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Antibiotic-Resistance Profile in Environmental Bacteria Isolated

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Antibiotic-Resistance Profile in Environmental Bacteria Isolated Environmental Microbiology (2009) 11(6), 1506–1517 doi:10.1111/j.1462-2920.2009.01878.x Antibiotic-resistance profile in environmental bacteria isolated from penicillin production wastewater treatment plant and the receiving riveremi_1878 1506..1517 Dong Li,1 Min Yang,1* Jianying Hu,2 Jing Zhang,1 belong to ESBL was detected in 17.3% and 11.0% of Ruyin Liu,1 Xin Gu,1 Yu Zhang1 and Zhenyu Wang1 strains isolated from wastewater and downstream 1State Key Laboratory of Environmental Aquatic river respectively. Class I integrons were detected in Chemistry, Research Center for Eco-Environmental 14% of wastewater isolates and 9.1% of downstream Sciences, Beijing 100085, China. isolates, and primarily contained gene cassettes con- 2College of Environmental Science, Peking University, ferring resistance to aminoglycoside antibiotics. The Beijing, China. unexpectedly high levels of multiple antibiotic resis- tance in strains from wastewater and downstream river were speculated to be mainly due to multidrug Summary efflux systems. The antibiotic-resistance characteristics of bacterial strains in antibiotic production wastewater treatment Introduction plants (WWTP) that contain high concentrations of antibiotics are unknown, as are the environmental There has been considerable concern regarding environ- effects of the discharge of wastewater from such ments containing antibiotics due to the possibility of facilities. In this study, 417 strains were individually antibiotic-resistant strains becoming dominant in the bac- isolated from the effluent of a WWTP that treated terial communities in such ecosystems (Guardabassi penicillin G production wastewater, as well as from et al., 1998; Aarestrup et al., 2002; Wittwer et al., 2005; downstream and upstream areas of the receiving Jindal et al., 2006; Heuer and Smalla, 2007). Until now, river. The minimum inhibition concentrations (MICs) most environmental investigations about antibiotic resis- of 18 antibiotics representing seven classes were tance have focused on stock farms, poultry farms, fish- then determined for each of these strains. Relatively eries, surface water, and lakes. The use of biological high similarity in the bacterial composition existed systems for the treatment of antibiotic production waste- between the wastewater and downstream river water creates a unique ecosystem that contains much samples when compared with the upstream sample. higher concentrations of antibiotics than normal aquatic High resistance ratios and MIC values were observed environments (Li et al., 2008), and thus may be an for almost all antibiotics in wastewater isolates, fol- important reservoir of antibiotic-resistant bacteria. Fur- lowed by strains from downstream river, of which the thermore, the treated wastewater is discharged into the resistance ratios and levels were still significantly receiving surface water, which might contribute to the higher than those of upstream strains. The resistance occurrence of antibiotic-resistant bacteria in downstream ratios and levels also significantly differed among river. However, to our knowledge, no systematic investi- strains belonged to different species in the penicillin gations have been performed about bacterial antibiotic production wastewater effluent and downstream resistance in such environments until now. In this study, river. In both samples, the resistances to b-lactam bacterial resistance characteristics were evaluated in antibiotics were more frequent, with much higher wastewater effluent from a biological system designed to levels, than the other class antibiotics. Then five treat penicillin G production wastewater from an antibi- clinically important resistant genes mainly coding otic production facility, as well as in the receiving river. for extended-spectrum b-lactamases (ESBLs) were The resistance profiles of bacteria in the upstream river determined for all strains, only blaTEM-1 which did not were also determined to evaluate the contribution of wastewater discharge to antibiotic resistance in the downstream river samples. Received 11 March, 2008; accepted 13 December, 2008. *For corre- spondence. E-mail [email protected]; Tel. +86-10-62923475; Meanwhile, most environmental investigations about Fax +86-10-62923541. antibiotic resistance have only included important © 2009 Society for Applied Microbiology and Blackwell Publishing Ltd Antibiotic resistance profile in environmental bacteria 1507 pathogens such as Escherichia coli (Hamelin et al., 2007), Results Enterococci (Aarestrup et al., 2002), Aeromonas spp. Characteristics of water samples (Huddleston et al., 2006) and Campylobacter (Wittwer et al., 2005). It should be noted that the majority