Applied Microbiology and Biotechnology

, Volume 82, Issue 3, pp 397–414 | Cite as

Antibiotic resistance genes in water environment

  • Xu-Xiang Zhang
  • Tong Zhang
  • Herbert H. P. Fang


The use of antibiotics may accelerate the development of antibiotic resistance genes (ARGs) and bacteria which shade health risks to humans and animals. The emerging of ARGs in the water environment is becoming an increasing worldwide concern. Hundreds of various ARGs encoding resistance to a broad range of antibiotics have been found in microorganisms distributed not only in hospital wastewaters and animal production wastewaters, but also in sewage, wastewater treatment plants, surface water, groundwater, and even in drinking water. This review summarizes recently published information on the types, distributions, and horizontal transfer of ARGs in various aquatic environments, as well as the molecular methods used to detect environmental ARGs, including specific and multiplex PCR (polymerase chain reaction), real-time PCR, DNA sequencing, and hybridization based techniques.


Antibiotic resistance gene Environmental pollution Gene transfer Molecular detection method Water environment 



The authors wish to thank the Hong Kong Research Grants Council for the financial support of this study (HKU 7129/05E and HKU 7195/06E).


  1. Abriouel H, Omar NB, Molinos AC, López RL, Grande MJ, Martínez-Viedma P, Ortega E, Cañamero MM, Galvez A (2008) Comparative analysis of genetic diversity and incidence of virulence factors and antibiotic resistance among enterococcal populations from raw fruit and vegetable foods, water and soil, and clinical samples. Int J Food Microbiol 123:38–49Google Scholar
  2. Agersø Y, Sandvang D (2005) Class 1 integrons and tetracycline resistance genes in Alcaligenes, Arthrobacter, and Pseudomonas spp. isolated from pigsties and manured soil. Appl Environ Microbiol 71:7941–7947Google Scholar
  3. Agersø Y, Petersen A (2007) The tetracycline resistance determinant Tet 39 and the sulphonamide resistance gene sulII are common among resistant Acinetobacter spp. isolated from integrated fish farms in Thailand. J Antimicrob Chemother 59:23–27Google Scholar
  4. Agersø Y, Bruun MS, Dalsgaard I, Larsen JL (2007) The tetracycline resistance gene tet(E) is frequently occurring and present on large horizontally transferable plasmids in Aeromonas spp. from fish farms. Aquaculture 266:47–52Google Scholar
  5. Ahmed AM, Furuta K, Shimomura K, Kasama Y, Shimamoto T (2006) Genetic characterization of multidrug resistance in Shigella spp. from Japan. J Med Microbiol 55:1685–1691Google Scholar
  6. Akinbowale OL, Peng H, Barton MD (2007a) Class 1 integron mediates antibiotic resistance in Aeromonas spp. from rainbow trout farms in Australia. Int J Antimicrob Agents 29:S113Google Scholar
  7. Akinbowale OL, Peng H, Barton MD (2007b) Diversity of tetracycline resistance genes in bacteria from aquaculture sources in Australia. J Appl Microbiol 103:2016–2025Google Scholar
  8. Alekshun MN, Levy SB (2007) Molecular mechanisms of antibacterial multidrug resistance. Cell 128:1037–1050Google Scholar
  9. Alpay-Karaoglu S, Ozgumus OB, Sevim E, Kolayli F, Sevimi A, Yesilgil P (2007) Investigation of antibiotic resistance profile and TEM-type beta-lactamase gene carriage of ampicillin-resistant Escherichia coli strains isolated from drinking water. Ann Microbiol 57:281–288Google Scholar
  10. Aminov RI, Mackie RI (2007) Evolution and ecology of antibiotic resistance genes. FEMS Microbiol Lett 271:147–161Google Scholar
  11. Aminov RI, Chee-Sanford JC, Garrigues N, Teferedegne B, Krapac IJ, White BA, Mackie RI (2002) Development, validation, and application of PCR primers for detection of tetracycline efflux genes of Gram-negative bacteria. Appl Environ Microbiol 68:1786–1793Google Scholar
  12. Antunes P, Machado J, Peixe L (2006) Characterization of antimicrobial resistance and class 1 and 2 integrons in Salmonella enterica isolates from different sources in Portugal. J Antimicrob Chemother 58:297–304Google Scholar
  13. Antunes P, Machado J, Peixe L (2007) Dissemination of a new gene cluster comprising sul3 (tnp-sul3-tnp) linked to class 1 integrons with an unusual 3’CS region (qacH) among Salmonella isolates. Int J Antimicrob Agents 29:S112–S113Google Scholar
  14. Antwerpen MH, Schellhase M, Ehrentreich-Foerster E, Witte W, Nuebel U (2007) DNA microarray for detection of antibiotic resistance determinants in Bacillus anthracis and closely related Bacillus cereus. Mol Cell Probes 21:152–160Google Scholar
  15. Ardic N, Ozyurt M, Sareyyupoglu B, Haznedaroglu T (2005) Investigation of erythromycin and tetracycline resistance genes in methicillin-resistant staphylococci. Int J Antimicrob Agents 26:213–218Google Scholar
