Metagenomic Profiling of Antibiotic Resistance Genes and Mobile Genetic Elements in a Tannery Wastewater Treatment Plant

PLoS ONE

Volumn 8, Issue 10, 2013, Pages

  Wang, Zhu ^a   Zhang, Xu Xiang ^a   Huang, Kailong ^a   Miao, Yu ^a   Shi, Peng ^a   Liu, Bo ^a   Long, Chao ^a   Li, Aimin ^a  

^a NANJING UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; MOBILE GENETIC ELEMENT; UNCLASSIFIED DRUG;

ACTINOBACTERIA; ANTIBIOTIC RESISTANCE; ANTIBIOTIC RESISTANCE GENE; ARCHAEON; ARTICLE; BACTERIAL GENE; BACTEROIDETES; CLASS 1 INTEGRASE GENE; COMMUNITY STRUCTURE; FIRMICUTES; GENE IDENTIFICATION; HIGH THROUGHPUT SEQUENCING; LEATHER INDUSTRY; METAGENOMICS; MICROBIAL COMMUNITY; NONHUMAN; PROTEOBACTERIA; SLUDGE; SUL1 GENE; TET GENE; TET33 GENE; WASTE WATER TREATMENT PLANT;

BIODIVERSITY; DNA TRANSPOSABLE ELEMENTS; DRUG RESISTANCE, MICROBIAL; GENES, RRNA; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; METAGENOMICS; SEWAGE;

EID: 84885040181     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0076079     Document Type: Article

References (67)

