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Resistome metagenomics from plate to farm: The resistome and microbial composition during food waste feeding and composting on a Vermont poultry farm


Autoři: Korin Eckstrom aff001;  John W. Barlow aff002
Působiště autorů: Department of Microbiology and Molecular Genetics, The University of Vermont, Burlington, Vermont, United States of America aff001;  Department of Animal and Veterinary Sciences, The University of Vermont, Burlington, Vermont, United States of America aff002
Vyšlo v časopise: PLoS ONE 14(11)
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pone.0219807

Souhrn

Food waste diversion and composting, either mandated or voluntary, are growing alternatives to traditional waste disposal. An acceptable source of agricultural feed and composting material, methane-emitting food residuals, including post-consumer food scraps, are diverted from landfills allowing recapture of nutrients that would otherwise be lost. However, risk associated with the transfer of antimicrobial resistant bacteria (ARB), antibiotic resistance genes (ARGs), or pathogens from food waste is not well characterized. Using shotgun metagenomic sequencing, ARGs, microbial content, and associated virulence factors were successfully identified across samples from an integrated poultry farm that feeds post-consumer food waste. A total of 495 distinct bacterial species or sub-species, 50 ARGs, and 54 virulence gene sequences were found. ARG sequences related to aminoglycoside, tetracycline, and macrolide resistance were most prominent, while most virulence gene sequences were related to transposon or integron activity. Microbiome content was distinct between on-farm samples and off-farm food waste collection sites, with a reduction in pathogens throughout the composting process. While most samples contained some level of resistance, only 3 resistance gene sequences occurred in both on- and off-farm samples and no multidrug resistance (MDR) gene sequences persisted once on the farm. The risk of incorporating novel or multi-drug resistance from human sources appears to be minimal and the practice of utilizing post-consumer food scraps as feed for poultry and composting material may not present a significant risk for human or animal health. Pearson correlation and co-inertia analysis identified a significant interaction between resistance and virulence genes (P = 0.05, RV = 0.67), indicating that ability to undergo gene transfer may be a better marker for ARG risk than presence of specific bacterial species. This work expands the knowledge of ARG fate during food scrap animal feeding and composting and provides a methodology for reproducible analysis.

Klíčová slova:

Antibiotic resistance – Antimicrobial resistance – Farms – Livestock – Metagenomics – Poultry – Shotgun sequencing – Virulence factors


Zdroje

1. Ventola LC. The antibiotic resistance crisis: part 1: causes and threats. P & T: a peer-reviewed journal for formulary management. 2015;40: 277–83.

2. State of Vermont. Act 148: An act relating to establishing universal recycling of solid waste. 2012. https://dec.vermont.gov/waste-management/solid/universal-recycling (accessed 5 November 2019.)

3. Vermont Agency of Agriculture, Food and markets. Guidance on feeding food scraps to pigs. 2018 https://agriculture.vermont.gov/sites/agriculture/files/documents/Feeding%20Food%20Scraps%20to%20Pigs%20January%202018.pdf (accessed 5 November 2019.)

4. Bezanson GS, MacInnis R, Potter G, Hughes T. Presence and potential for horizontal transfer of antibiotic resistance in oxidase-positive bacteria populating raw salad vegetables. International Journal of Food Microbiology. 2008;127: 37–42. doi: 10.1016/j.ijfoodmicro.2008.06.008 18632174

5. Sultana F, Kamrunnahar, Afroz H, Jahan A, Fakruddin M, Datta S. Multi–antibiotic resistant bacteria in frozen food (ready to cook food) of animal origin sold in Dhaka, Bangladesh. Asian Pacific Journal of Tropical Biomedicine. 2014;4: S268–S271. doi: 10.12980/APJTB.4.2014B85 25183094

6. Kevenk T, Gulel G. Prevalence, Antimicrobial Resistance and Serotype Distribution of Listeria monocytogenes Isolated from Raw Milk and Dairy Products. Journal of Food Safety. 2016;36: 11–18. doi: 10.1111/jfs.12208