of resistant Most of penicillin G was eliminated during the wastewa- bacteria in environments are indigenous species, which ter treatment processes. The concentration of penicillin constitute a reservoir that could contribute to the mainte- G was 153 Ϯ 4 mgl-1 in raw penicillin production waste- nance and spread of antibiotic-resistance genes to human water, and 1.68 Ϯ 0.48 mgl-1 in the wastewater effluent. pathogens through horizontal gene transfer facilitated by In the receiving river, the concentration decreased mobile genetic elements such as plasmids, transposons from 0.31 Ϯ 0.04 mgl-1 at the discharging point to under and integrons (Kruse and Sørum, 1994; Scott et al., 1997; the detection limit (0.03 mgl-1) at the downstream sam- Adams et al., 1998; Hamelin et al., 2007), especially in pling site (approximately 30 km from the discharge wastewater treatment plant (WWTP) environments (Szc- point). No penicillin G could be detected in the upstream zepanowski et al., 2004; Schlüter et al., 2007). The eluci- river samples. More detailed characteristics of the dation of antibiotic resistance characteristics of the whole wastewater and surface water such as pH, temperature, bacterial community is in need to assess bacterial resis- chemical oxygen demand (COD) and biochemical tance comprehensively. Thus, in this study, bacterial iso- oxygen demand for five days (BOD5) could be found lates were recovered from penicillin production wastewater elsewhere (Li et al., 2008). effluent and river water samples using non-selective Total cell counts were roughly 5.4 ¥ 107, 3.9 ¥ 107 and culture media, and then tested for susceptibility to 18 kinds 2.3 ¥ 106 cells ml-1 in the penicillin production wastewater of antimicrobial agents after identification. effluent, downstream river water and upstream river water As penicillin G was first discovered, several new genera- respectively. It seemed that the discharge of treated tions of b-lactam antibiotics have been developed, includ- wastewater resulted in an increased total count in down- ing penicillins, early cephalosporins, second- and third- stream river when compared with upstream river. Further- generation cephalosporins, b-lactam/b-lactamase inhibitor more, 6.8 ¥ 104, 5.3 ¥ 104 and 8.9 ¥ 103 cfu ml-1 were combinations, and carbapenems. All of these antibiotics individually obtained on Tryptic soy agar (TSA) for treated contain a core b-lactam ring, but have disparate side- penicillin production wastewater, downstream river and chains. b-Lactam antibiotics have become the agents most upstream river. The ratios of cfu versus total cell counts frequently used for the treatment of bacterial infections by ranged from 0.13% to 0.39%. inhibiting bacterial cell wall synthesis, whereas the b-lactam ring is susceptible to hydrolysis by b-lactamase Bacterial compositions enzymes produced by resistant bacteria (Livermore, 1995). To date, several hundred of b-lactamase have been A total of 179, 163 and 75 strains were individually iso- identified and classified into four groups based on molecu- lated from the penicillin production wastewater effluent, lar or functional characteristics (Bush et al., 1995; Jacoby, the downstream river and the upstream river water 2006). A large number of these enzymes are derivatives of samples. Following polymerase chain reaction (PCR) TEM, SHV and oxacillin (OXA) and so on, which are amplification and restriction fragment length polymor- important b-lactamase widely encountered in clinical phism (RFLP) grouping, 130, 106 and 23 representative therapy (Paterson and Bonomo, 2005). On the other hand, PCR products were sequenced, and most of the class I integrons have been commonly reported to contain sequences showed high similarities to known species. All antibiotic-resistance gene cassettes and associated with strains were identified to at least the genus level (Table 1), other mobile elements such as plasmids and transposons, and the majority of them belonged to glucose non- which could contribute to the spread of resistance genes fermenting gram-negative bacilli (Schreckenberger, (Agersø and Sandvang, 2005). Thus, all bacterial isolates 1995), with most of isolate species commonly encoun- in this study were examined for the occurrence of five tered in WWTPs and fresh water. Overall, 28, 30 and 10 clinically important b-lactamase determinants, as well as bacterial species or genera of unidentified species were for the presence of class I integrons to determine the isolated from wastewater effluent, downstream river and possible horizontal transfer of resistance genes. upstream river samples respectively. Wastewater and It should be noted that bacterial resistance to antibiotics downstream river water samples contained 12 common may also be intrinsic except for acquired. For example, species, while only one species was found in both the enterococci
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