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Soil Antibiotics and Transfer of Antibiotic Resistance Genes Affecting Wildlife

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Book cover Antibiotics and Antibiotics Resistance Genes in Soils

Part of the book series: Soil Biology ((SOILBIOL,volume 51))

Abstract

Antibiotics are used in large quantities both in human and veterinary medicine. Due to incomplete metabolism, antibiotics are released and spread into the terrestrial environment. The application of manure in the agricultural fields is the leading cause of the antibiotic spread in soils. Depending on the structural characteristics of each class of antibiotic, they can be adsorbed and fixated on soils with different strengths and may remain there for a long period of time. Repeated use of manure containing antibiotics and resistant bacteria affects the soil microbial communities in various aspects, including the development of antibiotic resistant bacteria due to selective pressure and horizontal gene transfer. Different bacterial species harbor distinct resistance genes, and they were found in humans and domestic animals. These resistance genes were also found in wild animals which had no apparent contact with antibiotics. However, the soil antibiotics may have had spread the resistance genes through different ecological niches reaching the wild animals.

The original version of this chapter was revised. An erratum to this chapter can be found at DOI 10.1007/978-3-319-66260-2_22.

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References

  • Alder AC, McArdell CS, Golet EM, Ibric S, Molnar E, Nipales NS, Giger W (2001) Occurrence and fate of fluoroquinolone, macrolide, and sulfonamide antibiotics during wastewater treatment and in ambient waters in Switzerland. In: Daughton CG, Jones-Lepp T (eds) Pharmaceuticals and personal care products in the environment: scientific and regulatory issues. American Chemical Society, Washington, DC, pp 56–69

    Chapter  Google Scholar 

  • Allen HK, Donato J, Wang HH, Cloud-Hansen KA, Davies J, Handelsman J (2010) Call of the wild: antibiotic resistance genes in natural environments. Nat Rev Microbiol 8:251–259

    Article  CAS  PubMed  Google Scholar 

  • Araújo C, Torres C, Silva N, Carneiro C, Gonçalves A, Radhouani H, Correia S, da Costa PM, Paccheco R, Zarazaga M, Ruiz-Larrea F, Poeta P, Igrejas G (2010) Vancomycin-resistant enterococci from Portuguese wastewater treatment plants. J Basic Microbiol 50(6):605–609

    Article  PubMed  Google Scholar 

  • Barrett JR (2012) Preventing antibiotic resistance in the wild: a new end point for environmental risk assessment. Environ Health Perspect 120:a321

    Article  PubMed  PubMed Central  Google Scholar 

  • Beers MH (2006) The Merck manual of diagnosis and therapy, 18th edn. Merck, Whitehouse Station, NJ

    Google Scholar 

  • Bound JP, Voulvoulis M (2004) Pharmaceuticals in the aquatic environment—a comparison of risk assessment strategies. Chemosphere 56:1143–1155

    Article  CAS  PubMed  Google Scholar 

  • Boxall ABA, Blackwell P, Cavallo R, Kay P, Tolls J (2002) The sorption and transport of a sulphonamide antibiotic in soil systems. Toxicol Lett 131:19–28

    Article  CAS  PubMed  Google Scholar 

  • Boxall ABA, Kolpin DW, Halling-Sørensen B, Tolls J (2003) Are veterinary medicines causing environmental risks? Environ Sci Technol 37:286–294

    Article  Google Scholar 

  • Boxall AB, Fogg LA, Blackwell PA, Kay P, Pemberton EJ, Croxford A (2004) Veterinary medicines in the environment. Rev Environ Contam Toxicol 180:1–91

    CAS  PubMed  Google Scholar 

  • Cabrita J, Rodrigues J, Braganca F, Morgado C, Pires I, Goncalves AP (1992) Prevalence, biotypes, plasmid profile and antimicrobial resistance of Campylobacter isolated from wild and domestic animals from northeast Portugal. J Appl Bacteriol 73:279–285

    Article  CAS  PubMed  Google Scholar 

  • Christian T, Schneider R, Farber HA, Skutlarek D, Meyer MT, Goldbach HE (2003) Determination of antibiotic residues in manure, soil, and surface waters. Acta Hydrochim Hydrobiol 31:36–44

    Article  CAS  Google Scholar 

  • Cole D, Drum DJ, Stalknecht DE, White DG, Lee MD, Ayers S, Sobsey M, Maurer JJ (2005) Free-living Canada geese and antimicrobial resistance. Emerg Infect Dis 11:935–938

