Triclocarban Influences Antibiotic Resistance and Alters Anaerobic Digester Microbial Community Structure

Environmental Science and Technology

Volumn 50, Issue 1, 2016, Pages 126-134

  Carey, Daniel E ^a   Zitomer, Daniel H ^a   Hristova, Krassimira R ^b   Kappell, Anthony D ^b   McNamara, Patrick J ^a  

^a Marquette University   (United States)

^b Marquette University   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBIOTICS; BIOLOGICAL MATERIALS; BIOMARKERS; BIOSOLIDS; ENCODING (SYMBOLS); FATTY ACIDS; GENE ENCODING; GENES; METHANE; MICROORGANISMS; SOCIAL SCIENCES; VOLATILE FATTY ACIDS;

ANAEROBIC ENVIRONMENT; ANTIBIOTIC RESISTANCE; ANTIBIOTIC RESISTANCE GENES; BACKGROUND CONCENTRATION; MEDIAN CONCENTRATION; MICROBIAL COMMUNITY STRUCTURES; MULTIDRUG EFFLUX PUMPS; ORGANIC MICRO-POLLUTANTS;

PULP DIGESTERS;

INTEGRASE; METHANE; TRICLOCARBAN; VOLATILE FATTY ACID; CARBANILIDE DERIVATIVE;

ANTIBIOTIC RESISTANCE; COMMUNITY STRUCTURE; CONCENTRATION (COMPOSITION); GENE EXPRESSION; MICROBIAL COMMUNITY;

ACCLIMATIZATION; ANAEROBIC DIGESTION; ANTIBIOTIC RESISTANCE; ARTICLE; BIOSOLID; COMMUNITY STRUCTURE; CONTROLLED STUDY; INTEGRON; MICROBIAL COMMUNITY; MULTIDRUG RESISTANCE; NONHUMAN; TOXIC CONCENTRATION; ANAEROBIC GROWTH; DRUG EFFECTS; MICROBIAL CONSORTIUM; PHYSIOLOGY;

ANAEROBIOSIS; CARBANILIDES; DRUG RESISTANCE, BACTERIAL; MICROBIAL CONSORTIA;

EID: 84953379286     PISSN: 0013936X     EISSN: 15205851     Source Type: Journal    
DOI: 10.1021/acs.est.5b03080     Document Type: Article

References (53)

