Abstract
Antibiotics are successful drugs used in human and animal therapy; however, they must be considered as environmental pollutants. This study aims to isolate and characterize the extended-spectrum β-lactamase (ESBL) producing Escherichia coli soil from Azores Archipelago subjected to livestock agricultural practices. Twenty-four soil samples were collected from three different pasture systems with different number of cattle heads, and from a control site. Antibiotic susceptibility method was performed by Kirby–Bauer disk diffusion method against 16 antibiotics, and the presence of genes encoding lactamases, antimicrobial resistance genes, virulence factors, and phylogenetic groups was determined by polymerase chain reaction (PCR). Nine ESBLs were recovered from the three grazing sites, and all isolates presented the beta-lactamase genes blaCTX-M-3 and blaSHV. E. coli isolates were resistance to tetracycline and streptomycin and harbored the tetB, strA, and strB genes. One isolate also showed resistance to sulfonamides, and the genes sul1 and sul2 were detected. The isolates were grouped into the following phylogenic groups: B1 (n = 6), D (n = 2), and A (n = 1). The presence of antibiotics and resistance genes in soils may be the source to the development of antimicrobial resistance, which may have negative consequences in human and animal health.
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References
Ben Said L, Jouini A, Klibi N, Dziri R, Alonso CA, Boudabous A, Ben Slama K, Torres C (2015) Detection of extended-spectrum beta-lactamase (ESBL)-producing Enterobacteriaceae in vegetables, soil and water of the farm environment in Tunisia. Int J Food Microbiol 203:86–92. https://doi.org/10.1016/j.ijfoodmicro.2015.02.023
Berendsen BJA, Wegh RS, Memelink J, Zuidema T, Stolker LAM (2015) The analysis of animal faeces as a tool to monitor antibiotic usage. Talanta 132:258–268. https://doi.org/10.1016/j.talanta.2014.09.022
Blaak H, van Hoek AHAM, Hamidjaja RA, van der Plaats RQJ, Kerkhof-de Heer L, de Roda Husman AM, Schets FM (2015) Distribution, numbers, and diversity of ESBL-producing E. coli in the poultry farm environment. PLoS One 10:e0135402
Bonnedahl J, Stedt J, Waldenström J, Svensson L, Drobni M, Olsen B (2015) Comparison of extended-spectrum β-lactamase (ESBL) CTX-M genotypes in Franklin Gulls from Canada and Chile. PLoS One 10:e0141315
Boulianne M, Arsenault J, Daignault D, Archambault M, Letellier A, Dutil L (2016) Drug use and antimicrobial resistance among Escherichia coli and Enterococcus spp. isolates from chicken and Turkey flocks slaughtered in Quebec, Canada. Can J Vet Res 80:49–59
Bulycheva EV, Korotkova EI, Voronova OA, Kustova AA, Petrova EV (2014) Fluorescence analysis of E. coli bacteria in water. Procedia Chem 10:179–183. https://doi.org/10.1016/j.proche.2014.10.031
Campos J, Mourão J, Pestana N, Peixe L, Novais C, Antunes P (2013) Microbiological quality of ready-to-eat salads: an underestimated vehicle of bacteria and clinically relevant antibiotic resistance genes. Int J Food Microbiol 166:464–470. https://doi.org/10.1016/j.ijfoodmicro.2013.08.005
Carvalho I, Del Campo R, Sousa M, Silva N, Carrola J, Marinho C, Santos T, Carvalho S, Nóvoa M, Quaresma M, Pereira JE, Cobo M, Igrejas G, Poeta P (2017) Antimicrobial-resistant Escherichia coli and Enterococcus spp. isolated from Miranda donkey (Equus asinus): an old problem from a new source with a different approach. J Med Microbiol 66:191–202. https://doi.org/10.1099/jmm.0.000423
CLSI (2017) Clinical and laboratory standards institute. Performance standards for antimicrobial susceptibility testing. Clinical and Laboratory Standards Institute, Wayne
Costa D, Vinué L, Poeta P, Coelho AC, Matos M, Sáenz Y, Somalo S, Zarazaga M, Rodrigues J, Torres C (2009) Prevalence of extended-spectrum beta-lactamase-producing Escherichia coli isolates in faecal samples of broilers. Vet Microbiol 138:339–344. https://doi.org/10.1016/j.vetmic.2009.03.029