  16. Auerbach EA, Seyfried EE, McMahon KD (2007) Tetracycline resistance genes in activated sludge wastewater treatment plants. Water Res 41:1143–1151Google Scholar
  17. Baker-Austin C, Wright MS, Stepanauskas R, McArthur JV (2006) Co-selection of antibiotic and metal resistance. Trends Microbiol 14:176–182Google Scholar
  18. Batt AL, Snow DD, Aga DS (2006) Occurrence of sulfonamide antimicrobials in private water wells in Washington County, Idaho, USA. Chemosphere 64:1963–1971Google Scholar
  19. Bell JM, Paton JC, Turnidge J (1998) Emergence of vancomycin-resistant enterococci in Australia: phenotypic and genotypic characteristics of isolates. J Clin Microbiol 36:2187–2190Google Scholar
  20. Berg J, Tom-Petersen A, Nybroe O (2005) Copper amendment of agricultural soil selects for bacterial antibiotic resistance in the field. Lett Appl Microbiol 40:146–151Google Scholar
  21. Blahna MT, Zalewski CA, Reuer J, Kahlmeter G, Foxman B, Marrs CF (2006) The role of horizontal gene transfer in the spread of trimethoprim-sulfamethoxazole resistance among uropathogenic Escherichia coli in Europe and Canada. J Antimicrob Chemother 57:666–672Google Scholar
  22. Bönemann G, Stiens M, Pühler A, Schlüter A (2006) Mobilizable IncQ-related plasmid carrying a new quinolone resistance gene, qnrS2, isolated from the bacterial community of a wastewater treatment plant. Antimicrob Agents Chemother 50:3075–3080Google Scholar
  23. Call DR (2005) Challenges and opportunities for pathogen detection using DNA microarrays. Crit Rev Microbiol 31:91–99Google Scholar
  24. Call DR, Borucki MK, Loge FJ (2003) Detection of bacterial pathogens in environmental samples using DNA microarrays. J Microbiol Methods 53:235–243Google Scholar
  25. Caplin JL, Hanlon GW, Taylor HD (2008) Presence of vancomycin and ampicillin-resistant Enterococcus faecium of epidemic clonal complex-17 in wastewaters from the south coast of England. Environ Microbiol 10:885–892Google Scholar
  26. Cernat R, Balotescu C, Ivanescu D, Nedelcu D, Lazar V, Bucur M, Valeanu D, Tudorache R, Mitache M, Dragoescu M (2007) Mechanisms of resistance in multiple-antibiotic-resistant Escherichia coli strains isolated from drinking and recreational, salmaster waters. Int J Antimicrob Agents 29:S274Google Scholar
  27. Cetin ES, Gunes H, Kaya S, Aridogan BC, Demirci M (2008) Macrolide-lincosamide-streptogramin B resistance phenotypes in clinical staphylococcal isolates. Int J Antimicrob Agents 31:364–368Google Scholar
  28. Chee-Sanford JC, Aminov RI, Krapac IJ, Garrigues-Jeanjean N, Mackie RI (2001) Occurrence and diversity of tetracycline resistance genes in lagoons and groundwater underlying two swine production facilities. Appl Environ Microbiol 67:1494–1502Google Scholar
  29. Chen J, Yu ZT, Michel FC Jr, Wittum T, Morrison M (2007) Development and application of real-time PCR assays for quantification of erm genes conferring resistance to macrolides-lincosamides-streptogramin B in livestock manure and manure management systems. Appl Environ Microbiol 73:4407–4416Google Scholar
  30. Chen SH, Li YM, Yu CH (2008a) Oligonucleotide microarray: a new rapid method for screening the 23S rRNA gene of Helicobacter pylori for single nucleotide polymorphisms associated with clarithromycin resistance. J Gastroenterol Hepatol 23:126–131Google Scholar
  31. Chen S, Zhang MJ, Ma HH, Saiyin H, Shen SQ, Xi JJ, Wan B, Yu L (2008b) Oligo-microarray analysis reveals the role of cyclophilin A in drug resistance. Cancer Chemother Pharmacol 61:459–469Google Scholar
  32. Crowley D, Cryan B, Lucey B (2008) First detection of a class 2 integron among clinical isolates of Serratia marcescens. Br J Biomed Sci 65:86–89Google Scholar
  33. Dalsgaard A, Forslund A, Serichantalergs O, Sandvang D (2000) Distribution and content of class 1 integrons in different Vibrio cholerae O-serotype strains isolated in Thailand. Antimicrob Agents Chemother 44:1315–1321Google Scholar
  34. Dancer SJ, Shears P, Platt DJ (1997) Isolation and characterization of coliforms from glacial ice and water in Canada’s high arctic. J Appl Microbiol 82:597–609Google Scholar
  35. Dang HY, Zhang XX, Song LS, Chang YQ, Yang GP (2006) Molecular characterizations of oxytetracycline resistant bacteria and their resistance genes from mariculture waters of China. Mar Pollut Bull 52:1494–1503Google Scholar
  36. Dang HY, Zhang XX, Song LS, Chang YQ, Yang GP (2007) Molecular determination of oxytetracycline-resistant bacteria and their resistance genes from mariculture environments of China. J Appl Microbiol 103:2580–2592Google Scholar