7. lveira-Filho V, Luz IS, Campos AF, lva W, Barros MS, Medeiros ES, et al. Antibiotic Resistance and Molecular Analysis of Staphylococcus aureus Isolated from Cow’s Milk and Dairy Products in Northeast Brazil. Journal of Food Protection. 2014;77: 583–591. doi: 10.4315/0362-028X.JFP-13-343 24680069

8. EPA. Food Waste Management in the United States, 2014. 2016. https://www.epa.gov/sites/production/files/2016-12/documents/food_waste_management_2014_12082016_508.pdf (accessed 5 November 2019.)

9. Zhu Y-G, Johnson TA, Su J-Q, Qiao M, Guo G-X, Stedtfeld RD, et al. Diverse and abundant antibiotic resistance genes in Chinese swine farms. Proceedings of the National Academy of Sciences. 2013;110: 3435–3440. doi: 10.1073/pnas.1222743110 23401528

10. Udikovic-Kolic N, Wichmann F, Broderick NA, Handelsman J. Bloom of resident antibiotic-resistant bacteria in soil following manure fertilization. Proceedings of the National Academy of Sciences. 2014;111: 15202–15207. doi: 10.1073/pnas.1409836111 25288759

11. Wichmann F, Udikovic-Kolic N, Andrew S, Handelsman J. Diverse Antibiotic Resistance Genes in Dairy Cow Manure. mBio. 2014;5: e01017–13. doi: 10.1128/mbio.01017-13 24757214

12. Ross J, Topp E. Abundance of Antibiotic Resistance Genes in Bacteriophage following Soil Fertilization with Dairy Manure or Municipal Biosolids, and Evidence for Potential Transduction. Applied and Environmental Microbiology. 2015;81: 7905–7913. doi: 10.1128/AEM.02363-15 26341211

13. Noyes NR, Yang X, Linke LM, Magnuson RJ, Cook SR, Zaheer R, et al. Characterization of the resistome in manure, soil and wastewater from dairy and beef production systems. Scientific Reports. 2016;6: srep24645. doi: 10.1038/srep24645 27095377

14. Qian X, Sun W, Gu J, Wang X-J, Zhang Y-J, Duan M-L, et al. Reducing antibiotic resistance genes, integrons, and pathogens in dairy manure by continuous thermophilic composting. Bioresource Technology. 2016;220: 425–432. doi: 10.1016/j.biortech.2016.08.101 27598571

15. Durso L, Miller DN, Wienhold BJ. Distribution and Quantification of Antibiotic Resistant Genes and Bacteria across Agricultural and Non-Agricultural Metagenomes. PLoS ONE. 2012;7: e48325. doi: 10.1371/journal.pone.0048325 23133629

16. Bengtsson-Palme J, Boulund F, Fick J, Kristiansson E, Larsson JD. Shotgun metagenomics reveals a wide array of antibiotic resistance genes and mobile elements in a polluted lake in India. Frontiers in Microbiology. 2014;5: 648. doi: 10.3389/fmicb.2014.00648 25520706

17. Rowe W, Verner-Jeffreys DW, Baker-Austin C, Ryan JJ, Maskell DJ, Pearce GP. Comparative metagenomics reveals a diverse range of antimicrobial resistance genes in effluents entering a river catchment. Water Science and Technology. 2016;73: 1541–1549. doi: 10.2166/wst.2015.634 27054725

18. Tuer S, Pryer KM, Miao VP, Palmer JD. Investigating Deep Phylogenetic Relationships among Cyanobacteria and Plastids by Small Subunit rRNA Sequence Analysis1. J Eukaryot Microbiol. 1999;46: 327–338. doi: 10.1111/j.1550-7408.1999.tb04612.x 10461381

19. López-García P, Rodríguez-Valera F, Pedrós-Alió C, Moreira D. Unexpected diversity of small eukaryotes in deep-sea Antarctic plankton. Nature. 2001;409: 603–607. doi: 10.1038/35054537 11214316

