Occurrence of antibiotic resistance and integronase genes in Taihu Lake

Authors

  • Jian Wang Wang
  • Haiqing Pu
  • Lin Ye
  • Liangyan Chen
  • Xuxiang Zhang

DOI:

https://doi.org/10.18063/AEB.2016.01.006.

Keywords:

antibiotic resistance genes, class 1 integrons, fecal coliforms, Taihu Lake, water environment

Abstract

Antibiotic resistance genes (ARGs), a potential threat to the health of humans and animals, have been widely detected in various environments. However, not much information about ARGs in freshwater lakes have been recorded. In this study, we investigated the occurrence of 17 kinds of ARGs and three types of integronase genes in Taihu Lake (China), an important drinking water source for local residents. Fecal coliforms were also isolated from the water and sediments for antimicrobial susceptibility tests and related ARGs detection. Results showed that tetracycline resistance gene tetC, sulfanilamide resistance genes sul1 and sul2, and class 1 integronase gene int1 were present in all water and sediment samples. TetG was present in all water samples but was mainly distributed in sediment samples from the northern region of Taihu Lake. β-Lactam resistance gene blaOXA-1 was present in all water samples but was absent in the sediment samples. TetM and tetO were found present in water and sediment samples from the western area of the lake. Remarkably, 95% of isolated fecal coliforms were resistant to trimethoprim and multi-drug resistant isolates were also observed. Sul1 and tetC genes were found to be carried by isolates resistant to corresponding antibiotics. This study provided baseline information about the occurrence of ARGs and integronase genes in Taihu Lake and the results may extend our knowledge about antibiotic resistance of microbial communities in the lake.

References

Zhang X X, Wu B, Zhang Y, et al. 2009, Class 1 integronase gene and tetracycline resistance genes tetA and tetC in different water environments of Jiangsu Province, China. Ecotoxicology, vol.18(6): 652–660. http://dx.doi.org/10.1007/s10646-009-0332-3.

Zhang X X, Zhang T and Fang H P, 2009, Antibiotic resistance genes in water environment. Applied Microbiology and Biotechnology, vol.82(3): 397–414. http://dx.doi.org/10.1007/s00253-008-1829-z.

Koonin E V, Makarova K S and Aravind L, 2001, Horizontal gene transfer in prokaryotes: quantification and classification. Annual Review of Microbiology, vol.55: 709–742. http://dx.doi.org/10.1146/annurev.micro.55.1.709.

Ding C and He J, 2010, Effect of antibiotics in the environment on microbial populations. Applied Microbiology and Biotechnology, vol.87(3): 925–941. http://dx.doi.org/10.1007/s00253-010-2649-5.

Martinez J L, 2009, Environmental pollution by antibiotics and by antibiotic resistance determinants. Environmental Pollution, vol.157(11): 2893–2902. http://dx.doi.org/10.1016/j.envpol.2009.05.051.

Kemper N, 2008, Veterinary antibiotics in the aquatic and terrestrial environment. Ecological Indicators, vol.8(1): 1–13. http://dx.doi.org/10.1016/j.ecolind.2007.06.002.

Roberts M C, 2005, Update on acquired tetracycline resistance genes. FEMS Microbiology Letters, vol.245(2): 195–203. http://dx.doi.org/10.1016/j.femsle.2005.02.034.

Kehrenberg C and Schwarz S, 2005, dfrA20, a novel trimethoprim resistance gene from Pasteurella multocida. Antimicrobial Agents and Chemotherapy, vol.49(1): 414–417. http://dx.doi.org/10.1128/AAC.49.1.414-417.2005.

Li X-Z, Mehrotra M, Ghimire S, et al. 2007, β-Lactam resistance and β-lactamases in bacteria of animal origin. Veterinary Microbiology, vol.121(3–4): 197–214. http://dx.doi.org/10.1016/j.vetmic.2007.01.015.

Nield B S, Holmes A J, Gillings M R, et al. 2001, Recovery of new integron classes from environmental DNA. FEMS Microbiology Letters, vol.195(1): 59–65. http://dx.doi.org/10.1111/j.1574-6968.2001.tb10498.x.

White P A, McIver C J and Rawlinson W D, 2001, Integrons and gene cassettes in the enterobacteriaceae. Antimicrobial Agents and Chemotherapy, vol.45(9): 2658– 2661. http://dx.doi.org/10.1128/AAC.45.9.2658-2661.2001.

Shen P P, Shi Q, Hua Z C, et al. 2003, Analysis of microcystins in cyanobacteria blooms and surface water samples from Meiliang Bay, Taihu Lake, China. Environment International, vol.29(5): 641–647. 13. Wang H, Wang C, Wu W, et al. 2003, Persistent organic pollutants in water and surface sediments of Taihu Lake, China and risk assessment. Chemosphere, vol.50(4): 557–562. http://dx.doi.org/10.1016/S0045-6535(02)00484-8.