  37. Dang HY, Ren J, Song LS, Sun S, An LG (2008) Dominant chloramphenicol-resistant bacteria and resistance genes in coastal marine waters of Jiaozhou Bay, China. World J Microb Biot 24(2):209–217Google Scholar
  38. da Silva MF, Vaz-Moreira I, Gonzalez-Pajuelo M, Nunes OC, Manaia CM (2007) Antimicrobial resistance patterns in Enterobacteriaceae isolated from an urban wastewater treatment plant. FEMS Microbiol Ecol 60:166–176Google Scholar
  39. Džidić S, Šušković J, Kos B (2008) Antibiotic resistance mechanisms in bacteria: biochemical and genetic aspects. Food Technol Biotech 46:11–21Google Scholar
  40. Engemann CA, Adams L, Knapp CW, Graham DW (2006) Disappearance of oxytetracycline resistance genes in aquatic systems. FEMS Microbiol Lett 263:176–182Google Scholar
  41. Engemann CA, Keen P, Knapp CW, Hall KJ, Graham DW (2008) Fate of tetracycline resistance genes in aquatic systems: Migration from the water column to peripheral biofilms. Environ Sci Technol 42:5131–5136Google Scholar
  42. Enne VI, Bennett PM, Livermore DM, Hall LM (2004) Enhancement of host fitness by the sul2-coding plasmid p9123 in the absence of selective pressure. J Antimicrob Chemother 53:958–963Google Scholar
  43. Filipova M, Bujdakova H, Drahovska H, Liskova A, Hanzen J (2006) Occurrence of aminoglycoside-modifying-enzyme genes aac(6′)-aph(2″), aph(3′), ant(4′) and ant(6) in clinical isolates of Enterococcus faecalis resistant to high-level of gentamicin and amikacin. Folia Microbiol 51:57–61Google Scholar
  44. Fluit AC, Schmitz FJ (1999) Class 1 integrons, gene cassettes, mobility, and epidemiology. Eur J Clin Microbiol Infect Dis 18:761–770Google Scholar
  45. Gilbride KA, Lee DY, Beaudette LA (2006) Molecular techniques in wastewater: understanding microbial communities, detecting pathogens, and real-time process control. J Microbiol Methods 66:1–20Google Scholar
  46. Guard-Bouldin J, Morales CA, Frye JG, Gast RK, Musgrove M (2007) Detection of Salmonella enterica subpopulations by phenotype microarray antibiotic resistance patterns. Appl Environ Microbiol 73:7753–7756Google Scholar
  47. Guillaume G, Verbrugge D, Chasseur-Libotte ML, Moens W, Collard JM (2000) PCR typing of tetracycline resistance determinants (Tet A–E) in Salmonella enterica serotype Hadar and in the microbial community of activated sludges from hospital and urban wastewater treatment facilities in Belgium. FEMS Microbiol Ecol 32:77–85Google Scholar
  48. Happi CT, Gbotosho GO, Folarin OA, Akinboye DO, Yusuf BO, Ebong OO, Sowunmi A, Kyle DE, Milhous W, Wirth DT, Oduola AMJ (2005) Polymorphisms in Plasmodium falciparum dhfr and dhps genes and age related in vivo sulfaxine-pyrimethamine resistance in malaria-infected patients from Nigeria. Acta Trop 95:183–193Google Scholar
  49. Hayes JR, Wagner DD, English LL, Carr LE, Joseph SW (2005) Distribution of streptogramin resistance determinants among Enterococcus faecium from a poultry production environment of the USA. J Antimicrob Chemother 55:123–126Google Scholar
  50. Hecht DW, Kos IM, Knopf SE, Vedantam G (2007) Characterization of BctA, a mating apparatus protein required for transfer of the Bacteroides fragilis conjugal element BTF-37. Res Microbiol 158:600–607Google Scholar
  51. Henriques IS, Fonseca F, Alves A, Saavedra MJ, Correia A (2006a) Occurrence and diversity of integrons and β-lactamase genes among ampicillin-resistant isolates from estuarine waters. Res Microbiol 157:938–947Google Scholar
  52. Henriques IS, Moura A, Alves A, Saavedra MJ, Correia A (2006b) Analysing diversity among β-lactamase encoding genes in aquatic environments. FEMS Microbiol Ecol 56:418–429Google Scholar
  53. Heuer H, Krögerrecklenfort E, Wellington EMH, Egan S, van Elsas JD, van Overbeek L, Collard JM, Guillaume G, Karagouni AD, Nikolakopoulou TL, Smalla, K (2002) Gentamicin resistance genes in environmental bacteria: prevalence and transfer. FEMS Microbiol Ecol 42:289–302Google Scholar
  54. Heuer H, Szczepanowski R, Schneiker S, Phler A, Top EM, Schlüter A (2004) The complete sequences of plasmids pB2 and pB3 provide evidence for a recent ancestor of the IncP-1b group without any accessory genes. Microbiology 150:3591–3599Google Scholar
  55. Heuer OE, Hammerum AM, Collignon P, Wegener HC (2006) Human health hazard from antimicrobial-resistant enterococci in animals and food. Clin Infect Dis 43:911–916Google Scholar
  56. Hu JY, Shi JC, Chang H, Li D, Yang M, Kamagata YC (2008) Phenotyping and genotyping of antihiotic-resistant Escherichia coli isolated from a natural river basin. Environ Sci Technol 42:3415–3420Google Scholar
  57. Huovinen P, Sundstrom L, Swedberg G, Skold O (1995) Trimethoprim and sulfonamide resistance. Antimicrob Agents Chemother 39:279–289Google Scholar