    Article  PubMed  PubMed Central  Google Scholar 

  • Daghrir R, Drogui P (2013) Tetracycline antibiotics in the environment: a review. Environ Chem Lett 11:209–227

    Article  CAS  Google Scholar 

  • Ding C, He J (2010) Effect of antibiotics in the environment on microbial populations. Appl Microbiol Biotechnol 87:925–941

    Article  CAS  PubMed  Google Scholar 

  • Ding GC, Radl V, Schloter-Hai B, Jechalke S, Heuer H, Smalla K, Schloter M (2014) Dynamics of soil bacterial communities in response to repeated application of manure containing sulfadiazine. PLoS One 9(3):e92958

    Article  PubMed  PubMed Central  Google Scholar 

  • Dojmi di Delupis G, Macri A, Civitareale C, Migliore L (1992) Antibiotics of zootechnical use: effects of high and low dose contamination on Daphnia magna. Aquat Toxicol 22:53–60

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Doretto KM, Rath S (2013) Sorption of sulfadiazine on Brazilian soils. Chemosphere 90:2027–2034

    Article  CAS  PubMed  Google Scholar 

  • Esiobu N, Armenta L, Ike J (2002) Antibiotic resistance in soil and water environments. Environ Health Res 12:133–144

    Article  Google Scholar 

  • Gillings MR (2013) Evolutionary consequences of antibiotic use for the resistome, mobilome and microbial pangenome. Front Microbiol 4:4

    Article  PubMed  PubMed Central  Google Scholar 

  • Gilliver MA, Bennett M, Begon M, Hazel SM, Hart CA (1999) Antibiotic resistance found in wild rodents. Nature 401:233–234

    Article  CAS  PubMed  Google Scholar 

  • Guenther S, Ewers C, Wieler LH (2011) Extended-spectrum beta-lactamases producing E. coli in wildlife, yet another form of environmental pollution? Front Microbiol 2:246

    Article  PubMed  PubMed Central  Google Scholar 

  • Halling-Sùrensen B, Nielsen SN, Lanzky PF, Ingerslev F, HoltenLützhùft HC, Jùrgensen SE (1998) Occurrence, fate and effects of pharmaceutical substances in the environment—a review. Chemosphere 36:357–393

    Article  Google Scholar 

  • Hammesfahr U, Heuer H, Manzke B, Smalla K, Thiele-Bruhn S (2008) Impact of the antibiotic sulfadiazine and pig manure on the microbial community structure in agricultural soils. Soil Biol Biochem 40:1583–1591

    Article  CAS  Google Scholar 

  • Heuer H, Focks A, Lamshöft M, Smalla K, Matthies M, Spiteller M (2008) Fate of sulfadiazine administered to pigs and its quantitative effect on the dynamics of bacterial resistance genes in manure and manured soil. Soil Biol Biochem 40:1892–1900

    Article  CAS  Google Scholar 

  • Hu X, Zhou Q, Luo Y (2010) Occurrence and source analysis of typical veterinary antibiotics in manure, soil, vegetables and groundwater from organic vegetable bases, northern China. Environ Pollut 158:2992–2998

    Article  CAS  PubMed  Google Scholar 

  • Hughes VM, Datta N (1983) Conjugative plasmids in bacteria of the ‘pre-antibiotic’ era. Nature 302:725–726

    Article  CAS  PubMed  Google Scholar 

  • Jechalke S, Heuer H, Siemens J, Amelung W, Smalla K (2014) Fate and effects of veterinary antibiotics in soil. Trends Microbiol 22:536–545

    Article  CAS  PubMed  Google Scholar 

  • Kahn CM, Line S (2005) Merck veterinary manual, 9th edn. Merck, Whitehouse Station, NJ

    Google Scholar 

  • Katz JM, Katz SE (1983) Microbial assay systems for determining antibiotic residues in soils. J Assoc Anal Chem 66:640–645

    CAS  Google Scholar 

  • Kay P, Blackwell PA, Boxall ABA (2003) Fate of veterinary antibiotics in a macroporous tile drained clay soil. Environ Toxicol Chem 23(5):1136–1144

    Article  Google Scholar 

  • Kim S, Carlson K (2007) Temporal and spatial trends in the occurrence of human and veterinary antibiotics in aqueous and river sediment matrices. Environ Sci Technol 41:50–57