1. U.S. EPA: TCC Consortium. High Production Volume Chemical Challenge Program Data Availability and Screening Level Assessment for Triclocarban, CAS#: 101-20-2, 2002; Report No. 201-14186A; http://www.epa.gov/chemrtk/tricloca/c14186cv.pdf; pp 1-38.
2. Halden, R.; Paull, D. Co-occurrence of triclocarban and triclosan in US water resources Environ. Sci. Technol. 2005, 39 (6) 1420-1426 10.1021/es049071e
3. Heidler, J.; Sapkota, A.; Halden, R. U. Partitioning, persistence, and accumulation in digested sludge of the topical antiseptic triclocarban during wastewater treatment Environ. Sci. Technol. 2006, 40 (11) 3634-3639 10.1021/es052245n
4. Pycke, B.; Roll, I.; Brownawell, B.; Kinney, C. a; Furlong, E. T.; Kolpin, D. W.; Halden, R. U. Transformation Products and Human Metabolites of Triclocarban and Triclosan in Sewage Sludge across the United States Environ. Sci. Technol. 2014, 48, 7881-7890 10.1021/es5006362
5. U.S. EPA. TargetedNational Sewage Sludge Survey Statistical Analysis Report. (2009, EPA-822-R-08-018. Washington, D.C.
6. Oggioni, M. R.; Furi, L.; Coelho, J. R.; Maillard, J.-Y.; Martínez, J. L. Recent advances in the potential interconnection between antimicrobial resistance to biocides and antibiotics Expert Rev. Anti-Infect. Ther. 2013, 11 (4) 363-366 10.1586/eri.13.16
7. Halden, R. U. On the Need and Speed of Regulating Triclosan and Triclocarban in the United States Environ. Sci. Technol. 2014, 48 (7) 3603-3611 10.1021/es500495p
8. Carey, D. E.; McNamara, P. J. The impact of triclosan on the spread of antibiotic resistance in the environment Front. Microbiol. 2015, 5, 1-11 10.3389/fmicb.2014.00780
9. McMurry, L. M.; Oethinger, M.; Levy, S. B. Overexpression of marA, soxS, or acrAB produces resistance to triclosan in laboratory and clinical strains of Escherichia coli FEMS Microbiol. Lett. 1998, 166 (2) 305-309 10.1111/j.1574-6968.1998.tb13905.x
10. Brenwald, N.; Fraise, A. Triclosan resistance in methicillin-resistant Staphylococcus aureus (MRSA) J. Hosp. Infect. 2003, 55, 141-144 10.1016/S0195-6701(03)00222-6
11. Chen, Y.; Pi, B.; Zhou, H.; Yu, Y.; Li, L. Triclosan resistance in clinical isolates of Acinetobacter baumannii J. Med. Microbiol. 2009, 58, 1086-1091 10.1099/jmm.0.008524-0
12. Pycke, B. F. G.; Crabbé, A.; Verstraete, W.; Leys, N. Characterization of triclosan-resistant mutants reveals multiple antimicrobial resistance mechanisms in Rhodospirillum rubrum S1H Appl. Environ. Microbiol. 2010, 76 (10) 3116-3123 10.1128/AEM.02757-09
13. Son, A.; Kennedy, I. M.; Scow, K. M.; Hristova, K. R. Quantitative gene monitoring of microbial tetracycline resistance using magnetic luminescent nanoparticles J. Environ. Monit. 2010, 12 (6) 1362-1367 10.1039/c001974g
14. Levy, S. B. Active efflux, a common mechanism for biocide and antibiotic resistance J. Appl. Microbiol. 2002, 92, 65S-71S 10.1046/j.1365-2672.92.5s1.4.x
15. Chuanchuen, R.; Beinlich, K.; Hoang, T. T.; Becher, A.; Karkhoff-Schweizer, R. R.; Schweizer, H. P. Cross-Resistance between Triclosan and Antibiotics in Pseudomonas aeruginosa Is Mediated by Multidrug Efflux Pumps: Exposure of a Susceptible Mutant Strain to Triclosan Selects nfxB Mutants Overexpressing MexCD-OprJ Antimicrob. Agents Chemother. 2001, 45 (2) 428-432 10.1128/AAC.45.2.428-432.2001
16. Braoudaki, M.; Hilton, A. C. Low level of cross-resistance between triclosan and antibiotics in Escherichia coli K-12 and E. coli O55 compared to E. coli O157 FEMS Microbiol. Lett. 2004, 235 (2) 305-309 10.1111/j.1574-6968.2004.tb09603.x
17. Walsh, S. E.; Maillard, J. Y.; Russell, A. D.; Catrenich, C. E.; Charbonneau, D. L.; Bartolo, R. G. Activity and mechanisms of action of selected biocidal agents on Gram-positive and -negative bacteria J. Appl. Microbiol. 2003, 94 (2) 240-247 10.1046/j.1365-2672.2003.01825.x
18. Holzem, R. M.; Stapleton, H. M.; Gunsch, C. K. Determining the Ecological Impacts of Organic Contaminants in Biosolids Using a High-Throughput Colorimetric Denitri fi cation Assay: A Case Study with Antimicrobial Agents Environ. Sci. Technol. 2014, 48 (3) 1646-1655 10.1021/es404431k