  58. Iversen A, Kühn I, Franklin A, Möllby R (2002) High prevalence of vancomycin-resistant enterococci in Swedish sewage. Appl Environ Microbiol 68:2838–2842Google Scholar
  59. Iversen A, Kühn I, Rahman M, Franklin A, Burman LG, Olsson-Liljequist B, Torell E, Möllby R (2004) Evidence for transmission between humans and the environment of a nosocomial strain of Enterococcus faecium. Environ Microbiol 6:55–59Google Scholar
  60. Jacobs L, Chenia HY (2007) Characterization of integrons and tetracycline resistance determinants in Aeromonas spp. isolated from South African aquaculture systems. Int J Food Microbiol 114:295–306Google Scholar
  61. Jensen LB, Agersø Y, Sengeløv G (2002) Presence of erm genes among macrolide-resistant Gram-positive bacteria isolated from Danish farm soil. Environ Int 28:487–491Google Scholar
  62. Kehrenberg C, Schwa S (2005) dfrA20, a novel trimethoprim resistance gene from Pasteurella multocida. Antimicrob Agents Chemother 49:414–417Google Scholar
  63. Kelmani Chandrakanth R, Raju S, Patil SA (2008) Aminoglycoside-resistance mechanisms in multidrug-resistant Staphylococcus aureus clinical isolates. Curr Mcirobiol 56:558–562Google Scholar
  64. Kemper N (2008) Veterinary antibiotics in the aquatic and terrestrial environment. Ecol Indic 8:1–13Google Scholar
  65. Kim SR, Nonaka L, Suzuki S (2004) Occurrence of tetracycline resistance genes tet(M) and tet(S) in bacteria from marine aquaculture sites. FEMS Microbiol Lett 237:147–156Google Scholar
  66. Kim SH, Wei CI, Tzou YM, An HJ (2005) Multidrug-resistant Klebsiella pneumoniae isolated from farm environments and retail products in Oklahoma. J Food Prot 68:2022–2029Google Scholar
  67. Kim YH, Jun LJ, Park SH, Yoon SH, Chuang JK, Kim JC, Jeong HD (2007) Prevalence of tet(B) and tet(M) genes among tetracycline-resistant Vibrio spp002E in the aquatic environments of Korea. Dis Aquat Organ 75:209–216Google Scholar
  68. Kobashi Y, Hasebe A, Nishio M, Uchiyama H (2007) Diversity of tetracycline resistance genes in bacteria isolated from various agricultural environments. Microb Environ 22:44–51Google Scholar
  69. Koksal F, Oguzkurt N, Samasti M, Altas K (2007) Prevalence and antimicrobial resistance patterns of Aeromonas strains isolated from drinking water samples in Istanbul, Turkey. Chemotherapy 53:30–35Google Scholar
  70. Kumar A, Schweizer HP (2005) Bacterial resistance to antibiotics: active efflux and reduced uptake. Adv Drug Deliv Rev 57:1486–1513Google Scholar
  71. Kümmerer K (2003) Significance of antibiotics in the environment. J Antimicrob Chemother 52:5–7Google Scholar
  72. Kümmerer K (2004) Resistance in the environment. J Antimicrob Chemother 54:311–320Google Scholar
  73. Labuschagne CDJ, Weldhagen GF, Ehlers MM, Dove MG (2008) Emergence of class 1 integron-associated GES-5 and GES-5-like extended-spectrum-lactamases in clinical isolates of Pseudomonas aeruginosa in South Africa. Int J Antimicrob Agents 31:527–530Google Scholar
  74. Lambert PA (2005) Bacterial resistance to antibiotics: Modified target sites. Adv Drug Deliv Rev 57:1471–1485Google Scholar
  75. Lee YJ, Han HS, Seong CN, Lee HY, Jung JS (1998) Distribution of genes coding for aminoglycoside acetyltransferases in gentamicin resistant bacteria isolated from aquatic environment. J Microbiol 36:249–255Google Scholar
  76. Levy SB, McMurry LM, Barbosa TM, Burdett V, Courvalin P, Hillen W, Roberts MC, Rood JI, Taylor DE (1999) Nomenclature for new tetracycline resistance determinants. Antimicrob Agents Chemother 43:1523–1524Google Scholar
  77. Li XZ, Mehrotra M, Ghimire S, Adewoye L (2007) β-Lactam resistance and β-lactamases in bacteria of animal origin. Vet Microbiol 121:197–214Google Scholar
  78. Lin J, Biyela PT (2005) Convergent acquisition of antibiotic resistance determinants amongst the Enterobacteriaceae sp. isolates of the Mhlathuze River, KwaZulu-Natal (RSA). Water SA 31:257–260Google Scholar
  79. Liu YF, Wang CH, Janapatla RP, Fu HM, Wu HM, Wu JJ (2007) Presence of plasmid pA15 correlates with prevalence of constitutive MLSB resistance in group A streptococcal isolates at a university hospital in southern Taiwan. J Antimicrob Chemother 59:1167–1170Google Scholar
  80. Livermore DM (1996) Are all beta-lactams created equal? Scand J Infect Dis Suppl 101:33–43Google Scholar
  81. Luo N, Pereira S, Sahin O, Lin J, Huang S, Michel L, Zhang Q (2005) Enhanced in vivo fitness of fluoroquinolone-resistant Campylobacter jejuni in the absence of antibiotic selection pressure. Proc Natl Acad Sci U S A 102:541–546Google Scholar