    Article  CAS  PubMed  Google Scholar 

  • Kim KR, Owens G, Kwon S, So K, Lee D, Ok YS (2011) Occurrence and environmental fate of veterinary antibiotics in the terrestrial environment. Water Air Soil Pollut 214:163–174

    Article  CAS  Google Scholar 

  • Kolz AC, Moorman TB, Ong SK, Scoggin KD, Douglass EA (2005) Degradation and metabolite production of tylosin in anaerobic and aerobic swine-manure lagoons. Water Environ Res 77:49–56

    Article  CAS  PubMed  Google Scholar 

  • Kozak GK, Boerlin P, Janecko N, Reid-Smith RJ, Jardine C (2009) Antimicrobial resistance in Escherichia coli isolates from swine and wild small mammals in the proximity of swine farms and in natural environments in Ontario, Canada. Appl Environ Microbiol 75:559–566

    Article  CAS  PubMed  Google Scholar 

  • Landers TF, Cohen B, Wittum TE, Larson EL (2012) A review of antibiotic use in food animals: perspective, policy, and potential. Public Health Rep 127:4–22

    Article  PubMed  PubMed Central  Google Scholar 

  • Lanhammer JP (1989) Untursuchungen zum Verbleib antimikrobiell wirksamer Aezneistoffe als in Gulle und im landwirtschaftlichen Umfeld. PhD dissertation, Universität Bonn, Germany, p 138

    Google Scholar 

  • Le-Minh N, Khan SJ, Drewes JE, Stuetz RM (2010) Fate of antibiotics during municipal water recycling treatment processes. Water Res 44:4295–4323

    Article  CAS  PubMed  Google Scholar 

  • Mallon DJ, Corkill JE, Hazel SM, Wilson JS, French NP, Bennett M, Hart CA (2002) Excretion of vancomycin-resistant enterococci by wild mammals. Emerg Infect Dis 8:636–638

    Article  PubMed  PubMed Central  Google Scholar 

  • Martinez JL (2012) Natural antibiotic resistance and contamination by antibiotic resistance determinants: the two ages in the evolution of resistance to antimicrobials. Front Microbiol 3:1

    Article  PubMed  PubMed Central  Google Scholar 

  • Midtvedt T (2001) Antibiotics in the Environment: zinc bacitracin ± environmental toxicity and breakdown. In: Kümmerer K (ed) Pharmaceuticals in the environment: sources, fate, effects and risks. Springer, Berlin, pp 77–79

    Chapter  Google Scholar 

  • Mitscher LA (1978) The chemistry of the tetracycline antibiotics. Marcel Dekker, Basel, p 330

    Google Scholar 

  • Nwosu V (2001) Antibiotic resistance with particular reference to soil microorganisms. Res Microbiol 152:421–430

    Article  CAS  PubMed  Google Scholar 

  • O’Brien TF (2002) Emergence, spread, and environmental effect of antimicrobial resistance: how use of an antimicrobial anywhere can increase resistance to any antimicrobial anywhere else. Clin Infect Dis 34(3):S78–S84

    Article  PubMed  Google Scholar 

  • Osterblad M, Norrdahl K, Korpimaki E, Huovinen P (2001) Antibiotic resistance. How wild are wild mammals? Nature 409:37–38

    Article  CAS  PubMed  Google Scholar 

  • Pallecchi L, Bartoloni A, Paradisi F, Rossolini GM (2008) Antibiotic resistance in the absence of antimicrobial use: mechanisms and implications. Expert Rev Anti Infect Ther 6:725–732

    Article  PubMed  Google Scholar 

  • Poeta P, Costa D, Igrejas G, Rodrigues J, Torres C (2007) Phenotypic and genotypic characterization of antimicrobial resistance in faecal enterococci from wild boars (Susscrofa). Vet Microbiol 125:368–374

    Article  CAS  PubMed  Google Scholar 

  • Poirel L, Kampfer P, Nordmann P (2002) Chromosome-encoded Ambler class A beta-lactamase of Kluyverageorgiana, a probable progenitor of a subgroup of CTX-M extended-spectrum beta-lactamases. Antimicrob Agents Chemother 46:4038–4040

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Poulsen PHB, Al-Soud W, Bergmark K, Magid J, Hansen LH, Sørensen SJ (2013) Effects of fertilization with urban and agricultural organic wastes in a field trial—prokaryotic diversity investigated by pyrosequencing. Soil Biol Biochem 57:784–793

