Abstract
Environmental microbiology investigation was performed to determine the molecular diversity of β-lactamase genes among ampicillin-resistant bacteria from Jiaozhou Bay. β-lactamase genes were detected in 93.8% of the bacterial isolates identified as Enterobacteriaceae. The most frequently detected gene was bla TEM, followed by bla SHV, bla OAX-1, bla MOX and bla CMY. Most of the isolates (68.8%) were positive for the intI1 integrase gene, and two isolates were also found for the intI2 gene. The dfr and aadA gene cassettes were predominant. Anthropogenic contamination from onshore sewage processing plants might contribute predominantly to the β-lactamase gene reservoir in the studied coastal waters. Environmental antibiotic-resistant bacteria and resistance genes may serve as bioindicators of coastal environmental quality or biotracers of the potential contamination sources. This is the first report of the prevalence and characterization of β-lactamase genes and integrons in coastal Enterobacteriaceae from China.
Similar content being viewed by others
References
Alonso A, Sanchez P, Martinez JL (2001) Environmental selection of antibiotic resistance genes. Environ Microbiol 3:1–9. doi:10.1046/j.1462-2920.2001.00161.x
Alpay-Karaoglu S, Ozgumus OB, Sevim E, Kolayli F, Sevim A, Yesilgil P (2007) Investigation of antibiotic resistance profiles and TEM-type β-lactamase gene carriage of ampicillin-resistant Escherichia coli strains isolated from drinking water. Ann Microbiol 57:281–288
Altschul S, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W et al (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402. doi:10.1093/nar/25.17.3389
Alvarez M, Tran JH, Chow N, Jacoby GA (2004) Epidemiology of conjugative plasmid-mediated AmpC β-lactamases in the United States. Antimicrob Agents Chemother 48:533–537. doi:10.1128/AAC.48.2.533-537.2004
Barlow RS, Pemberton JM, Desmarchelier PM, Gobius KS (2004) Isolation and characterization of integron-containing bacteria without antibiotic selection. Antimicrob Agents Chemother 48:838–842. doi:10.1128/AAC.48.3.838-842.2004
Biyela PT, Lin J, Bezuidenhout CC (2004) The role of aquatic ecosystems as reservoirs of antibiotic resistant bacteria and antibiotic resistance genes. Water Sci Technol 50:45–50
Bonfiglio G, Perilli M, Stefani S, Amicosante G, Nicoletti G (2002) Prevalence of extended spectrum β-lactamases among Enterobacteriaceae: an Italian survey. Int J Antimicrob Agents 19:213–217. doi:10.1016/S0924-8579(01)00497-6
Bradford PA (2001) Extended-spectrum β-lactamase in the 21st century: characterization, epidemiology and detection of this important resistance threat. Clin Microbiol Rev 14:933–951. doi:10.1128/CMR.14.4.933-951.2001
Cabello FC (2006) Heavy use of prophylactic antibiotics in aquaculture: a growing problem for human and animal health and for the environment. Environ Microbiol 8:1137–1144. doi:10.1111/j.1462-2920.2006.01054.x
Cantón R, Novais A, Valverde A, Machado E, Peixe L, Baquero F et al (2008) Prevalence and spread of extended-spectrum β-lactamase-producing Enterobacteriaceae in Europe. Clin Microbiol Infect 14:144–153. doi:10.1111/j.1469-0691.2007.01850.x
Colom K, Pérez J, Alonso R, Fernández-Aranguiz A, Lariño E, Cisterna R (2003) Simple and reliable multiplex PCR assay for detection of bla TEM, bla SHV and bla OXA-1 genes in Enterobacteriaceae. FEMS Microbiol Lett 223:147–151. doi:10.1016/S0378-1097(03)00306-9
Costanzo SD, Murby J, Bates J (2005) Ecosystem response to antibiotics entering the aquatic environment. Mar Pollut Bull 51:218–223. doi:10.1016/j.marpolbul.2004.10.038
Dang HY, Lovell CR (2000) Bacterial primary colonization and early succession on surfaces in marine waters as determined by amplified rRNA gene restriction analysis and sequence analysis of 16S rRNA genes. Appl Environ Microbiol 66:467–475. doi:10.1128/AEM.66.2.467-475.2000