  82. Macauley JJ, Adams CD, Mormile MR (2007) Diversity of tet resistance genes in tetracycline resistant bacteria isolated from a swine lagoon with low antibiotic impact. Can J Microbiol 53:1307–1315Google Scholar
  83. Mackie RI, Koike S, Krapac I, Chee-Sanford J, Maxwell S, Aminov RI (2006) Tetracycline residues and tetracycline resistance genes in groundwater impacted by swine production facilities. Anim Biotechnol 17:157–176Google Scholar
  84. Malik A, Çelik EK, Bohn C, Böckelmann U, Knobel K, Grohmann E (2008) Detection of conjugative plasmids and antibiotic resistance genes in anthropogenic soils from Germany and India. FEMS Microbiol Lett 279:207–216Google Scholar
  85. Markoulatos P, Siafakas N, Moncany M (2002) Multiplex polymerase chain reaction: a practical approach. J Clin Lab Anal 16:47–51Google Scholar
  86. Mendez B, Tachibana C, Levy SB (1980) Heterogeneity of tetracycline resistance determinants. Plasmid 3:99–108Google Scholar
  87. Messi P, Guerrieri E, de Niederhäusern S, Sabia C, Bondi M (2006) Vancomycin-resistant enterococci (VRE) in meat and environmental samples. Int J Food Microbiol 107:218–222Google Scholar
  88. Mispagel H, Gray JT (2005) Antibiotic resistance from wastewater oxidation ponds. Water Environ Res 77:2996–3002Google Scholar
  89. Mohapatra H, Mohapatra SS, Mantri CK, Colwell RR, Singh DV (2008) Vibrio cholerae non-O1, non-O139 strains isolated before 1992 from Varanasi, India are multiple drug resistant, contain intSXT, dfr18 and aadA5 genes. Environ Microbiol 10:866–873Google Scholar
  90. Moosavian M, Tajbakhsh S, Samarbaf-Zadeh AR (2007) Rapid detection of clarithromycin-resistant Helicobacter pylori in patients with dyspepsia by fluorescent in situ hybridization (FISH) compared with the E-test. Ann Saudi Med 27:84–88CrossRefGoogle Scholar
  91. Morsczeck C, Langendörfer D, Schierholz JM (2004) A quantitative real-time PCR assay for the detection of tetR of Tn10 in Escherichia coli using SYBR Green and the Opticon. J Biochem Biophys Methods 59:217–227Google Scholar
  92. Moura A, Henriques I, Ribeiro R, Correia A (2007) Prevalence and characterization of integrons from bacteria isolated from a slaughterhouse wastewater treatment plant. J Antimicrob Chemother 60:1243–1250Google Scholar
  93. 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 157:220–226Google Scholar
  94. Naas T (2007) Insertion sequences, transposons and repeated elements. Int J Antimicrob Agents 29:S1Google Scholar
  95. Nikolakopoulou TL, Egan S, van Overbeek LS, Guillaume G, Heuer H, Wellington EMH, van Elsas JD, Collard JM, Smalla K, Karagouni AD (2005) PCR detection of oxytetracycline resistance genes otr(A) and otr(B) in tetracycline-resistant Streptomycete isolates from diverse habitats. Curr Microbiol 51:211–216Google Scholar
  96. Nonaka L, Ikeno K, Suzuki S (2007) Distribution of tetracycline resistance gene, tet(M), in Gram-positive and Gram-negative bacteria isolated from sediment and seawater at a coastal aquaculture site in Japan. Microb Environ 22:355–364Google Scholar
  97. Nrochet M, Couve E, Zouine M, Povart C, Glaser P (2008) A naturally occurring gene amplification leading to sulfonamide and trimethoprim resistance in Streptococcus agalactiae. J Bacteriol 190:672–680Google Scholar
  98. Obst U, Schwartz T, Volkmann H (2006) Antibiotic resistant pathogenic bacteria and their resistance genes in bacterial biofilms. Int J Artif Organs 29:387–394Google Scholar
  99. Ohlsen K, Ternes T, Werner G, Wallner U, Loffler D, Ziebuhr W, Witte W, Hacher J (2003) Impact of antibiotics on conjugational resistance gene transfer in Staphylococcus aureus in sewage. Environ Microbiol 5:711–716Google Scholar
  100. Okitsu N, Kaieda S, Yano H, Nakano R, Hosaka Y, Okamoto R, Kobayashi T, Inoue M (2005) Characterization of ermB gene transposition by Tn1545 and Tn917 in macrolide-resistant Streptococcus pneumoniae isolates. J Clin Microbiol 43:168–173Google Scholar
  101. 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 45:379–387Google Scholar
  102. Park JC, Lee JC, Oh JY, Jeong YW, Cho JW, Joo HS, Lee WK, Lee WB (2003) Antibiotic selective pressure for the maintenance of antibiotic resistant genes in coliform bacteria isolated from the aquatic environment. Water Sci Technol 47:249–253Google Scholar
  103. Patterson AJ, Colangeli R, Spigaglia P, Scott KP (2007) Distribution of specific tetracycline and erythromycin resistance genes in environmental samples assessed by macroarray detection. Environ Microbiol 9:703–715Google Scholar
  104. Pei RT, Kim SC, Carlson KH, Pruden A (2006) Effect of river landscape on the sediment concentrations of antibiotics and corresponding antibiotic resistance genes (ARG). Water Res 40:2427–2435Google Scholar