    Article  CAS  Google Scholar 

  • Radhouani H, Poeta P, Igrejas G, Gonçalves A, Vinué L, Torres C (2009) Antimicrobial resistance and phylogenetic groups in isolates of Escherichia coli from seagulls at the Berlengas nature reserve. Vet Rec 165:138–142

    Article  CAS  PubMed  Google Scholar 

  • Radhouani H, Igrejas G, Pinto L, Gonçalves A, Coelho C, Rodrigues J, Poeta P (2011) Molecular characterization of antibiotic resistance in enterococci recovered from seagulls (Larus cachinnans) representing an environmental health problem. J Environ Monitor 13:2227–2233

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Samuelsen OB (1994) Simultaneous determination of ormethoprim and sulphadimethoxine in plasma and muscle of Atlantic salmon (Salmo salar). J Chromatogr B 660:412–417

    Article  CAS  Google Scholar 

  • Sarmah AK, Meyer MT, Boxall AB (2006) A global perspective on the use, sales, exposure pathways, occurrence, fate and effects of veterinary antibiotics (VAs) in the environment. Chemosphere 65:725–759

    Article  CAS  PubMed  Google Scholar 

  • Silva N, Felgar A, Goncalves A, Correia S, Pacheco R, Araujo C, Igrejas G, Poeta P (2010) Absence of extended-spectrum-beta-lactamase-producing Escherichia coli isolates in migratory birds: song thrush (Turdus philomelos). J Antimicrob Chemother 65:1306–1307

    Article  CAS  PubMed  Google Scholar 

  • Silva N, Igrejas G, Rodrigues P, Rodrigues T, Gonçalves A, Felgar AC, Pacheco R, Gonçalves D, Cunha R, Poeta P (2011) Molecular characterization of vancomycin-resistant enterococci and extended-spectrum beta-lactamase-containing Escherichia coli isolates in wild birds from the Azores Archipelago. Avian Pathol 40:473–479

    Article  CAS  PubMed  Google Scholar 

  • Stokes HW, Gillings MR (2011) Gene flow, mobile genetic elements and the recruitment of antibiotic resistance genes into Gram-negative pathogens. FEMS Microbiol Rev 35:790–819

    Article  CAS  PubMed  Google Scholar 

  • Tasho RP, Cho JY (2016) Veterinary antibiotics in animal waste, its distribution in soil and uptake by plants: a review. Sci Total Environ 563–564:366–376

    Article  PubMed  Google Scholar 

  • Thiele-Bruhn S (2003) Pharmaceutical antibiotic compounds in soils—a review. J Plant Nutr Soil Sci 166:145–167

    Article  CAS  Google Scholar 

  • Udikovic-Kolica N, Wichmanna F, Brodericka NA, Handelsmana J (2014) Bloom of resident antibiotic-resistant bacteria in soil following manure fertilization. PNAS 111:42

    Google Scholar 

  • Uhrich SRW, Navarro DA, Zimmerman L, Aga DS (2014) Assessing antibiotic sorption in soil: a literature review and new case studies on sulfonamides and macrolides. Chem Cent J 8:1–12

    Article  Google Scholar 

  • Wang M, Tang JC (2010) Research of antibiotics pollution in soil environments and its ecological toxicity. J Agro Environ Sci 29:261–266

    Google Scholar 

  • World Health Organization (2014) Antimicrobial resistance: global report on surveillance

    Google Scholar 

  • Wright GD (2010) Antibiotic resistance in the environment: a link to the clinic? Curr Opin Microbiol 13:589–594

    Article  CAS  PubMed  Google Scholar 

  • Xi C, Zhang Y, Marrs CF, Ye W, Simon C, Foxman B (2009) Prevalence of antibiotic resistance in drinking water treatment and distribution systems. Appl Environ Microbiol 75:5714–5718

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhou Q, Zhang MC, Shuang CD, Li ZQ, Li AM (2012) Preparation of a novel magnetic powder resin for the rapid removal of tetracycline in the aquatic environment. Chin Chem Lett 23:745–748

    Article  CAS  Google Scholar 

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Silva, V., Carvalho, I., Igrejas, G., Poeta, P. (2017). Soil Antibiotics and Transfer of Antibiotic Resistance Genes Affecting Wildlife. In: Hashmi, M., Strezov, V., Varma, A. (eds) Antibiotics and Antibiotics Resistance Genes in Soils. Soil Biology, vol 51. Springer, Cham. https://doi.org/10.1007/978-3-319-66260-2_16

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