Qu W, Dickman M and Wang S, 2001, Multivariate analysis of heavy metal and nutrient concentrations in sediments of Taihu Lake, China. Hydrobiologia, vol.450(1): 83–89. http://dx.doi.org/10.1023/A:1017551701587.

Wang X, Lu Y, Han J, et al. 2007, Identification of anthropogenic influences on water quality of rivers in Taihu watershed. Journal of Environmental Sciences, vol.19(4): 475–481. http://dx.doi.org/10.1016/S1001-0742(07)60080-1.

Sayah R S, Kaneene J B, Johnson Y, et al. 2005, Patterns of antimicrobial resistance observed in escherichia coli isolates obtained from domestic- and wild-animal fecal samples, human septage, and surface water. Applied and Environmental Microbiology, vol.71(3): 1394– 1404. http://dx.doi.org/10.1128/AEM.71.3.1394-1404.2005.

Schmidt A S, Bruun M S, Dalsgaard I, et al. 2000, Occurrence of antimicrobial resistance in fish-pathogenic and environmental bacteria associated with four danish rainbow trout farms. Applied and Environmental Microbiology, vol.66(11): 4908–4915.

http://dx.doi.org/10.1128/AEM.66.11.4908-4915.2000.

Han N N, Zhang S H, Wang P F, et al. 2013, Characterization of antibiotic resistance E. coli and antibiotic resistance genes in aquatic environment of Taihu Lake, China. Applied Mechanics and Materials, vol.295–298: 630–634. http://dx.doi.org/10.4028/www.scientific.net/AMM.295-298.630.

Niemi M, Sibakov M and Niemela S, 1983, Antibiotic resistance among different species of fecal coliforms isolated from water samples. Applied and Environmental Microbiology, vol.45(1): 79–83.

Gueimonde M, Tölkkö S, Korpimäki T, et al. 2004, New real-time quantitative pcr procedure for quantification of bifidobacteria in human fecal samples. Applied and Environmental Microbiology, vol.70(7):, 4165–4169. http://dx.doi.org/10.1128/AEM.70.7.4165-4169.2004.

Sandalli C, Özgümüş O B and Sevim A, 2010, Characterization of tetracycline resistance genes in tetracycline- resistant Enterobacteriaceae obtained from a coliform collection. World Journal of Microbiology and Biotechnology, vol.26(11): 2099–2103. http://dx.doi.org/10.1007/s11274-010-0381-z.

Tao R, Ying G G, Su H C, et al. 2010, Detection of antibiotic resistance and tetracycline resistance genes in Enterobacteriaceae isolated from the Pearl rivers in South China. Environmental Pollution, vol.158(6): 2101– 2109. http://dx.doi.org/10.1016/j.envpol.2010.03.004.

Gao P, Mao D, Luo Y, et al. 2012, Occurrence of sulfonamide and tetracycline-resistant bacteria and resistance genes in aquaculture environment. Water Research, vol.46(7): 2355–2364. http://dx.doi.org/10.1016/j.watres.2012.02.004.

Zou S, Zhu C, He Z, et al. 2009, Preliminary studies on the pollution levels of antibiotic resistance genes in the water of Beijiang River, South China. Asian Journal of Ecotoxicology, vol.4: 655–660.

Chen H, Shu W, Chang X, et al. 2010, The profile of antibiotics resistance and integrons of extended-spectrum beta-lactamase producing thermotolerant coliforms isolated from the Yangtze River basin in Chongqing. Environmental Pollution, vol.158(7): 2459–2464. http://dx.doi.org/10.1016/j.envpol.2010.03.023.

Feng L, 2010, The presence of antibiotic resistance genes in typical region of Tianjin and the environmental behavior of DNA. Nankai University.

Wang C, Lu G, Peifang W, et al. 2011, Assessment of environmental pollution of Taihu Lake by combining active biomonitoring and integrated biomarker response. Environmental Science and Technology, vol.45(8): 3746–3752. http://dx.doi.org/10.1021/es1037047.

Phuong Hoa P T, Nonaka L, Hung Viet P, et al. 2008, Detection of the sul1, sul2, and sul3 genes in sulfonamide-resistant bacteria from wastewater and shrimp ponds of north Vietnam. Science of the Total Environment, vol.405(1–3): 377–384. http://dx.doi.org/10.1016/j.scitotenv.2008.06.023.

Ji X, Liu F, Shen Q, et al. 2011, Quantitative detection of sulfonamides and tetracycline antibiotics and resistance genes in sewage farms. Ecology and Environmental Science, 2011-05: 927–933.

McKinney C W, Loftin K A, Meyer M T, et al. 2010, tet and sul antibiotic resistance genes in livestock lagoons of various operation type, configuration, and antibiotic occurrence. Environmental Science and Technology, vol.44(16): 6102–6109. http://dx.doi.org/10.1021/es9038165.