  105. Poppe C, Martin L, Muckle A, Archambault M, McEwen S, Weir E (2006) Characterization of antimicrobial resistance of Salmonella Newport isolated from animals, the environment, and animal food products in Canada. Can J Vet Res 70:105–114Google Scholar
  106. Prabhu DIG, Pandian RS, Vasan PT (2007) Pathogenicity, antibiotic susceptibility and genetic similarity of environmental and clinical isolates of Vibrio cholerae. Indian J Exp Biol 45:817–823Google Scholar
  107. Pruden A, Pei R, Storteboom H, Carlson K (2006) Antibiotic resistance genes as emerging contaminants: Studies in Northern Colorado. Environ Sci Technol 40:7445–7450Google Scholar
  108. Rahman MH, Nonaka L, Tago R, Suzuki S (2008) Occurrence of two genotypes of tetracycline (TC) resistance gene tet(M) in the TC-resistant bacteria in marine sediments of Japan. Environ Sci Technol 42:5055–5061Google Scholar
  109. Ram S, Vajpayee P, Shanker R (2008) Contamination of potable water distribution systems by multiantimicrobial-resistant enterohemorrhagic Escherichia coli. Environ Health Perspect 116:448–452Google Scholar
  110. Ramachandran D, Bhanumathi R, Singh DV (2007) Multiplex PCR for detection of antibiotic resistance genes and the SXT element: application in the characterization of Vibrio cholerae. J Med Microbiol 56:346–351Google Scholar
  111. Ramón-García S, Otal I, Martín C, Gómez-Lus R, Aínsa JA (2006) Novel streptomycin resistance gene from Mycobacterium fortuitum. Antimicrob Agents Chemother 50:3920–3922Google Scholar
  112. Rasmussen LD, Sorensen SJ (1998) The effect of long-term exposure to mercury on the bacterial community in marine sediment. Curr Microbiol 36:291–297Google Scholar
  113. Reinert RR, Franken C, van der Linden M, Lütticken R, Cil M, Al-Lahham A (2004) Molecular characterisation of macrolide resistance mechanisms of Streptococcus pneumoniae and Streptococcus pyogenes isolated in Germany, 2002-2003. Int J Antimicrobl Agents 24:43–47Google Scholar
  114. Roberts MC (2002) Resistance to tetracycline, macrolide-lincosamide-streptogramin, trimethoprim, and sulfonamide drug classes. Mol Biotechnol 20:261–283Google Scholar
  115. Roberts MC (2003) Acquired tetracycline and/or macrolide–lincosamides–streptogramin resistance in anaerobes. Anaerobe 9:63–69Google Scholar
  116. Roberts MC (2005) Update on acquired tetracycline resistance genes. FEMS Microbiol Lett 245:195–203Google Scholar
  117. Roberts MC (2008) Update on macrolide-lincosamide-streptogramin, ketolide, and oxazolidinone resistance genes. FEMS Microbiol Lett 282:147–159Google Scholar
  118. Roberts MC, Kenny GE (1986) Dissemination of the tetM tetracycline resistance determinant to Ureaplasma urealyticum. Antimicrob Agents Chemother 29:350–352Google Scholar
  119. Roberts MC, Sutcliffe J, Courvalin P, Jensen LB, Rood J, Seppala H (1999) Nomenclature for macrolide and macrolide-lincosamide streptogramin B antibiotic resistance determinants. Antimicrob Agents Chemother 43:2823–2830Google Scholar
  120. Rodríguez C, Lang L, Wang A, Altendorf K, García F, Lipski A (2006) Lettuce for human consumption collected in Costa Rica contains complex communities of culturable oxytetracycline-and gentamicin-resistant bacteria. Appl Environ Microbiol 72:5870–5876Google Scholar
  121. Russmann H, Adler K, Haas R, Gebert B, Koletzko S, Heesemann J (2001) Rapid and accurate determination of genotypic clarithromycin resistance in cultured Helicobacter pylori by fluorescent in situ hybridization. J Clin Microbiol 39:4142–4144Google Scholar
  122. Rysz M, Alvarez PJJ (2004) Amplification and attenuation of tetracycline resistance in soil bacteria: aquifer column experiments. Water Res 38:3705–3712Google Scholar
  123. Salyers AA, Amabile-Cuevas CF (1997) Why are antibiotic resistance genes so resistant to elimination? Antimicrob Agents Chemother 41:2321–2325Google Scholar
  124. Sarmah AK, Meyer MT, Boxall ABA (2006) A global perspective on the use, sales, exposure pathways, occurrence, fate and effects of veterinary antibiotics (VAs) in the environment. Chemosphere 65:725–759Google Scholar
  125. Schlüter A, Heuer H, Szczepanowski R, Poler SM, Schneiker S, Pühler A, Top EM (2005) Plasmid pB8 is closely related to the prototype IncP-1b plasmid R751 but transfers poorly to Escherichia coli and carries a new transposon encoding a small multidrug resistance (SMR) efflux protein. Plasmid 54:135–148Google Scholar
  126. Schlüter A, Szczepanowski R, Kurz N, Schneiker S, Krahn I, Pühler A (2007a) Erythromycin resistance-conferring plasmid pRSB105, isolated from a sewage treatment plant, harbors a new macrolide resistance determinant, an integron-containing Tn402-like element, and a large region of unknown function. Appl Environ Microbiol 73:1952–1960Google Scholar
