Oh K.B. Yang H. Lee H.C. Jo Y.J. Lee H.S. Lee S. Byun S.J. Administration of L. Salivarius Expressing 3D8 ScFv as a Feed Additive Improved the Growth Performance, Immune Homeostasis, and Gut Microbiota of Chickens Anim. Sci. J. 2020 91 e13399 10.1111/asj.13399 32512648 · DOI
- [88]Khan S. Chousalkar K.K. Short-Term Feeding of Probiotics and Synbiotics Modulates Caecal Microbiota during Salmonella Typhimurium Infection but Does Not Reduce Shedding and Invasion in Chickens Appl. Microbiol. Biotechnol. 2020 104 319 334 10.1007/s00253-019-10220-7 31758235 · DOI
- [89]Ahmed M. Lyass L. Markham P.N. Taylor S.S. Vázquez-Laslop N. Neyfakh A.A. Two Highly Similar Multidrug Transporters of Bacillus Subtilis Whose Expression Is Differentially Regulated J. Bacteriol. 1995 177 3904 3910 10.1128/jb.177.14.3904-3910.1995 7608059 PMC177116 · DOI
- [90]Neyfakh A.A. Bidnenko V.E. Chen L.B. Efflux-Mediated Multidrug Resistance in Bacillus Subtilis: Similarities and Dissimilarities with the Mammalian System Proc. Natl. Acad. Sci. USA 1991 88 4781 4785 10.1073/pnas.88.11.4781 1675788 PMC51750 · DOI
- [91]Klyachko K.A. Schuldiner S. Neyfakh A.A. Mutations Affecting Substrate Specificity of the Bacillus Subtilis Multidrug Transporter Bmr J. Bacteriol. 1997 179 2189 2193 10.1128/jb.179.7.2189-2193.1997 9079903 PMC178954 · DOI
- [92]Podlesek Z. Comino A. Herzog-Velikonja B. Zgur-Bertok D. Komel R. Grabnar M. Bacillus Licheniformis Bacitracin-Resistance ABC Transporter: Relationship to Mammalian Multidrug Resistance Mol. Microbiol. 1995 16 969 976 10.1111/j.1365-2958.1995.tb02322.x 7476193 · DOI
- [93]Jack D.L. Storms M.L. Tchieu J.H. Paulsen I.T. Saier M.H. A Broad-Specificity Multidrug Efflux Pump Requiring a Pair of Homologous SMR-Type Proteins J. Bacteriol. 2000 182 2311 2313 10.1128/JB.182.8.2311-2313.2000 10735877 PMC111283 · DOI
- [94]Agersø Y. Bjerre K. Brockmann E. Johansen E. Nielsen B. Siezen R. Stuer-Lauridsen B. Wels M. Zeidan A.A. Putative Antibiotic Resistance Genes Present in Extant Bacillus Licheniformis and Bacillus Paralicheniformis Strains Are Probably Intrinsic and Part of the Ancient Resistome PLoS ONE 2019 14 e0210363 10.1371/journal.pone.0210363 30645638 PMC6333372 · DOI
- [95]Pawlowski A.C. Stogios P.J. Koteva K. Skarina T. Evdokimova E. Savchenko A. Wright G.D. The Evolution of Substrate Discrimination in Macrolide Antibiotic Resistance Enzymes Nat. Commun. 2018 9 112 10.1038/s41467-017-02680-0 29317655 PMC5760710 · DOI
- [96]Hachmann A.-B. Sevim E. Gaballa A. Popham D.L. Antelmann H. Helmann J.D. Reduction in Membrane Phosphatidylglycerol Content Leads to Daptomycin Resistance in Bacillus Subtilis Antimicrob. Agents Chemother. 2011 55 4326 4337 10.1128/AAC.01819-10 21709092 PMC3165287 · DOI
- [97]Hachmann A.-B. Angert E.R. Helmann J.D. Genetic Analysis of Factors Affecting Susceptibility of Bacillus Subtilis to Daptomycin Antimicrob. Agents Chemother. 2009 53 1598 1609 10.1128/AAC.01329-08 19164152 PMC2663116 · DOI
- [98]Ernst C.M. Staubitz P. Mishra N.N. Yang S.-J. Hornig G. Kalbacher H. Bayer A.S. Kraus D. Peschel A. The Bacterial Defensin Resistance Protein MprF Consists of Separable Domains for Lipid Lysinylation and Antimicrobial Peptide Repulsion PLoS Pathog. 2009 5 e1000660 10.1371/journal.ppat.1000660 19915718 PMC2774229 · DOI
- [99]Urshev Z. Yungareva T. Initial Safety Evaluation of Enterococcus Faecium LBB.E81 Biotechnol. Biotechnol. Equip. 2021 35 11 17 10.1080/13102818.2020.1840438 · DOI · Paper page