20. Rove MT, Jones DR, Northcutt JK, Harrison MA, Cox NA. Impact of Commercial Processing on the Microbiology of Shell Eggs. Journal of Food Protection. 2016;68: 2367–2375. doi: 10.4315/0362-028x-68.11.2367 16300075

21. Andrews S. FastQC: a quality control tool for high throughput sequence data. Available online at: http://www.bioinformatics.babraham.ac.uk/projects/fastqc. 2010;

22. Salter SJ, Cox MJ, Turek EM, Calus ST, Cookson WO, Moffatt MF, et al. Reagent and laboratory contamination can critically impact sequence-based microbiome analyses. BMC Biology. 2014;12: 1–12. doi: 10.1186/1741-7007-12-1

23. Kim D, Hofstaedter CE, Zhao C, Mattei L, Tanes C, Clarke E, et al. Optimizing methods and dodging pitfalls in microbiome research. Microbiome. 2017;5: 52. doi: 10.1186/s40168-017-0267-5 28476139

24. and Warnes MR. gplots: Various R Programming Tools for Plotting Data. https://CRANR-project.org/package=gplots. 2016;

25. and Oksanen EM. vegan: Community Ecology Package. https://CRANR-project.org/package=vegan. 2018;

26. with contributions from and many Jr CF. Hmisc: Harrell Miscellaneous. https://CRANR-project.org/package=Hmisc. 2018;

27. Culhane AC, Thioulouse J, Perrière G, Higgins DG. MADE4: an R package for multivariate analysis of gene expression data. Bioinformatics. 2005;21: 2789–2790. doi: 10.1093/bioinformatics/bti394 15797915

28. Wickham H. ggplot2: Elegant Graphics for Data Analysis. Springer-Verlag New York. 2009;

29. Jalali S, Kohli S, Latka C, Bhatia S, Vellarikal S, dhar Sivasubbu, et al. Screening Currency Notes for Microbial Pathogens and Antibiotic Resistance Genes Using a Shotgun Metagenomic Approach. PLOS ONE. 2015;10: e0128711. doi: 10.1371/journal.pone.0128711 26035208

30. McIntyre AB, Ounit R, Afshinnekoo E, Prill RJ, Hénaff E, Alexander N, et al. Comprehensive benchmarking and ensemble approaches for metagenomic classifiers. Genome Biology. 2017;18: 182. doi: 10.1186/s13059-017-1299-7 28934964

31. Cagle R, Ramachandran P, Reed E, Commichaux S, Mammel MK, Lacher DW, et al. Microbiota of the Hickey Run Tributary of the Anacostia River. Microbiol Resour Announc. 2019;8. doi: 10.1128/mra.00123-19 30938701

32. Hamner S, Brown BL, Hasan NA, Franklin MJ, Doyle J, Eggers MJ, et al. Metagenomic Profiling of Microbial Pathogens in the Little Bighorn River, Montana. Int J Environ Res Pu. 2019;16: 1097. doi: 10.3390/ijerph16071097 30934749

33. Ng C, Tay M, Tan B, Le T-H, Haller L, Chen H, et al. Characterization of Metagenomes in Urban Aquatic Compartments Reveals High Prevalence of Clinically Relevant Antibiotic Resistance Genes in Wastewaters. Frontiers in Microbiology. 2017;8: 2200. doi: 10.3389/fmicb.2017.02200 29201017

34. Roberts MC. Update on acquired tetracycline resistance genes. FEMS Microbiology Letters. 2005;245: 195–203. doi: 10.1016/j.femsle.2005.02.034 15837373

35. Luna V, Roberts M. The presence of the tetO gene in a variety of tetracycline-resistant Streptococcus pneumoniae serotypes from Washington State. Journal of Antimicrobial Chemotherapy. 1998;42: 613–619. doi: 10.1093/jac/42.5.613 9848445