  127. Schlüter A, Szczepanowski R, Pühler A, Top EM (2007b) Genomics of IncP-1 antibiotic resistance plasmids isolated from wastewater treatment plants provides evidence for a widely accessible drug resistance gene pool. FEMS Microbiol Rev 31:449–477Google Scholar
  128. Schmidt AS, Bruun MS, Dalsgaard I, Larsen JL (2001) Incidence, distribution, and spread of tetracycline resistance determinants and integron-associated antibiotic resistance genes among motile aeromonads from a fish farming environment. Appl Environ Microbiol 67:5675–5682Google Scholar
  129. Schwartz T, Kohnen W, Jansen B, Obst U (2003) Detection of antibiotic-resistant bacteria and their resistance genes in wastewater, surface water, and drinking water biofilms. FEMS Microbiol Ecol 43:325–335Google Scholar
  130. Schwarz S, Kehrenberg C, Doublet B, Cloeckaert A (2004) Molecular basis of bacterial resistance to chloramphenicol and florfenicol. FEMS Microbiol Rev 28:519–542Google Scholar
  131. Seveno NA, kallifidas D, Smalla K, van Elsas JD, Collard JM, Karagouni AD, Wellington EMH (2002) Occurrence and reservoirs of antibiotic resistance genes in the environment. Rev Med Microbiol 13:15–27Google Scholar
  132. Shakil S, Khan R, Zarrilli R, Khan AU (2008) Aminoglycosides versus bacteria—a description of the action, resistance mechanism, and nosocomial battleground. J Biomed Sci 15:5–14Google Scholar
  133. Sköld O (2000) Sulfonamide resistance: mechanisms and trends. Drug Resist Updat 3:155–160Google Scholar
  134. Sköld O (2001) Resistance to trimethoprim and sulfonamides. Vet Res 32:261–273Google Scholar
  135. Smalla K, Sobecky PA (2002) The prevalence and diversity of mobile genetic elements in bacterial communities of different environmental habitats: insights gained from different methodological approaches. FEMS Microbiol Ecol 42:165–175Google Scholar
  136. Smith MS, Yang RK, Knapp CW, Niu YF, Peak N, Hanfelt MM, Galland JC, Graham DW (2004) Quantification of tetracycline resistance genes in feedlot lagoons by real-time PCR. Appl Environ Microbiol 12:7372–7377Google Scholar
  137. Spence RP, Wright V, Ala-Aldeen DAA, Turner DP, Wooldridge KG, James R (2008) Validation of virulence and epidemiology DNA microarray for identification and characterization of Staphylococcus aureus isolates. J Clin Microbiol 46:1620–1627Google Scholar
  138. Srinivasan V, Nam HM, Nguyen LT, Tamilselvam B, Murinda SE, Oliver SP (2005) Prevalence of antimicrobial resistance genes in Listeria monocytogenes isolated from dairy farms. Foodborne Pathog Dis 2:201–211Google Scholar
  139. Stepanauskas R, Glenn TC, Jagoe CH, Tuckfield RC, Lindell AH, McArthur JV (2005) Elevated microbial tolerance to metals and antibiotics in metal-contaminated industrial environments. Environ Sci Technol 39:3671–3678Google Scholar
  140. Summers AO (2006) Genetic linkage and horizontal gene transfer, the roots of the antibiotic multi-resistance problem. Anim Biotechnol 17:125–135Google Scholar
  141. Suzuki S, Kobayashi T, Suehiro F, Tuyen CB, Tana TS (2008) High occurrence rate of tetracycline (TC)-resistant bacteria and TC resistance genes relates to microbial diversity in sediment of Mekong River main waterway. Microb Environ 23:149–152Google Scholar
  142. Szczepanowski R, Krahn I, Linke B, Goesmann A, Pühler A, Schlüter A (2004) Antibiotic multiresistance plasmid pRSB101 isolated from a wastewater treatment plant is related to plasmids residing in phytopathogenic bacteria and carries eight different resistance determinants including a multidrug transport system. Microbiology 150:3613–3630Google Scholar
  143. Szczepanowski R, Braun S, Riedel V, Schneiker S, Krahn I, Pühler A, Schlüter A (2005) The 120 592 bp IncF plasmid pRSB107 isolated from a sewage-treatment plant encodes nine different antibiotic-resistance determinants, two iron-acquisition systems and other putative virulence-associated functions. Microbiology 151:1095–1111Google Scholar
  144. Tatavarthy A, Peak K, Veguilla W, Reeves F, Cannons A, Amuso P, Cattani J (2006) Comparison of antibiotic susceptibility profiles and molecular typing patterns of clinical and environmental Salmonella enterica serotype Newport. J Food Prot 69:749–756Google Scholar
  145. Tauch A, Schlüter A, Bischoff N, Goesmann A, Meyer F, Pühler A (2003) The 79,370-bp conjugative plasmid pB4 consists of an IncP-1b backbone loaded with a chromate resistance transposon, the strA-strB streptomycin resistance gene pair, the oxacillinase gene bla NPS-1, and a tripartite antibiotic efflux system of the resistance-nodulation-division family. Mol Genet Genomics 268:570–584Google Scholar
