Microbiome and antimicrobial resistance genes in microbiota of cloacal samples from European herring gulls (Larus argentatus)

Abstract

Introduction: The aim of the study was to determine microbiota in the cloacal samples of European herring gulls (Larus argentatus) and to compare a variety of genes encoding antimicrobial resistance in cultivable and non-cultivable bacteria.

Material and Methods: Cloacal samples from European herring gulls were collected from a Kaunas city dump. Cultivable microbiota were isolated, their microbial susceptibility was tested, and genes encoding antimicrobial resistance were detected. Additionally, a metagenomic study was performed using Next-Generation Sequencing (NGS).

Results: In total, 697 different operational taxonomic units at genus level were detected; however, only 63 taxonomic units were detected at the amount of ≥0.1% of the total number of DNA copies. Catellicoccus marimammalium was found to have the highest prevalence. The bacterial amount of other genera was up to 5% with the most highly prevalent being Psychrobacter (4.7%), Helicobacter (4.5%), unclassified Enterococcaceae (3.2%), Pseudomonas (2.9%), and Brachyspira (2.6%).

Conclusions:C. marimammalium are predominant microbiota in the cloacal samples of Larus argentatus. This species of gulls is a reservoir of bacteria carrying a wide-spectrum of genes encoding antimicrobial resistance. The same genes were detected in both cultivable microbiota and in the total DNA of the samples.

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  • 1. Bauer A.W., Kirby W.M.M., Sherris J.C., Turk M.: Antibiotic susceptibility testing by a standardized single disk method. Am J Clin Pathol 1966, 45, 493–496.

  • 2. Bonnedahl J., Järhult J.: Antibiotic resistance in wild birds. Ups J Med Sci 2014, 119, 113–116, doi: 10.3109/03009734.2014.905663.

  • 3. Caprioli A., Busani L., Martel J.L., Helmuth R.: Monitoring of antibiotic resistance in bacteria of animal origin: epidemiological and microbiological methodologies. Int J Antimicrob Agents 2000, 14, 295–301.

  • 4. Clinical and Laboratory Standards Institute CLSI.: Performance standards for antimicrobial disk susceptibility tests; approved standard – eleventh edition. CLSI Documents M02-A11, Wayne, USA, 2012.

  • 5. Dolejska M., Cizek A., Literak I.: High prevalence of antimicrobial-resistant genes and integrons in Escherichia coli isolates from black-headed gulls in the Czech Republic. J Appl Microbiol 2007, 103, 11–19.

  • 6. Irlinger F., Loux V., Bento P., Gibrat J., Straub C., Bonnarme P., Landaud S., Monnet C.: Genome sequence of Staphylococcus equorum subsp. equorum Mu2, isolated from a French smearripened cheese. J Bacteriol 2012, 194, 5141–5142, doi: 10.1128/JB.01038-12.

  • 7. Liakopoulos A., Mevius D.J, Olsen B., Bonnedahl J.: The colistin resistance mcr-1 gene is going wild. J Antimicrob Chemother 2016, 71, 2335–2336, doi: 10.1093/jac/dkw262.

  • 8. Lu J., Santo Domingo J.W., Lamendella R., Edge T., Hill S.: Phylocgenetic diversity and molecular detection of bacteria in full faeces. Appl Environ Microbiol 2008, 74, 3969–3976.

  • 9. Manges A.R.: Genomic epidemiology: revealing hidden reservoirs for Klebsiella pneumoniae. Clin Infect Dis 2015, 61, 900–902, doi: 10.1093/cid/civ433.

  • 10. Mittal S., Mallik S., Sharma S., Virdi J.S.: Characteristics of β-lactamases and their genes (blaA and blaB) in Yersinia intermedia and Y. frederiksenii. BMC Microbiol 2007, 7, 25, doi: 10.1186/1471-2180-7-25.

  • 11. Neo E., La T., Phillips N.D., Alikani M.Y., Hampson D.J.: The pathogenic intestinal spirochatae Brachyspira pilosicoli forms a diverse recombinant species demonstrating some local clustering of related strains and potential for zoonotic spread. Gut Pathog 2013, 5, 24, doi: 10.1186/1757-4749-5-24.