36. Diarra MS, Rempel H, Champagne J, Masson L, Pritchard J, Topp E. Distribution of Antimicrobial Resistance and Virulence Genes in Enterococcus spp. and Characterization of Isolates from Broiler Chickens. Applied and Environmental Microbiology. 2010;76: 8033–8043. doi: 10.1128/AEM.01545-10 20971861

37. Yang X, Noyes NR, Doster E, Martin JN, Linke LM, Magnuson RJ, et al. Use of Metagenomic Shotgun Sequencing Technology To Detect Foodborne Pathogens within the Microbiome of the Beef Production Chain. Applied and Environmental Microbiology. 2016;82: 2433–2443. doi: 10.1128/AEM.00078-16 26873315

38. Jia S, Zhang X-X, Miao Y, Zhao Y, Ye L, Li B, et al. Fate of antibiotic resistance genes and their associations with bacterial community in livestock breeding wastewater and its receiving river water. Water Research. 2017;124: 259–268. doi: 10.1016/j.watres.2017.07.061 28763642

39. Szekeres E, Baricz A, Chiriac C, Farkas A, Opris O, Soran M-L, et al. Abundance of antibiotics, antibiotic resistance genes and bacterial community composition in wastewater effluents from different Romanian hospitals. Environmental Pollution. 2017;225: 304–315. doi: 10.1016/j.envpol.2017.01.054 28347610

40. Bennett P. Plasmid encoded antibiotic resistance: acquisition and transfer of antibiotic resistance genes in bacteria. British Journal of Pharmacology. 2008;153: S347–S357. doi: 10.1038/sj.bjp.0707607 18193080

41. Danon M, Franke‐Whittle IH, Insam H, Chen Y, Hadar Y. Molecular analysis of bacterial community succession during prolonged compost curing. FEMS Microbiology Ecology. 2008;65: 133–144. doi: 10.1111/j.1574-6941.2008.00506.x 18537836

42. Neher DA, Weicht TR, Bates ST, Leff JW, Fierer N. Changes in Bacterial and Fungal Communities across Compost Recipes, Preparation Methods, and Composting Times. PLoS ONE. 2013;8: e79512. doi: 10.1371/journal.pone.0079512 24278144

43. Huang K, Xia H, Cui G, Li F. Effects of earthworms on nitrification and ammonia oxidizers in vermicomposting systems for recycling of fruit and vegetable wastes. Science of The Total Environment. 2017;578: 337–345. doi: 10.1016/j.scitotenv.2016.10.172 27842968

44. Hénault-Ethier L, Martin V, Gélinas Y. Persistence of Escherichia coli in batch and continuous vermicomposting systems. Waste Management. 2016;56: 88–99. doi: 10.1016/j.wasman.2016.07.033 27499290

45. Dolka B, Chrobak-Chmiel D, Czopowicz M, Szeleszczuk P. Characterization of pathogenic Enterococcus cecorum from different poultry groups: Broiler chickens, layers, turkeys, and waterfowl. Plos One. 2017;12: e0185199. doi: 10.1371/journal.pone.0185199 28934313

46. Song A, In LL, Lim S, Rahim R. A review on Lactococcus lactis: from food to factory. Microb Cell Fact. 2017;16: 55. doi: 10.1186/s12934-017-0669-x 28376880

47. Santajit S, Indrawattana N. Mechanisms of Antimicrobial Resistance in ESKAPE Pathogens. BioMed Research International. 2016;2016: 2475067. doi: 10.1155/2016/2475067 27274985

48. Schürch AC, Schaik W. Challenges and opportunities for whole‐genome sequencing–based surveillance of antibiotic resistance. Annals of the New York Academy of Sciences. 2017;1388: 108–120. doi: 10.1111/nyas.13310 28134443

49. Whiley H, Ross K. Salmonella and Eggs: From Production to Plate. Int J Environ Res Pu. 2015;12: 2543–2556. doi: 10.3390/ijerph120302543 25730295