19. Heidler, J.; Sapkota, A.; Halden, R. U. Partitioning, persistence, and accumulation in digested sludge of the topical antiseptic triclocarban during wastewater treatment Environ. Sci. Technol. 2006, 40 (11) 3634-3639 10.1021/es052245n
20. Venkatesan, A. K.; Halden, R. U. Wastewater treatment plants as chemical observatories to forecast ecological and human health risks of manmade chemicals Sci. Rep. 2014, 4 (3731) 1-7 10.1038/srep03731
21. McNamara, P. J.; Lapara, T. M.; Novak, P. J. The impacts of triclosan on anaerobic community structures, function, and antimicrobial resistance Environ. Sci. Technol. 2014, 48, 7393-7400 10.1021/es501388v
22. Urakawa, H.; Martens-Habbena, W.; Stahl, D. A. High abundance of ammonia-oxidizing archaea in coastal waters, determined using a modified DNA extraction method Appl. Environ. Microbiol. 2010, 76 (7) 2129-2135 10.1128/AEM.02692-09
23. Ramsden, S. J.; Ghosh, S.; Bohl, L. J.; Lapara, T. M. Phenotypic and genotypic analysis of bacteria isolated from three municipal wastewater treatment plants on tetracycline-amended and ciprofloxacin-amended growth media J. Appl. Microbiol. 2010, 109 (5) 1609-1618 10.1111/j.1365-2672.2010.04787.x
24. Diehl, D. L.; LaPara, T. M. Effect of temperature on the fate of genes encoding tetracycline resistance and the integrase of class 1 integrons within anaerobic and aerobic digesters treating municipal wastewater solids Environ. Sci. Technol. 2010, 44 (23) 9128-9133 10.1021/es102765a
25. Rasmussen, J. L.; Odelson, D. A.; Macrina, F. L. Complete nucleotide sequence and transcription of ermF, a macrolide-lincosamide-streptogramin B resistance determinant from Bacteroides fragilis J. Bacteriol. 1986, 168 (2) 523-533
26. Mazel, D. Integrons: agents of bacterial evolution Nat. Rev. Microbiol. 2006, 4 (8) 608-20 10.1038/nrmicro1462
27. Pruden, A.; Arabi, M.; Storteboom, H. N. Correlation between upstream human activities and riverine antibiotic resistance genes Environ. Sci. Technol. 2012, 46 (21) 11541-11549 10.1021/es302657r
28. Slapeta, J.; Dowd, S. E.; Alanazi, A. D.; Westman, M. E.; Brown, G. K. Differences in the faecal microbiome of non-diarrhoeic clinically healthy dogs and cats associated with Giardia duodenalis infection: impact of hookworms and coccidia Int. J. Parasitol. 2015, 45 (9-10) 585-594 10.1016/j.ijpara.2015.04.001
29. Kolderman, E.; Bettampadi, D.; Samarian, D.; Dowd, S. E.; Foxman, B.; Jakubovics, N. S.; Rickard, A. H. L-Arginine Destabilizes Oral Multi-Species Biofilm Communities Developed in Human Saliva PLoS One 2015, 10 (5) e0121835 10.1371/journal.pone.0121835
30. Schauer-Gimenez, A. E.; Zitomer, D. H.; Maki, J. S.; Struble, C. A. Bioaugmentation for improved recovery of anaerobic digesters after toxicant exposure Water Res. 2010, 44 (12) 3555-3564 10.1016/j.watres.2010.03.037
31. McNamara, P. J.; Krzmarzick, M. J. Triclosan enriches for Dehalococcoides-like Chloroflexi in anaerobic soil at environmentally relevant concentrations FEMS Microbiol. Lett. 2013, 344 (1) 48-52 10.1111/1574-6968.12153
32. Ahring, B. K.; Sandberg, M.; Angelidaki, I. Volatile fatty acids as indicators of process imbalance in anaerobic digestors Appl. Microbiol. Biotechnol. 1995, 43 (3) 559-565 10.1007/s002530050451
33. Hickey, R. F.; Switzenbaum, M. S. The response and utility of hydrogen and carbon monoxide as process indicators of anaerobic digesters subject to organic and hydraulic overloads Water Environ. Fed. 1991, 63 (2) 129-140
34. Russell, A. D. Do biocides select for antibiotic resistance? J. Pharm. Pharmacol. 2000, 52 (2) 227-233 10.1211/0022357001773742
35. Chapman, J. S. Biocide resistance mechanisms Int. Biodeterior. Biodegrad. 2003, 51 (2) 133-138 10.1016/S0964-8305(02)00097-5
36. Li, X. Z.; Nikaido, H.; Poole, K. Role of MexA-MexB-OprM in antibiotic efflux in Pseudomonas aeruginosa Antimicrob. Agents Chemother. 1995, 39 (9) 1948-1953 10.1128/AAC.39.9.1948