  • 12. Radhouani H., Poeta P., Gonçalves A., Pacheco R., Sargo R., Igrejas G.: Wild birds as biological indicators of environmental pollution: antimicrobial resistance patterns of Escherichia coli and enterococci isolated from common buzzards (Buteo buteo). J Med Microbiol 2012, 61, 837–843, doi 10.1099/jmm.0.038364-0.

  • 13. Rizi K.S., Peerayeh S.N., Bakhshi B., Rahbar M.: Prevalence of integrons and antimicrobial resistance genes among clinical isolates of Enterobacter spp. from hospitals in Tehran. Int J Enteric Pathog 2015, 3, 22531, doi: 10.17795/ijep22531.

  • 14. Ruzauskas M., Couto N., Kerziene S., Siugzdiniene R., Klimiene I., Virgailis M., Pomba C.: Prevalence, species distribution and antimicrobial resistance patterns of methicillin-resistant staphylococci in Lithuanian pet animals. Acta Vet Scand 2015, 57, 27, doi: 10.1186/s13028-015-0117-z.

  • 15. Ruzauskas M., Siugzdiniene R., Butrimaite-Ambrozeviciene C., Zymantiene J., Klimiene I., Vaskeviciute L., Mockeliunas R., Virgailis M.: Prevalence and characterization of multi-resistant Staphylococcus spp., isolated from poultry liver. J Food Safety 2016, 36, 508–514, doi: 10.1111/jfs.12270.

  • 16. Ruzauskas M., Siugzdiniene R., Klimiene I., Virgailis M., Mockeliunas R., Vaskeviciute L., Zienius D.: Prevalence of methicillin-resistant Staphylococcus haemolyticus in companion animals: a cross-sectional study. Ann Clin Microbiol Antimicrob 2014, 13, 56, doi: 10.1186/s12941-014-0056-y.

  • 17. Ruzauskas M., Vaskeviciute L.: Detection of the mcr-1 gene in Escherichia coli prevalent in the migratory bird species Larus argentatus. J Antimicrob Chemother 2016, 71, 2333–2334, doi: 10.1093/jac/dkw245.

  • 18. Seputiene V., Bogdaite A., Ruzauskas M., Suziedeliene E.: Antibiotic resistance genes and virulence factors in Enterococcus faecium and Enterococcus faecalis from diseased farm animals: pigs, cattle and poultry. Pol J Vet Sci 2012, 15, 431–438, doi: 10.2478/v10181-012-0067-6.

  • 19. Seputiene V., Povilonis J., Ruzauskas M., Virgailis M., Zlabys P., Suziedeliene E.: Quinolone resistance among Salmonella enterica and Escherichia coli in Lithuania. Biologija, 2006, 3, 74–78.

  • 20. Shobrak M.Y., Abo-Amer A.E.: Role of wild birds as carriers of multi-drug resistant Escherichia coli and Escherichia vulneris. Braz J Microbiol 2014, 45, 1199–1209.

  • 21. Smith S., Wang J., Fanning S., McMahon B.J.: Antimicrobial resistant bacteria in wild mammals and birds: a coincidence or cause of concern? Ir Vet J 2014, 67, 8, doi: 10.1186/2046-0481-67-8.

  • 22. Stedt J., Bonnedahl J., Hernandez J., McMahon B.J., Hasan B., Olsen B., Drobni M., Waldenström J.: Antibiotic resistance patterns in Escherichia coli from gulls in nine European countries. Infect Ecol Epidemiol 2014, 4, 10.3402/iee.v4.21565, doi: 10.3402/iee.v4.21565.

  • 23. Vredenburg J., Varela A.R., Hasan B., Bertilsson S., Olsen B., Narciso-da-Rocha C., Bonnedahl J., Stedt J., DaCosta P.M., Manaia C.M.: Quinolone-resistant Escherichia coli isolated from birds of prey in Portugal are genetically distinct from those isolated from water environments and gulls in Portugal, Spain and Sweden. Environ Microbiol 2014, 16, 995–1004, doi: 10.1111/1462-2920.12231.

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