50. US Food and Drug Administration. Prevention of Salmonella Enteritidis in Shell Eggs During Production, Storage, and Transportation: Guidance for Industry. 2015; Accessed 24Oct2019; Available from: https://www.fda.gov/media/83513/download

51. Bell RL, Jarvis KG, Ottesen AR, McFarland MA, Brown EW. Recent and emerging innovations in Salmonella detection: a food and environmental perspective. Microb Biotechnol. 2016;9: 279–292. doi: 10.1111/1751-7915.12359 27041363

52. Sekse C, Holst-Jensen A, Dobrindt U, Johannessen GS, Li W, Spilsberg B, et al. High Throughput Sequencing for Detection of Foodborne Pathogens. Front Microbiol. 2017;8: 2029. doi: 10.3389/fmicb.2017.02029 29104564

53. Ramaraj T, Matyi SA, Sundararajan A, Lindquist IE, Devitt NP, Schilkey FD, et al. Draft Genome Sequences of Vancomycin-Susceptible Staphylococcus aureus Related to Heterogeneous Vancomycin-Intermediate S. aureus. Genome Announcements. 2014;2: e01033–14. doi: 10.1128/genomeA.01033-14 25301662

54. Iwao Y, Takano T, Hung W-C, Higuchi W, Isobe H, Nishiyama A, et al. The emerging ST8 methicillin-resistant Staphylococcus aureus clone in the community in Japan: associated infections, genetic diversity, and comparative genomics. Journal of Infection and Chemotherapy. 2012;18: 228–240. doi: 10.1007/s10156-012-0379-6 22350401

55. Liao H, Lu X, Rensing C, Friman V, Geisen S, Chen Z, et al. Hyperthermophilic composting accelerates the removal of antibiotic resistance genes and mobile genetic elements in sewage sludge. Environmental Science & Technology. 2017;52: 266–276. doi: 10.1021/acs.est.7b04483 29199822

56. Bengtsson-Palme J, Angelin M, Huss M, Kjellqvist S, Kristiansson E, Palmgren H, et al. The Human Gut Microbiome as a Transporter of Antibiotic Resistance Genes between Continents. Antimicrobial Agents and Chemotherapy. 2015;59: 6551–6560. doi: 10.1128/AAC.00933-15 26259788

57. Luo G, Li B, Li L-G, Zhang T, Angelidaki I. Antibiotic resistance genes and correlations with microbial community and metal resistance genes in full-scale biogas reactors as revealed by metagenomic analysis. Environmental Science & Technology. 2017;51: 4069–4080. doi: 10.1021/acs.est.6b05100 28272884

58. Hwang S, Kim C, Ji S-G, Go J, Kim H, Yang S, et al. Network-assisted investigation of virulence and antibiotic-resistance systems in Pseudomonas aeruginosa. Scientific Reports. 2016;6: 26223. doi: 10.1038/srep26223 27194047

59. Rosengren LB, Waldner CL, Reid-Smith RJ. Associations between Antimicrobial Resistance Phenotypes, Antimicrobial Resistance Genes, and Virulence Genes of Fecal Escherichia coli Isolates from Healthy Grow-Finish Pigs. Applied and Environmental Microbiology. 2009;75: 1373–1380. doi: 10.1128/AEM.01253-08 19139228

60. Zhang T, Yang Y, Pruden A. Effect of temperature on removal of antibiotic resistance genes by anaerobic digestion of activated sludge revealed by metagenomic approach. Applied Microbiology and Biotechnology. 2015;99: 7771–7779. doi: 10.1007/s00253-015-6688-9 25994259

61. Dray S, Chessel D, Thioulouse J. Co-inertia analysis and the linking of ecological data tables. Ecology. 2003;84: 3078–3089.