1. Luo Y, Xu L, Rysz M, Wang Y, Zhang H, et al. (2011) Occurrence and transport of tetracycline, sulfonamide, quinolone, and macrolide antibiotics in the Haihe River Basin, China. Environ Sci Technol 45: 1827-1833. doi:10.1021/es104009s. PubMed: 21309601.
2. Hvistendahl M, (2012) Public health. China takes aim at rampant antibiotic resistance. Science 336: 795. doi:10.1126/science.336.6083.795. PubMed: 22605727.
3. Goto T, Ito Y, Yamada S, Matsumoto H, Oka H, (2005) High-throughput analysis of tetracycline and penicillin antibiotics in animal tissues using electrospray tandem mass spectrometry with selected reaction monitoring transition. J Chromatogr A 1100: 193-199. doi:10.1016/j.chroma.2005.09.056. PubMed: 16214156.
4. Gratacos-Cubarsi M, Castellari M, Garcia-Regueiro JA, (2006) Detection of sulphamethazine residues in cattle and pig hair by HPLC-DAD. J Chromatogr B Anal Technol Biomed Life Sci 832: 121-126. doi:10.1016/j.jchromb.2006.01.002.
5. Bittencourt MS, Martins MT, de Albuquerque FG, Barreto F, Hoff R, (2012) High-throughput multiclass screening method for antibiotic residue analysis in meat using liquid chromatography-tandem mass spectrometry: a novel minimum sample preparation procedure. Foods Addit Contam A Chem Anal Control Expo Risk Assess 29: 508-516. doi:10.1080/19440049.2011.606228. PubMed: 21988236.
6. Tariq SR, Shah MH, Shaheen N, Khalique A, Manzoor S, et al. (2006) Multivariate analysis of trace metal levels in tannery effluents in relation to soil and water: a case study from Peshawar, Pakistan. J Environ Manage 79: 20-29. doi:10.1016/j.jenvman.2005.05.009. PubMed: 16154685.
7. Tisler T, Zagorc-Koncan J, Cotman M, Drolc A, (2004) Toxicity potential of disinfection agent in tannery wastewater. Water Res 38: 3503-3510. doi:10.1016/j.watres.2004.05.011. PubMed: 15325176.
8. Baker-Austin C, Wright MS, Stepanauskas R, McArthur JV, (2006) Co-selection of antibiotic and metal resistance. Trends Microbiol 14: 176-182. doi:10.1016/j.tim.2006.02.006. PubMed: 16537105.
9. Verma T, Srinath T, Gadpayle RU, Ramteke PW, Hans RK, et al. (2001) Chromate tolerant bacteria isolated from tannery effluent. Bioresoure Technol 78: 31-35. doi:10.1016/S0960-8524(00)00168-1. PubMed: 11265785.
10. Alam MZ, Ahmad S, Malik A, (2011) Prevalence of heavy metal resistance in bacteria isolated from tannery effluents and affected soil. Environ Monit Assess 178: 281-291. doi:10.1007/s10661-010-1689-8. PubMed: 20824329.
11. Lefebvre O, Vasudevan N, Thanasekaran K, Moletta R, Godon JJ, (2006) Microbial diversity in hypersaline wastewater: the example of tanneries. Extremophiles 10: 505-513. doi:10.1007/s00792-006-0524-1. PubMed: 16738814.
12. Chen J, Tang Y-Q, Wu X-L, (2012) Bacterial community shift in two sectors of a tannery plant and its Cr (VI) removing potential. Geomicrobiol J 29: 226-235. doi:10.1080/01490451.2011.558562.
13. Zhang T, Zhang XX, Ye L, (2011) Plasmid metagenome reveals high levels of antibiotic resistance genes and mobile genetic elements in activated sludge. PLOS ONE 6: e26041. doi:10.1371/journal.pone.0026041. PubMed: 22016806.
14. Tennstedt T, Szczepanowski R, Krahn I, Pühler A, Schlüter A, (2005) Sequence of the 68,869 bp IncP-1α plasmid pTB11 from a waste-water treatment plant reveals a highly conserved backbone, a Tn402-like integron and other transposable elements. Plasmid 53: 218-238. doi:10.1016/j.plasmid.2004.09.004. PubMed: 15848226.
15. Ma L, Zhang XX, Cheng S, Zhang Z, Shi P, et al. (2011) Occurrence, abundance and elimination of class 1 integrons in one municipal sewage treatment plant. Ecotoxicology 20: 968-973. doi:10.1007/s10646-011-0652-y. PubMed: 21431316.
16. Shi P, Jia S, Zhang XX, Zhang T, Cheng S, et al. (2013) Metagenomic insights into chlorination effects on microbial antibiotic resistance in drinking water. Water Res 47: 111-120. doi:10.1016/j.watres.2012.09.046. PubMed: 23084468.