  146. Taviani E, Ceccarelli D, Lazaro N, Bani S, Cappuccinelli P, Colwell RR, Colombo MM (2008) Environmental Vibrio spp., isolated in Mozambique, contain a polymorphic group of integrative conjugative elements and class 1 integrons. FEMS Microbiol Ecol 64:45–54Google Scholar
  147. Tennstedt T, Szczepanowski R, Braun S, Pühler A, Schlüter A (2003) Occurrence of integron-associated resistance gene cassettes located on antibiotic resistance plasmids isolated from a wastewater treatment plant. FEMS Microbiol Ecol 45:239–252Google Scholar
  148. Tennstedt T, Szczepanowski R, Krahn I, Pühler A, Schlüter A (2005) Sequence of the 68,869 bp IncP-1a plasmid pTB11 from a waste-water treatment plant reveals a highly conserved backbone, a Tn402-like integron and other transposable elements. Plasmid 53:218–238Google Scholar
  149. Thompson SA, Maani EV, Lindell AH, King CJ, McArthur JV (2007) Novel tetracycline resistance determinant isolated from an environmental strain of Serratia marcescens. Appl Environ Microbiol 73:2199–2206Google Scholar
  150. Vakulenko SB, Mobashery S (2003) Versatility of aminoglycosides and prospects for their future. Clin Microbiol Rev 16:430–450Google Scholar
  151. Volkmann H, Schwartz T, Bischoff P, Kirchen S, Obst U (2004) Detection of clinically relevant antibiotic-resistance genes in municipal wastewater using real-time PCR (TaqMan). J Microbiol Methods 56:277–286Google Scholar
  152. Walsh C (2000) Molecular mechanisms that confer antibacterial drug resistance. Nature 406:775–781Google Scholar
  153. Walsh TR, Howe RA (2002) The prevalence and mechanisms of vancomycin resistance in Staphylococcus aureus. Annu Rev Microbiol 56:657–675Google Scholar
  154. Weldhagen GF (2004) Integrons and beta-lactamases-a novel perspective on resistance. Int J Antimicrob Agents 23:556–562Google Scholar
  155. Werner G, Bartel M, Wellinghausen N, Essig A, Klare I, Witte W, Poppert S (2007) Detection of mutations conferring resistance to linezolid in Enterococcus spp. by fluorescence in situ hybridization. J Clin Microbiol 45:3421–3423Google Scholar
  156. Wright GD (2005) Bacterial resistance to antibiotics: enzymatic degradation and modification. Adv Drug Deliv Rev 57:1451–1470Google Scholar
  157. Wright GD (2007) The antibiotic resistome: the nexus of chemical and genetic diversity. Nat Rev Microbiol 5:175–186Google Scholar
  158. Wright MS, Peltier GL, Stepanauskas R, McArthur JV (2006) Bacterial tolerances to metals and antibiotics in metal-contaminated and reference streams. FEMS Microbiol Ecol 58:293–302Google Scholar
  159. Wright MS, Baker-Austin C, Lindell AH, Stepanauskas R, Stikes HW, McArthur JV (2008) Influence of industrial contamination on mobile genetic elements: class 1 integron abundance and gene cassette structure in aquatic bacterial communities. ISME J 2:417–428Google Scholar
  160. Yang S, Carlson K (2003) Evolution of antibiotic occurrence in a river through pristine, urban and agricultural landscapes. Water Res 37:4645–4656Google Scholar
  161. Yu ZT, Michel FC Jr, Hansen G, Wittum T, Morrison M (2005) Development and application of real-time PCR assays for quantification of genes encoding tetracycline resistance. Appl Environ Microbiol 71:6926–6933Google Scholar
  162. Zhang T, Fang HHP (2006) Applications of real-time polymerase chain reaction for quantification of microorganisms in environmental samples. Appl Microbiol Biotechnol 70:281–289Google Scholar
  163. Zhou QX, Luo Y, Wang ME (2007) Environmental residues and ecotoxicity of antibiotics and their resistance gene pollution: a review. Asian J Ecotoxicol 2:243–251Google Scholar
  164. Zhu B (2007) Abundance dynamics and sequence variation of neomycin phosphotransferase gene (nptII) homologs in river water. Aquat Microb Ecol 48:131–140Google Scholar
  165. Zhu LX, Wang D, Zhang GB, Jiang D, Zhang ZW, Zhang Q, Mitchelson K, Cheng J (2007a) Development of a base stacking hybridization-based microarray method for rapid identification of clinical isolates. Diagn Microbiol Infect Dis 59:149–156Google Scholar
  166. Zhu LX, Zhang ZW, Wang C, Yang HW, Jiang D, Zhang Q, Mitchelson K, Cheng J (2007b) Use of a DNA microarray for simultaneous detection of antibiotic resistance genes among staphylococcal clinical isolates. J Clin Microbiol 45:3514–3521Google Scholar

Copyright information

© Springer-Verlag 2008

Authors and Affiliations

  • Xu-Xiang Zhang
    • 1
    • 2
  • Tong Zhang
    • 1
  • Herbert H. P. Fang
    • 1
  1. 1.Environmental Biotechnology Lab,Department of Civil EngineeringThe University of Hong KongHong KongChina
  2. 2.Department of Environmental ScienceNanjing UniversityNanjingChina

Personalised recommendations