62. Schroeder M, Brooks BD, Brooks AE. The Complex Relationship between Virulence and Antibiotic Resistance. Genes. 2017;8: 39. doi: 10.3390/genes8010039 28106797

63. Wang C, Dong D, Strong P, Zhu W, Ma Z, Qin Y, et al. Microbial phylogeny determines transcriptional response of resistome to dynamic composting processes. Microbiome. 2017;5: 103. doi: 10.1186/s40168-017-0324-0 28814344

64. Arango-Argoty G, Dai D, Pruden A, Vikesland P, Heath L, Zhang L. NanoARG: a web service for detecting and contextualizing antimicrobial resistance genes from nanopore-derived metagenomes. Microbiome. 2019;7: 88. doi: 10.1186/s40168-019-0703-9 31174603

65. Huson DH, Albrecht B, Bağcı C, Bessarab I, Górska A, Jolic D, et al. MEGAN-LR: new algorithms allow accurate binning and easy interactive exploration of metagenomic long reads and contigs. Biol Direct. 2018;13: 6. doi: 10.1186/s13062-018-0208-7 29678199

66. Kamathewatta K, Bushell R, Young N, Stevenson M, Billman-Jacobe H, Browning G, et al. Exploration of antibiotic resistance risks in a veterinary teaching hospital with Oxford Nanopore long read sequencing. Plos One. 2019;14: e0217600. doi: 10.1371/journal.pone.0217600 31145757

67. Jia B, Raphenya AR, Alcock B, Waglechner N, Guo P, Tsang KK, et al. CARD 2017: expansion and model-centric curation of the comprehensive antibiotic resistance database. Nucleic Acids Research. 2017; 45: D566–D573. doi: 10.1093/nar/gkw1004 27789705

68. Ramirez MS, Tolmasky ME. Aminoglycoside modifying enzymes. Drug Resistance Updates. 2010; 13: 151–171. doi: 10.1016/j.drup.2010.08.003 20833577

69. Flórez A, Reyes‐Gavilán CG, Wind A, Mayo B, Margolles A. Ubiquity and diversity of multidrug resistance genes in Lactococcus lactis strains isolated between 1936 and 1995. FEMS Microbiology Letters. 2006; 263: 21–25. doi: 10.1111/j.1574-6968.2006.00371.x 16958846

70. Su X-Z, Chen J, Mizushima T, Kuroda T, Tsuchiya T. Abe M, an H+-Coupled Acinetobacter baumannii Multidrug Efflux Pump Belonging to the MATE Family of Transporters. Antimicrobial Agents and Chemotherapy. 2005; 49: 4362–4364. doi: 10.1128/AAC.49.10.4362-4364.2005 16189122

71. Srinivasan V, Rajamohan G, Gebreyes WA. Role of AbeS, a Novel Efflux Pump of the SMR Family of Transporters, in Resistance to Antimicrobial Agents in Acinetobacter baumannii. Antimicrobial Agents and Chemotherapy. 2009; 53: 5312–5316. doi: 10.1128/AAC.00748-09 19770280

72. Coyne S, Rosenfeld N, Lambert T, Courvalin P, Périchon B. Overexpression of Resistance-Nodulation-Cell Division Pump AdeFGH Confers Multidrug Resistance in Acinetobacter baumannii. Antimicrob Agents Ch. 2010; 54: 4389–4393. doi: 10.1128/aac.00155-10 20696879

73. Damier-Piolle L, Magnet S, Brémont S, Lambert T, Courvalin P. AdeI JK, a Resistance-Nodulation-Cell Division Pump Effluxing Multiple Antibiotics in Acinetobacter baumannii. Antimicrob Agents Ch. 2008; 52: 557–562. doi: 10.1128/aac.00732-07 18086852

74. Yin Y, He X, Szewczyk P, Nguyen T, Chang G. Structure of the Multidrug Transporter EmrD from Escherichia coli. Science. 2006; 312: 741–744. doi: 10.1126/science.1125629 16675700