Dang H, Zhang X, Song L, Chang Y, Yang G (2007) Molecular determination of oxytetracycline resistant bacteria and their resistance genes from mariculture environments of China. J Appl Microbiol 103:2580–2592. doi:10.1111/j.1365-2672.2007.03494.x
Dang HY, Ren J, Song LS, Sun S, An LG (2008a) Diverse tetracycline resistant bacteria and resistance genes from coastal waters of Jiaozhou Bay. Microb Ecol 55:237–246. doi:10.1007/s00248-007-9271-9
Dang HY, Ren J, Song LS, Sun S, An LG (2008b) Dominant chloramphenicol-resistant bacteria and resistance genes in coastal marine waters of Jiaozhou Bay, China. World J Microbiol Biotechnol 24:209–217. doi:10.1007/s11274-007-9458-8
Felsenstein J (1989) PHYLIP—phylogeny inference package (version 3.2). Cladistics 5:164–166
French GL (2005) Clinical impact and relevance of antibiotic resistance. Adv Drug Deliv Rev 57:1514–1527. doi:10.1016/j.addr.2005.04.005
Goldstein C, Lee MD, Sanchez S, Hudson C, Philips B, Register B (2001) Incidence of class 1 and 2 integrases in clinical and commensal bacteria from livestock, companion animals, and exotics. Antimicrob Agents Chemother 45:723–726. doi:10.1128/AAC.45.3.723-726.2001
Henriques I, Moura A, Alves A, Saavedra MJ, Correia A (2006) Occurrence and diversity of integrons and β-lactamase genes among ampicillin-resistant isolates from estuarine waters. Res Microbiol 157:938–947. doi:10.1016/j.resmic.2006.09.003
Hong Y, Park H, Lee W, Song J, Jeong D (2005) Evaluation of phenotypic screening methods for detecting plasmid-mediated AmpC β-lactamases-producing isolates of Escherichia coli and Klebsiella pneumoniae. Diagn Microbiol Infect Dis 53:319–323. doi:10.1016/j.diagmicrobio.2005.07.004
Kim S, Aga DS (2007) Potential ecological and human health impacts of antibiotics and antibiotic-resistant bacteria from wastewater treatment plants. J Toxicol Environ Health B Crit Rev 10:559–573. doi:10.1080/15287390600975137
Kraft CA, Timbury MC, Platt DJ (1986) Distribution and genetic location of Tn7 in trimethoprim-resistant Escherichia coli. J Med Microbiol 22:125–131
Lee K, Lee M, Shin JH, Lee MH, Kang SH, Park AJ et al (2006) Prevalence of plasmid-mediated AmpC β-lactamases in Escherichia coli and Klebsiella pneumoniae in Korea. Microb Drug Resist 12:44–49. doi:10.1089/mdr.2006.12.44
Leverstein-van Hall MA, Blok HEM, Donders ART, Paauw A, Fluit AC, Verhoef J (2003) Multidrug resistance among Enterobacteriaceae is strongly associated with the presence of integrons and is independent of species or isolate origin. J Infect Dis 187:251–259. doi:10.1086/345880
Levesque C, Piche L, Larose C, Roy PH (1995) PCR mapping of integrons reveals several novel combinations of resistance genes. Antimicrob Agents Chemother 39:185–191
Lin J, Biyela PT (2005) Convergent acquisition of antibiotic resistance determinants amongst the Enterobacteriaceae isolates of the Mhlathuze River, KwaZulu-Natal (RSA). Water SA 31:257–260
Liu Z, Wei H, Liu G, Zhang J (2004) Simulation of water exchange in Jiaozhou Bay by average residence time approach. Estuar Coast Shelf Sci 61:25–35. doi:10.1016/j.ecss.2004.04.009
Liu SM, Zhang J, Chen HT, Zhang GS (2005) Factors influencing nutrient dynamics in the eutrophic Jiaozhou Bay, North China. Prog Oceanogr 66:66–85. doi:10.1016/j.pocean.2005.03.009
Mukherjee S, Chakraborty R (2006) Incidence of class 1 integrons in multiple antibiotic-resistant gram-negative copiotrophic bacteria from the River Torsa in India. Res Microbiol 157:220–226. doi:10.1016/j.resmic.2005.08.003
Nathisuwan S, Burgess DS, Lewis JS 2nd (2001) Extended-spectrum β-lactamases: epidemiology, detection, and treatment. Pharmacotherapy 21:920–928. doi:10.1592/phco.21.11.920.34529