17. Kristiansson E, Fick J, Janzon A, Grabic R, Rutgersson C, et al. (2011) Pyrosequencing of antibiotic-contaminated river sediments reveals high levels of resistance and gene transfer elements. PLOS ONE 6: e17038. doi:10.1371/journal.pone.0017038. PubMed: 21359229.
18. Monier JM, Demanèche S, Delmont TO, Mathieu A, Vogel TM, et al. (2011) Metagenomic exploration of antibiotic resistance in soil. Curr Opin Microbiol 14: 229-235. doi:10.1016/j.mib.2011.04.010. PubMed: 21601510.
19. Yu K, Zhang T, (2012) Metagenomic and metatranscriptomic analysis of microbial community structure and gene expression of activated sludge. PLOS ONE 7: e38183. doi:10.1371/journal.pone.0038183. PubMed: 22666477.
20. Singh KM, Jakhesara SJ, Koringa PG, Rank DN, Joshi CG, (2012) Metagenomic analysis of virulence-associated and antibiotic resistance genes of microbes in rumen of Indian buffalo (Bubalus bubalis). Gene 507: 146-151. doi:10.1016/j.gene.2012.07.037. PubMed: 22850272.
21. Gomez-Alvarez V, Revetta RP, Santo Domingo JW, (2012) Metagenome analyses of corroded concrete wastewater pipe biofilms reveal a complex microbial system. BMC Microbiol 12: 122. doi:10.1186/1471-2180-12-122. PubMed: 22727216.
22. Goecks J, Nekrutenko A, Taylor J, Galaxy Team (2010) Galaxy: a comprehensive approach for supporting accessible, reproducible, and transparent computational research in the life sciences. Genome Biol 11: R86. doi:10.1186/gb-2010-11-8-r86. PubMed: 20738864.
23. Gomez-Alvarez V, Teal TK, Schmidt TM, (2009) Systematic artifacts in metagenomes from complex microbial communities. ISME J, 3: 1314-1317. PubMed: 19587772.
24. Pfister CA, Meyer F, Antonopoulos DA, (2010) Metagenomic profiling of a microbial assemblage associated with the California mussel: a node in networks of carbon and nitrogen cycling. PLOS ONE 5: e10518. doi:10.1371/journal.pone.0010518. PubMed: 20463896.
25. Overbeek R, Disz T, Stevens R, (2004) A Peer-to-Peer Environment for Annotation of Genomes: The SEED.
26. Overbeek R, Begley T, Butler RM, Choudhuri JV, Chuang HY, et al. (2005) The subsystems approach to genome annotation and its use in the project to annotate 1000 genomes. Nucleic Acids Res 33: 5691-5702. doi:10.1093/nar/gki866. PubMed: 16214803.
27. Liu B, Pop M, (2009) ARDB--Antibiotic Resistance Genes Database. Nucleic Acids Res 37: D443-D447. doi:10.1093/nar/gkn656. PubMed: 18832362.
28. Siguier P, Perochon J, Lestrade L, Mahillon J, Chandler M, (2006) ISfinder: the reference centre for bacterial insertion sequences. Nucleic Acids Res 34: D32-D36. doi:10.1093/nar/gkj014. PubMed: 16381877.
29. Moura A, Soares M, Pereira C, Leitão N, Henriques I, et al. (2009) INTEGRALL: a database and search engine for integrons, integrases and gene cassettes. Bioinformatics 25: 1096-1098. doi:10.1093/bioinformatics/btp105. PubMed: 19228805.
30. Zhang T, Shao MF, Ye L, (2011) 454 Pyrosequencing reveals bacterial diversity of activated sludge from 14 sewage treatment plants. ISME J 6: 1137-1147. PubMed: 22170428.
31. Xia S, Duan L, Song Y, Li J, Piceno YM, et al. (2010) Bacterial community structure in geographically distributed biological wastewater treatment reactors. Environ Sci Technol 44: 7391-7396. doi:10.1021/es101554m. PubMed: 20812670.
32. Snaidr J, Amann R, Huber I, Ludwig W, Schleifer KH, (1997) Phylogenetic analysis and in situ identification of bacteria in activated sludge. Appl Environ Microbiol 63: 2884-2896. PubMed: 9212435.
33. Murugananthan M, Bhaskar Raju G, Prabhakar S, (2004) Separation of pollutants from tannery effluents by elector flotation. Sep Purif Technol 40: 69-75. doi:10.1016/j.seppur.2004.01.005.
34. Thomas F, Hehemann JH, Rebuffet E, Czjzek M, Michel G, (2011) Environmental and gut bacteroidetes: the food connection. Front Microbiol 2: 93. PubMed: 21747801.