Jiang L, Chen S, Yang R, et al. 2008, Occurrence of antibiotics in the aquatic environment of the Changjiang Delta, China. Environmental Chemistry, vol.27: 371–374.

Yang Y, Jiang N, Yin L, et al. 2005, RS-based dynamic monitoring of lake area and enclosure culture in east Taihu Lake. Journal of Lake Science, vol.17: 927–933.

Ruiz E, Rezusta A, Saenz Y, et al. 2011, New genetic environments of aac(6’)-Ib-cr gene in a multiresistant Klebsiella oxytoca strain causing an outbreak in a pediatric intensive care unit. Diagnostic Microbiolgy and Infectious Disease, vol.69(2): 236–238. http://dx.doi.org/10.1016/j.diagmicrobio.2010.09.004.

Lee K, Yong D, Yum J H, et al. 2003, Diversity of TEM-52 extended-spectrum β-lactamase-producing non- typhoidal Salmonella isolates in Korea. Journal of Antimicrobial Chemotherapy, vol.52(3): 493–496. http://dx.doi.org/10.1093/jac/dkg385.

Ryoo N H, Lee K, Lim J B, et al. 2009, Outbreak by meropenem-resistant Pseudomonas aeruginosa producing IMP-6 metallo-β-lactamase in a Korean hospital. Diagnostic Microbiology and Infectious Disease, vol.63(1): 115–117. http://dx.doi.org/10.1016/j.diagmicrobio.2008.08.019.

Zhang S T, Lv L, Zhang Y, et al. 2013, Occurrence and variations of five classes of antibiotic resistance genes along the Jiulong River in southeast China. Journal of Environmental Biology, vol.34(2 Spec No): 345–351.

Tennstedt T, Szczepanowski R, Braun S, et al. 2003, Occurrence of integron-associated resistance gene cassettes located on antibiotic resistance plasmids isolated from a wastewater treatment plant. FEMS Microbiololgy Ecology, vol.45(3): 239–252. http://dx.doi.org/10.1016/S0168-6496(03)00164-8.

Fluit A C and Schmitz F J, 1999, Class 1 integrons, gene cassettes, mobility, and epidemiology. European Journal of Clinical Microbiology and Infectious Diseases, vol.18(11): 761–770. http://dx.doi.org/10.1007/s100960050398.

da Silva T F B X, Ramos D T, Dziedzic M, et al. 2011, Microbiological quality and antibiotic resistance analysis of a Brazilian water supply source. Water, Air, and Soil Pollution, vol.218(1): 611–618. http://dx.doi.org/10.1007/s11270-010-0672-x.

Pathak S P and Gopal K, 2008, Prevalence of bacterial contamination with antibiotic resistant and enterotoxigenic fecal coliforms in treated drinking water. Journal of Toxicology and Environmental Health, Part A: Current Issues, vol.71(7): 427–433. http://dx.doi.org/10.1080/15287390701838796.

Howell J M, Coyne M S and Cornelius P L, 2008, Effect of sediment particle size and temperature on fecal bacteria mortality rates and the fecal coliform/fecal streptococci ratio. Journal of Environmental Quality, vol.25(6): 1216– 1220. http://dx.doi.org/10.2134/jeq1996.00472425002500060007x.

Sköld O, 2001, Resistance to trimethoprim and sulfonamides. Veterinary Research, vol.32(3–4): 261–273. http://dx.doi.org/10.1051/vetres:2001123.

Ng L K, Martin I, Alfa M, et al. 2001, Multiplex PCR for the detection of tetracycline resistant genes. Molecular and Cellular Probes, vol.15(4): 209–215. http://dx.doi.org/10.1006/mcpr.2001.0363.

Kerrn M B, Klemmensen T, Frimodt-Møller N, et al. 2002, Susceptibility of Danish Escherichia coli strains isolated from urinary tract infections and bacteraemia, and distribution of sul genes conferring sulphonamide resistance. Journal of Antimicrobial Chemotherapy, vol.50(4): 513–516.

http://dx.doi.org/10.1093/jac/dkf164.

Pei R, Kim S-C, Carlson K H, et al. 2006, Effect of river landscape on the sediment concentrations of antibiotics and corresponding antibiotic resistance genes (ARG). Water Research, vol.40(12): 2427–2435. http://dx.doi.org/10.1016/j.watres.2006.04.017.

Szczepanowski R, Linke B, Krahn I, et al. 2009, Detection of 140 clinically relevant antibiotic resistance genes in the plasmid metagenome of wastewater treatment plant bacteria showing reduced susceptibility to selected antibiotics. Microbiology, vol.155: 2306–2319. http://dx.doi.org/10.1099/mic.0.028233-0.

Downloads

Published

2016-04-01

Issue

Section

Ecotoxicology and Ecosystem Health