37. De Angelis, F.; Lee, J. K.; O'Connell, J. D.; Miercke, L. J. W.; Verschueren, K. H.; Srinivasan, V.; Bauvois, C.; Govaerts, C.; Robbins, R. A.; Ruysschaert, J.-M. et al. Metal-induced conformational changes in ZneB suggest an active role of membrane fusion proteins in efflux resistance systems Proc. Natl. Acad. Sci. U. S. A. 2010, 107 (24) 11038-11043 10.1073/pnas.1003908107
38. Li, X. Z.; Livermore, D. M.; Nikaido, H. Role of efflux pump(s) in intrinsic resistance of Pseudomonas aeruginosa: Resistance to tetracycline, chloramphenicol, and norfloxacin Antimicrob. Agents Chemother. 1994, 38 (8) 1732-1741 10.1128/AAC.38.8.1732
39. Poole, K.; Tetro, K.; Zhao, Q. Expression of the multidrug resistance operon mexA-mexB-oprM in Pseudomonas aeruginosa: mexR encodes a regulator of operon expression Antimicrob. Agents Chemother. 1996, 40 (9) 2021-2028
40. Pycke, B. F. G.; Vanermen, G.; Monsieurs, P.; De Wever, H.; Mergeay, M.; Verstraete, W.; Leys, N. Toxicogenomic response of Rhodospirillum rubrum S1H to the micropollutant triclosan Appl. Environ. Microbiol. 2010, 76 (11) 3503-3513 10.1128/AEM.01254-09
41. Zhang, T.; Zhang, X.-X.; Ye, L. Plasmid metagenome reveals high levels of antibiotic resistance genes and mobile genetic elements in activated sludge PLoS One 2011, 6 (10) e26041 10.1371/journal.pone.0026041
42. Munir, M.; Xagoraraki, I. Levels of Antibiotic Resistance Genes in Manure, Biosolids, and Fertilized Soil J. Environ. Qual. 2011, 40 (1) 248 10.2134/jeq2010.0209
43. Burch, T. R.; Sadowsky, M. J.; LaPara, T. M. Air-drying beds reduce the quantities of antibiotic resistance genes and class 1 integrons in residual municipal wastewater solids Environ. Sci. Technol. 2013, 47 (17) 9965-9971 10.1021/es4024749
44. Ma, Y.; Wilson, C. A.; Novak, J. T.; Riffat, R.; Aynur, S.; Murthy, S.; Pruden, A. Effect of various sludge digestion conditions on sulfonamide, macrolide, and tetracycline resistance genes and class I integrons Environ. Sci. Technol. 2011, 45 (18) 7855-7861 10.1021/es200827t
45. Ghosh, S.; Ramsden, S. J.; LaPara, T. M. The role of anaerobic digestion in controlling the release of tetracycline resistance genes and class 1 integrons from municipal wastewater treatment plants Appl. Microbiol. Biotechnol. 2009, 84 (4) 791-796 10.1007/s00253-009-2125-2
46. Patel, G. B.; Sprott, G. D.; Fein, J. E. Isolation and Characterization of Methanobacterium espanolae sp. nov., a Mesophilic, Moderately Acidiphilic Methanogen Int. J. Syst. Bacteriol. 1990, 40 (1) 12-18 10.1099/00207713-40-1-12
47. Raoult, D.; Ogata, H.; Robert, C.; Suhre, K.; Drancourt, M.; Claverie, J. Tropheryma whipplei Twist: A Human Pathogenic Actinobacteria With a Reduced Genome Genome Res. 2003, 13 (8) 1800-1809 10.1101/gr.1474603
48. Shimizu, T.; Ohtani, K.; Hirakawa, H.; Ohshima, K.; Yamashita, A.; Shiba, T.; Ogasawara, N.; Hattori, M.; Kuhara, S.; Hayashi, H. Complete genome sequence of Clostridium perfringens, an anaerobic flesh-eater Proc. Natl. Acad. Sci. U. S. A. 2002, 99 (2) 996-1001 10.1073/pnas.022493799
49. Russell, J. B.; Rychlik, J. L. Factors that alter rumen microbial ecology Science 2001, 292 (5519) 1119-1122 10.1126/science.1058830
50. Boskey, E. R.; Telsch, K. M.; Whaley, K. J.; Moench, T. R.; Cone, R. A. Acid production by vaginal flora in vitro is consistent with the rate and extent of vaginal acidification Infect. Immun. 1999, 67 (10) 5170-5175
51. Boyanova, L.; Kolarov, R.; Gergova, G.; Dimitrova, L.; Mitov, I. Trends in antibiotic resistance in Prevotella species from patients of the University Hospital of Maxillofacial Surgery, Sofia, Bulgaria, in 2003-2009 Anaerobe 2010, 16 (5) 489-492 10.1016/j.anaerobe.2010.07.004
52. Bouallagui, H.; Torrijos, M.; Godon, J. J.; Moletta, R.; Cheikh, R. B.; Touhami, Y.; Delgenes, J. P.; Hamdi, M. Microbial monitoring by molecular tools of a two-phase anaerobic bioreactor treating fruit and vegetable wastes Biotechnol. Lett. 2004, 26 (10) 857-862 10.1023/B:BILE.0000025892.19733.18
53. Chen, S.; Dong, X. Proteiniphilum acetatigenes gen. nov., sp. nov., from a UASB reactor treating brewery wastewater Int. J. Syst. Evol. Microbiol. 2005, 55 (6) 2257-2261 10.1099/ijs.0.63807-0