Olsen JE (1999) Antibiotic resistance: genetic mechanisms and mobility. Acta Vet Scand Supp 92:15–22
Ozgumus OB, Celik-Sevim E, Alpay-Karaoglu S, Sandalli C, Sevim A (2007) Molecular characterization of antibiotic resistant Escherichia coli strains isolated from tap and spring waters in a coastal region in Turkey. J Microbiol 45:379–387
Pfaller MA, Segreti J (2006) Overview of the epidemiological profile and laboratory detection of extended-spectrum β-lactamases. Clin Infect Dis 42:S153–S163. doi:10.1086/500662
Philippon A, Arlet G, Jacoby GA (2002) Plasmid-determined AmpC type β-lactamases. Antimicrob Agents Chemother 46:1–11. doi:10.1128/AAC.46.1.1-11.2002
Ploy MC, Lambert T, Couty JP, Denis F (2000) Integrons: an antibiotic resistance gene capture and expression system. Clin Chem Lab Med 38:483–487. doi:10.1515/CCLM.2000.070
Roe MT, Vega E, Pillai SD (2003) Antimicrobial resistance markers of class 1 and class 2 integron-bearing Escherichia coli from irrigation waters and sediments. Emerg Infect Dis 9:822–826
Rosser SJ, Young HK (1999) Identification and characterization of class 1 integrons in bacteria from an aquatic environment. J Antimicrob Chemother 44:8–11. doi:10.1093/jac/44.1.11
Rupp ME, Fey PD (2003) Extended spectrum β-lactamase (ESBL)-producing Enterobacteriaceae: considerations for diagnosis, prevention and drug treatment. Drugs 63:353–365. doi:10.2165/00003495-200363040-00002
Schwartz T, Kohnen W, Janses B, Obst U (2003) Detection of antibiotic-resistant bacteria and their resistance genes in wastewater, surface water, and drinking water biofilms. FEMS Microbiol Ecol 43:325–335. doi:10.1111/j.1574-6941.2003.tb01073.x
Shah AA, Hasan F, Ahmed S, Hameed A (2004) Extended-spectrum β-lactamases (ESBLs): characterization, epidemiology and detection. Crit Rev Microbiol 30:25–32. doi:10.1080/10408410490266429
Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 9:3251–3270
Villegas MV, Kattan JN, Quinteros MG, Casellas JM (2008) Prevalence of extended-spectrum β-lactamases in South America. Clin Microbiol Infect 14:154–158. doi:10.1111/j.1469-0691.2007.01869.x
Walther-Rasmussen J, Hoiby N (2002) Plasmid-borne AmpC β-lactamases. Can J Microbiol 48:479–493. doi:10.1139/w02-039
Weldhagen GF (2004) Integrons and β-lactamases—a novel perspective on resistance. Int J Antimicrob Agents 23:556–562. doi:10.1016/j.ijantimicag.2004.03.007
White DG, McDermott PF (2001) Biocides, drug resistance and microbial evolution. Curr Opin Microbiol 4:313–317. doi:10.1016/S1369-5274(00)00209-5
White PA, MacIver CJ, Rawlinson WD (2001) Integrons and gene cassettes in the Enterobacteriaceae. Antimicrob Agents Chemother 45:2658–2661. doi:10.1128/AAC.45.9.2658-2661.2001
Yao F, Qian YS, Chen SZ, Wang PF, Huan YC (2007) Incidence of extended-spectrum β-lactamases and characterization of integrons in extended-spectrum β-lactamase-producing Klebsiella pneumoniae isolated in Shantou, China. Acta Biochim Biophys Sin (Shanghai) 39:527–532. doi:10.1111/j.1745-7270.2007.00304.x
Young HK (1993) Antimicrobial resistance spread in aquatic environments. J Antimicrob Chemother 31:627–635. doi:10.1093/jac/31.5.627
Acknowledgements
This work was financially supported by the National Natural Science Foundation of China grants (NSFC Grant Nos. 40576069 and 40476058), the Hi-Tech Research and Development Program of China grant 2007AA091903, the China Ocean Mineral Resources R&D Association grants DYXM-115-02-2-6 and DYXM-115-02-2-20.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Wang, C., Dang, H. & Ding, Y. Incidence of diverse integrons and β-lactamase genes in environmental Enterobacteriaceae isolates from Jiaozhou Bay, China. World J Microbiol Biotechnol 24, 2889–2896 (2008). https://doi.org/10.1007/s11274-008-9827-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11274-008-9827-y