35. Vartoukian SR, Palmer RM, Wade WG, (2007) The division "Synergistes". Anaerobe 13: 99-106. doi:10.1016/j.anaerobe.2007.05.004. PubMed: 17631395.
36. Cheong DY, Hansen CL, (2006) Bacterial stress enrichment enhances anaerobic hydrogen production in cattle manure sludge. Appl Microbiol Biotechnol 72: 635-643. doi:10.1007/s00253-006-0313-x. PubMed: 16525779.
37. Godon JJ, Zumstein E, Dabert P, Habouzit F, Moletta R, (1997) Molecular microbial diversity of an anaerobic digester as determined by small-subunit rDNA sequence analysis. Appl Environ Microbiol 63: 2802-2813. PubMed: 9212428.
38. Santegoeds CM, Damgaard LR, Hesselink G, Zopfi J, Lens P, et al. (1999) Distribution of sulfate-reducing and methanogenic bacteria in anaerobic aggregates determined by microsensor and molecular analyses. Appl Environ Microbiol 65: 4618-4629. PubMed: 10508098.
39. Pender S, Toomey M, Carton M, Eardly D, Patching JW, et al. (2004) Long-term effects of operating temperature and sulphate addition on the methanogenic community structure of anaerobic hybrid reactors. Water Res 38: 619-630. doi:10.1016/j.watres.2003.10.055. PubMed: 14723931.
40. Kröber M, Bekel T, Diaz NN, Goesmann A, Jaenicke S, et al. (2009) Phylogenetic characterization of a biogas plant microbial community integrating clone library 16S-rDNA sequences and metagenome sequence data obtained by 454-pyrosequencing. J Biotechnol 142: 38-49. doi:10.1016/j.jbiotec.2009.02.010. PubMed: 19480946.
41. James TY, Kauff F, Schoch CL, Matheny PB, Hofstetter V, et al. (2006) Reconstructing the early evolution of Fungi using a six-gene phylogeny. Nature 443: 818-822. doi:10.1038/nature05110. PubMed: 17051209.
42. Uroz S, Ioannidis P, Lengelle J, Cébron A, Morin E, et al. (2013) Functional assays and metagenomic analyses reveals differences between the microbial communities inhabiting the soil horizons of a Norway spruce plantation. PLOS ONE 8: e55929. doi:10.1371/journal.pone.0055929. PubMed: 23418476.
43. Urich T, Lanzén A, Qi J, Huson DH, Schleper C, et al. (2008) Simultaneous assessment of soil microbial community structure and function through analysis of the meta-transcriptome. PLOS ONE 3: e2527. doi:10.1371/journal.pone.0002527. PubMed: 18575584.
44. Cabiscol E, Tamarit J, Ros J, (2000) Oxidative stress in bacteria and protein damage by reactive oxygen species. Int Microbiol 3: 3-8. PubMed: 10963327.
45. Goldberg AL, (2003) Protein degradation and protection against misfolded or damaged proteins. Nature 426: 895-899. doi:10.1038/nature02263. PubMed: 14685250.
46. Reeve CA, Bockman AT, Matin A, (1984) Role of protein degradation in the survival of carbon-starved Escherichia coli and Salmonella typhimurium. J Bacteriol 157: 758-763. PubMed: 6365890.
47. Marcelino M, Wallaert D, Guisasola A, Baeza JA, (2011) A two-sludge system for simultaneous biological C, N and P removal via the nitrite pathway. Water Sci Technol 64: 1142-1147. doi:10.2166/wst.2011.398. PubMed: 22214063.
48. Vejmelkova D, Sorokin DY, Abbas B, Kovaleva OL, Kleerebezem R, et al. (2012) Analysis of ammonia-oxidizing bacteria dominating in lab-scale bioreactors with high ammonium bicarbonate loading. Appl Microbiol Biotechnol 93: 401-410. doi:10.1007/s00253-011-3409-x. PubMed: 21691786.
49. Morris SM, (2007) Arginine metabolism: boundaries of our knowledge. J Nutr 137: 1602S-1609S. PubMed: 17513435.
50. Silva CC, Hayden H, Sawbridge T, Mele P, Kruger RH, et al. (2012) Phylogenetic and functional diversity of metagenomic libraries of phenol degrading sludge from petroleum refinery wastewater treatment system. AMB Express 2: 18. doi:10.1186/2191-0855-2-18. PubMed: 22452812.
51. Borràs S, Ríos-Kristjánsson JG, Companyó R, Prat MD, (2012) Analysis of fluoroquinolones in animal feeds by liquid chromatography with fluorescence detection. J Sep Sci 35: 2048-2053. doi:10.1002/jssc.201200302. PubMed: 22778021.