Fouhy F, Stanton C, Cotter PD, Hill C, Walsh F (2015) Proteomics as the final step in the functional metagenomics study of antimicrobial resistance. Front Microbiol 6:172. https://doi.org/10.3389/fmicb.2015.00172
Gao L, Hu J, Zhang X, Wei L, Li S, Miao Z, Chai T (2015) Application of swine manure on agricultural fields contributes to extended- spectrum ß-lactamase producing Escherichia coli spread in Tai’an, China. Front Microbiol 6. https://doi.org/10.3389/fmicb.2015.00313
Gonçalves A, Igrejas G, Radhouani H, Estepa V, Alcaide E, Zorrilla I, Serra R, Torres C, Poeta P (2011) Detection of extended-spectrum beta-lactamase-producing Escherichia coli isolates in faecal samples of Iberian lynx. Lett Appl Microbiol 54:73–77. https://doi.org/10.1111/j.1472-765X.2011.03173.x
Gonçalves A, Igrejas G, Radhouani H, Santos T, Monteiro R, Pacheco R, Alcaide E, Zorrilla I, Serra R, Torres C, Poeta P (2013) Detection of antibiotic resistant enterococci and Escherichia coli in free range Iberian Lynx (Lynx pardinus). Sci Total Environ 456–457:115–119. https://doi.org/10.1016/j.scitotenv.2013.03.073
Gothwal R, Shashidhar T (2015) Antibiotic pollution in the environment: a review. Clean (Weinh) 43:463–620. https://doi.org/10.1002/clen.201300989
Guerrero-Ramos E, Cordero J, Molina-González D, Poeta P, Igrejas G, Alonso-Calleja C, Capita R (2016) Antimicrobial resistance and virulence genes in enterococci from wild game meat in Spain. Food Microbiol 53:156–164. https://doi.org/10.1016/j.fm.2015.09.007
Hartmann A, Amoureux L, Locatelli A, Depret G, Jolivet C, Gueneau E, Neuwirth C (2012) Occurrence of CTX-M producing Escherichia coli in soils, cattle, and farm environment in France (Burgundy Region). Front Microbiol 3:83
Heuer H, Schmitt H, Smalla K (2011) Antibiotic resistance gene spread due to manure application on agricultural fields. Curr Opin Microbiol 14:236–243. https://doi.org/10.1016/j.mib.2011.04.009
Hosseini A, Azari AA, Danesh A (2016) Prevalence of extended-spectrum ß-lactamase-producing Escherichia coli in agricultural fields of Gorgan district using bovine manure. IJMM 6:687–692
Ji X, Shen Q, Liu F, Ma J, Xu G, Wang Y, Wu M (2012) Antibiotic resistance gene abundances associated with antibiotics and heavy metals in animal manures and agricultural soils adjacent to feedlots in Shanghai, China. J Hazard Mater 235–236:178–185. https://doi.org/10.1016/j.jhazmat.2012.07.040
Jones-Dias D, Manageiro V, Caniça M (2015) Influence of agricultural practice on mobile bla genes: IncI1-bearing CTX-M, SHV, CMY and TEM in Escherichia coli from intensive farming soils. Environ Microbiol 18:260–272. https://doi.org/10.1111/1462-2920.13021
Kyselková M, Kotrbová L, Bhumibhamon G, Chroňáková A, Jirout J, Vrchotová N, Schmitt H, Elhottová D (2015) Tetracycline resistance genes persist in soil amended with cattle feces independently from chlortetracycline selection pressure. Soil Biol Biochem 81:259–265. https://doi.org/10.1016/j.soilbio.2014.11.018
Lau MM, Ingham SC (2001) Survival of faecal indicator bacteria in bovine manure incorporated into soil. Lett Appl Microbiol 33:131–136. https://doi.org/10.1046/j.1472-765x.2001.00962.x
Marinho C, Igrejas G, Gonçalves A, Silva N, Santos T, Monteiro R, Gonçalves D, Rodrigues T, Poeta P (2014) Azorean wild rabbits as reservoirs of antimicrobial resistant Escherichia coli. Anaerobe 30:116–119. https://doi.org/10.1016/j.anaerobe.2014.09.009
Peng S, Zhou B, Wang Y, Lin X, Wang H, Qiu C (2016) Bacteria play a more important role than nutrients in the accumulation of tetracycline resistance in manure-treated soil. Biol Fertil Soils 52:655–663. https://doi.org/10.1007/s00374-016-1105-9
Queenan AM, Foleno B, Gownley C, Wira E, Bush K (2004) Effects of ioculum and β-lactamase activity in AmpC- and extended-spectrum β-lactamase (ESBL)-producing Escherichia coli and Klebsiella pneumoniae clinical isolates tested by using NCCLS ESBL methodology. J Clin Microbiol 42:269 LP–269275