- [100]Hassen B. Abbassi M.S. Ruiz-Ripa L. Mama O.M. Hassen A. Torres C. Hammami S. High Prevalence of Mcr-1 Encoding Colistin Resistance and First Identification of BlaCTX-M-55 in ESBL/CMY-2-Producing Escherichia Coli Isolated from Chicken Faeces and Retail Meat in Tunisia Int. J. Food Microbiol. 2020 318 108478 10.1016/j.ijfoodmicro.2019.108478 31855787 · DOI
- [101]Poirel L. Héritier C. Podglajen I. Sougakoff W. Gutmann L. Nordmann P. Emergence in Klebsiella Pneumoniae of a Chromosome-Encoded SHV Beta-Lactamase That Compromises the Efficacy of Imipenem Antimicrob. Agents Chemother. 2003 47 755 758 10.1128/AAC.47.2.755-758.2003 12543688 PMC151740 · DOI
- [102]Di Conza J.A. Badaracco A. Ayala J. Rodríguez C. Famiglietti A. Gutkind G.O. β-Lactamases Produced by Amoxicillin-Clavulanate-Resistant Enterobacteria Isolated in Buenos Aires, Argentina: A New BlaTEM Gene Rev. Argent. Microbiol. 2014 46 210 217 10.1016/S0325-7541(14)70075-6 25444130 · DOI
Cited by
Sorted by citations
Kerek, Á., Husz, L. H., Szarka, E., Tornyos, G. Á., & Jerzsele, Á. (2026) · Antibiotics · doi:10.3390/antibiotics15060544
“…carry detectable ARGs, but that public-health relevance depends on taxon identity, gene function, genomic context and mobility potential rather than on ARG counts alone [15–18 ,22, The results are directly aligned with the EFSA/FEEDAP safety concept for viable microorganisms used as feed additives.”
Self-citation
- Authors
- Kerek, Á., Román, I. L., Szabó, Á., Papp, M., Bányai, K., Kardos, G., Kaszab, E., Bali, K., Makrai, L., & Jerzsele, Á.
- Affiliations
- University of Veterinary Medicine (HU)
- Department of Pharmacology and Toxicology, University of Veterinary Medicine, István utca 2, H-1078 Budapest, Hungary
- University of Debrecen (HU)
- Autovakcina Kft., Szabadság sgrt. 57, H-1171 Budapest, Hungary
- Corresponding author
- Kerek, Ádám
- ORCID
- Venue
- Animals
- Publisher
- MDPI AG
- Published
- 2024-06-29
- Volume
- 14
- Issue
- 13
- Pages
- 1927
- ISSN
- 2076-2615 (ISSN-L)
- PMC
- PMC11240415
- OpenAlex
- W4400209737
- Cited by
- 8
- References
- 6
- Citations by year
- 2026: 5 · 2025: 3
- FWCI
- 1.00
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- Animals (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- University of Debrecen Electronic Archive (University of Debrecen) (submittedVersion, cc-by)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Funders
- Recovery and Resilience Facility (RRF) (RRF-2.3.1-21-2022-00001, RRF-2.3.1-21)
- National Recovery Fund budget estimate (RRF-2.3.1-21-2022-00001, RRF-2.3.1-21)
- National Research, Development, and Innovation Fund (RRF-2.3.1-21-2022-00001, RRF-2.3.1-21)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Medicine › Antibiotic Resistance in Bacteria
- Physical Sciences › Environmental Science › Pollution › Pharmaceutical and Antibiotic Environmental Impacts
- Life Sciences › Immunology and Microbiology › Applied Microbiology and Biotechnology › Antibiotic Use and Resistance
- Keywords
- veterinary probiotics, broiler chickens, antimicrobial resistance genes, resistome, gut microbiota, antibiotic use reduction, mobile genetic elements, plasmids, bacteriophages, fluoroquinolone resistance, critically important antibiotics, aac(6')-II, multidrug resistance genes, public health risk
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