52. Li J, Wang T, Shao B, Shen J, Wang S, et al. (2012) Plasmid-mediated quinolone resistance genes and antibiotic residues in wastewater and soil adjacent to swine feedlots: potential transfer to agricultural lands. Environ Health Perspect 120: 1144-1149. doi:10.1289/ehp.1104776. PubMed: 22569244.
53. Port JA, Wallace JC, Griffith WC, Faustman EM, (2012) Metagenomic profiling of microbial composition and antibiotic resistance determinants in Puget Sound. PLOS ONE 7: e48000. doi:10.1371/journal.pone.0048000. PubMed: 23144718.
54. Zhang XX, Zhang T, Fang HH, (2009) Antibiotic resistance genes in water environment. Appl Microbiol Biotechnol 82: 397-414. doi:10.1007/s00253-008-1829-z. PubMed: 19130050.
55. Zhang XX, Zhang T, (2011) Occurrence, abundance, and diversity of tetracycline resistance genes in 15 sewage treatment plants across China and other global locations. Environ Sci Technol 45: 2598-2604. doi:10.1021/es103672x. PubMed: 21388174.
56. Xu W, Zhang G, Li X, Zou S, Li P, et al. (2007) Occurrence and elimination of antibiotics at four sewage treatment plants in the Pearl River Delta (PRD), South China. Water Res 41: 4526-4534. doi:10.1016/j.watres.2007.06.023. PubMed: 17631935.
57. Zhao L, Dong YH, Wang H, (2010) Residues of veterinary antibiotics in manures from feedlot livestock in eight provinces of China. Sci Total Environ 408: 1069-1075. doi:10.1016/j.scitotenv.2009.11.014. PubMed: 19954821.
58. Heise J, Höltge S, Schrader S, Kreuzig R, (2006) Chemical and biological characterization of non-extractable sulfonamide residues in soil. Chemosphere 65: 2352-2357. doi:10.1016/j.chemosphere.2006.04.084. PubMed: 16774778.
59. Kim S, Eichhorn P, Jensen JN, Weber AS, Aga DS, (2005) Removal of antibiotics in wastewater: Effect of hydraulic and solid retention times on the fate of tetracycline in the activated sludge process. Environ Sci Technol 39: 5816-5823. doi:10.1021/es050006u. PubMed: 16124320.
60. Yu K, Zhang T, (2013) Construction of Customized Sub-Databases from NCBI-nr Database for Rapid Annotation of Huge Metagenomic Datasets Using a Combined BLAST and MEGAN Approach. PLOS ONE 8: e59831. doi:10.1371/journal.pone.0059831. PubMed: 23573212.
61. Moura A, Henriques I, Smalla K, Correia A, (2010) Wastewater bacterial communities bring together broad-host range plasmids, integrons and a wide diversity of uncharacterized gene cassettes. Res Microbiol 161: 58-66. doi:10.1016/j.resmic.2009.11.004. PubMed: 20004718.
62. Zhang XX, Zhang T, Zhang M, Fang HH, Cheng SP, (2009) Characterization and quantification of class 1 integrons and associated gene cassettes in sewage treatment plants. Appl Microbiol Biotechnol 82: 1169-1177. doi:10.1007/s00253-009-1886-y. PubMed: 19224208.
63. Léon G, Roy PH, (2003) Excision and integration of cassettes by an integron integrase of Nitrosomonas europaea. J Bacteriol 185: 2036-2041. doi:10.1128/JB.185.6.2036-2041.2003. PubMed: 12618471.
64. Hauser LJ, Land ML, Brown SD, Larimer F, Keller KL, et al. (2011) Complete genome sequence and updated annotation of Desulfovibrio alaskensis G20. J Bacteriol 193: 4268-4269. doi:10.1128/JB.05400-11. PubMed: 21685289.
65. Depardieu F, Reynolds PE, Courvalin P, (2003) VanD-type vancomycin-resistant Enterococcus faecium 10/96A. Antimicrob Agents Chemother 47: 7-18. doi:10.1128/AAC.47.1.7-18.2003. PubMed: 12499162.
66. Schleinitz KM, Vallaeys T, Kleinsteuber S, (2010) Structural characterization of ISCR8, ISCR22, and ISCR23, subgroups of IS91-like insertion elements. Antimicrob Agents Chemother 54: 4321-4328. doi:10.1128/AAC.00006-10. PubMed: 20625149.
67. 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: 1494-1502. doi:10.1128/AEM.67.4.1494-1502.2001. PubMed: 11282596.