Radhouani H, Igrejas G, Gonçalves A, Estepa V, Sargo R, Torres C, Poeta P (2013) Molecular characterization of extended-spectrum-beta-lactamase-producing Escherichia coli isolates from red foxes in Portugal. Arch Microbiol 195:141–144. https://doi.org/10.1007/s00203-012-0853-7
Radhouani H, Poeta P, Igrejas G, Goncalves A, Vinue 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. https://doi.org/10.1136/vr.165.5.138
Rebbah N, Messai Y, Châtre P, Haenni M, Madec JY, Bakour R (2017) Diversity of CTX-M extended-spectrum β-lactamases in Escherichia coli isolates from retail raw ground beef: first report of CTX-M-24 and CTX-M-32 in Algeria. Microb Drug Resist 24:896–908. https://doi.org/10.1089/mdr.2017.0171
Reinthaler FF, Feierl G, Galler H, Haas D, Leitner E, Mascher F, Melkes A, Posch J, Winter I, Zarfel G, Marth E (2010) ESBL-producing E. coli in Austrian sewage sludge. Water Res 44:1981–1985. https://doi.org/10.1016/j.watres.2009.11.052
Santman-Berends IMGA, Gonggrijp MA, Hage JJ, Heuvelink AE, Velthuis A, Lam TJGM, van Schaik G (2017) Prevalence and risk factors for extended-spectrum β-lactamase or AmpC-producing Escherichia coli in organic dairy herds in the Netherlands. J Dairy Sci 100:562–571. https://doi.org/10.3168/jds.2016-11839
Santos T, Silva N, Igrejas G, Rodrigues P, Micael J, Rodrigues T, Resendes R, Gonçalves A, Marinho C, Gonçalves D, Cunha R, Poeta P (2013) Dissemination of antibiotic resistant Enterococcus spp. and Escherichia coli from wild birds of Azores Archipelago. Anaerobe 24:25–31. https://doi.org/10.1016/j.anaerobe.2013.09.004
Silva N, Igrejas G, Gonçalves A, Poeta P (2012) Commensal gut bacteria: distribution of Enterococcus species and prevalence of Escherichia coli phylogenetic groups in animals and humans in Portugal. Ann Microbiol. 62:449–459. https://doi.org/10.1007/s13213-011-0308-4
Silva V, Peixoto F, Igrejas G, Parelho C, Garcia P, Carvalho I, Sousa M, Pereira JE, Rodrigues A, Poeta PACQD (2018) First report on vanA-Enterococcus faecalis recovered from soils subjected to long-term livestock agricultural practices in Azores Archipelago. IJER 12:39–44. https://doi.org/10.1007/s41742-018-0068-0
Srinivasan V, Nam H-M, Sawant AA, Headrick SI, Nguyen LT, Oliver SP (2008) Distribution of tetracycline and streptomycin resistance genes and class 1 Integrons in Enterobacteriaceae isolated from dairy and nondairy farm soils. Microb Ecol 55:184–193. https://doi.org/10.1007/s00248-007-9266-6
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. https://doi.org/10.1111/j.1574-6976.2011.00273.x
Tang Q, Song P, Li J, Kong F, Sun L, Xu L (2016) Control of antibiotic resistance in China must not be delayed: the current state of resistance and policy suggestions for the government, medical facilities, and patients. Biosci Trends 10:1–6. https://doi.org/10.5582/bst.2016.01034
Zheng B, Huang C, Xu H, Guo L, Zhang J, Wang X, Jiang X, Yu X, Jin L, Li X, Feng Y, Xiao Y, Li L (2017) Occurrence and genomic characterization of ESBL-producing, MCR-1-harboring Escherichia coli in farming soil. Front Microbiol 8:2510. https://doi.org/10.3389/fmicb.2017.02510
Funding
This work was supported by the Associate Laboratory for Green Chemistry- LAQV which is financed by national funds from FCT/MCTES (UID/QUI/50006/2020). Vanessa Silva received a PhD grant from FCT (Fundação para a Ciência e Tecnologia) (SFRH/BD/137947/2018).
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Silva, V., Peixoto, F., Parelho, C. et al. Occurrence of ESBL-producing Escherichia coli in soils subjected to livestock grazing in Azores archipelago: an environment-health pollution issue?. Int Microbiol 23, 619–624 (2020). https://doi.org/10.1007/s10123-020-00134-0
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DOI: https://doi.org/10.1007/s10123-020-00134-0