75. Daly M, Villa L, Pezzella C, Fanning S, Carattoli A. Comparison of multidrug resistance gene regions between two geographically unrelated Salmonella serotypes. Journal of Antimicrobial Chemotherapy. 2005; 55: 558–561. doi: 10.1093/jac/dki015 15722395

76. Sköld O. Resistance to trimethoprim and sulfonamides. Veterinary research. 2001; 32: 261–73. doi: 10.1051/vetres:2001123 11432417

77. Akhtar M, Hirt H, Zurek L. Horizontal Transfer of the Tetracycline Resistance Gene tetM Mediated by pCF10 Among Enterococcus faecalis in the House Fly (Musca domestica L.) Alimentary Canal. Microbial Ecology. 2009; 58: 509–518. doi: 10.1007/s00248-009-9533-9 19475445

78. Scott KP, Melville CM, Barbosa TM, Flint HJ. Occurrence of the New Tetracycline Resistance Gene tet(W) in Bacteria from the Human Gut. Antimicrobial Agents and Chemotherapy. 2000; 44: 775–777. doi: 10.1128/aac.44.3.775-777.2000 10681357

79. Volkers G, Palm GJ, Weiss MS, Wright GD, Hinrichs W. Structural basis for a new tetracycline resistance mechanism relying on the TetX monooxygenase. FEBS Letters. 2011; 585: 1061–1066. doi: 10.1016/j.febslet.2011.03.012 21402075

80. Yang W, Moore IF, Koteva KP, Bareich DC, Hughes DW, Wright GD. TetX Is a Flavin-dependent Monooxygenase Conferring Resistance to Tetracycline Antibiotics. Journal of Biological Chemistry. 2004; 279: 52346–52352. doi: 10.1074/jbc.M409573200 15452119

81. Murshed M, Shahnaz S, Malek M. Detection of resistance gene marker intl1 and antimicrobial resistance pattern of E. coli isolated from surgical site wound infection in Holy Family Red Crescent Medical College Hospital. Bangladesh Journal of Medical Microbiology. 2012; 4: 19–23. doi: 10.3329/bjmm.v4i2.10827

82. Anand T, Bera BC, Vaid RK, Barua S, Riyesh T, Virmani N, et al. Abundance of antibiotic resistance genes in environmental bacteriophages. J Gen Virol. 2016; doi: 10.1099/jgv.0.000639 27902329

83. Paczosa MK, Mecsas J. Klebsiella pneumoniae: Going on the Offense with a Strong Defense. Microbiol Mol Biol R. 2016; 80: 629–661. doi: 10.1128/mmbr.00078-15 27307579

84. Antunes P, Machado J, Sousa J, Peixe L. Dissemination of Sulfonamide Resistance Genes (sul1, sul2, and sul3) in Portuguese Salmonella enterica Strains and Relation with Integrons. Antimicrobial Agents and Chemotherapy. 2005; 49: 836–839. doi: 10.1128/AAC.49.2.836-839.2005 15673783

85. Ahmed HA, El-Hofy FI, afik S, Abdelrahman MA, Elsaid GA. Characterization of Virulence-Associated Genes, Antimicrobial Resistance Genes, and Class 1 Integrons in Salmonella enterica serovar Typhimurium Isolates from Chicken Meat and Humans in Egypt. Foodborne Pathogens and Disease. 2016; 13: 281–288. doi: 10.1089/fpd.2015.2097 26977940

86. Ramos JL, Martínez-Bueno M, Molina-Henares AJ, Ter^n W, Watanabe K, Zhang X, et al. The TetR Family of Transcriptional Repressors. Microbiol Mol Biol R. 2005; 69: 326–356. doi: 10.1128/mmbr.69.2.326–356.2005

87. Carnelli A, Mauri F, Demarta A. Characterization of genetic determinants involved in antibiotic resistance in Aeromonas spp. and fecal coliforms isolated from different aquatic environments. Research in Microbiology. 2017; 168: 461–471. doi: 10.1016/j.resmic.2017.02.006 28263906


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