The use of greywater for irrigation is becoming a common practice in arid regions such as the Southwestern US, the Middle East, Australia, and China. While greywater supplies nutrients to soil ecosystems, the possible impact of trace contaminants, particularly pharmaceuticals and personal care products, has not been determined. This paper examined the impact of triclosan, an antibacterial agent commonly added to consumer products, on microbial populations and microbial diversity in soil irrigated with greywater. While there was no change in the total number of heterotrophic microorganisms in the soil, both the types and the antibiotic resistance of the microorganisms were significantly influenced by triclosan. The proportion of the microbial isolates resistant to antibiotics increased while at the same time, overall diversity of the microbial community decreased. 1. Introduction Greywater (GW) is the used water from households,excluding sewage from toilets and, in some countries, waste materials from food preparation [1–3]. Greywater accounts for between 50 to 80% of wastewater coming from individual households [3–5]. The use of GW for the irrigation of lawns, ornamental plants, and other landscape vegetation has become an accepted practice in the Southwest US, the Middle East, and the Australian dry lands [4–6]. While GW irrigation is practiced primarily in arid regions, changing climate patterns, increased water demand associated with urbanization, and increased awareness of the need for water conservation will likely make water reuse more important in temperate regions [7–10]. Domestic GW differs in composition from typical domestic wastewater [11–13]. Greywater is highly variable in composition depending on the number and lifestyle of the residents in a household [11, 14, 15]. Greywater is notable for the high concentration of soaps, detergents, and oils it contains [12, 16]. In addition, GW has pharmaceuticals and personal care products (PPCPs), including antimicrobial agents such as triclosan, at concentrations equal to or higher than those in domestic wastewater [2, 17]. Triclosan (TCS; 5-chloro-2-(2, 4-dichlorophenoxy) phenol; CAS no. 9012-63-9) is the most commonly used antibacterial agent in the US. Current estimates are that the discharge of this compound into the US environment is in the range of 300,000–500,000？kg？yr？1 and use is increasing rapidly [18–21]. Triclosan is found in numerous products including clothing, toys, toothbrushes, rubber, hand soaps, toothpaste, deodorants, and laundry detergents [20]. A concentration of 0.1–0.3% of
References
[1]
R. K. Misra, J. H. Patel, and V. R. Baxi, “Reuse potential of laundry greywater for irrigation based on growth, water and nutrient use of tomato,” Journal of Hydrology, vol. 386, no. 1–4, pp. 95–102, 2010.
[2]
E. Donner, E. Eriksson, D. M. Revitt, L. Scholes, H. C. H. Lützh？ft, and A. Ledin, “Presence and fate of priority substances in domestic greywater treatment and reuse systems,” Science of the Total Environment, vol. 408, no. 12, pp. 2444–2451, 2010.
[3]
K. H. Baker, D. I. Harrow, and B. A. Ritchey, “Tricosan in greywater: implications for reuse,” in Low Impact Development 2010: Redefining Water in the City. Proceeding of the International Low Impact Development Conference, pp. 1036–1048, San Francisco, Calif, USA, April 2010.
[4]
O. Al-Jayyousi, “Greywater reuse: knowledge management for sustainability,” Desalination, vol. 167, no. 1–3, pp. 27–37, 2004.
[5]
D. Christova-Boal, R. E. Eden, and S. McFarlane, “Investigation into greywater reuse for urban residential properties,” Desalination, vol. 106, no. 1–3, pp. 391–397, 1996.
[6]
E. Madungwe and S. Sakuringwa, “Greywater reuse: a strategy for water demand management in Harare?” Physics and Chemistry of the Earth, Parts A/B/C, vol. 32, no. 15–18, pp. 1231–1236, 2007.
[7]
S. Godfrey, P. Labhasetwar, and S. Wate, “Greywater reuse in residential schools in Madhya Pradesh, India—a case study of cost-benefit analysis,” Resources, Conservation and Recycling, vol. 53, no. 5, pp. 287–293, 2009.
[8]
E. Friedler, R. Kovalio, and N. I. Galil, “On-site greywater treatment and reuse in multi-storey buildings,” Water Science and Technology, vol. 51, no. 10, pp. 187–194, 2005.
[9]
R. H. Kim, S. Lee, J. Jeong, J. H. Lee, and Y. K. Kim, “Reuse of greywater and rainwater using fiber filter media and metal membrane,” Desalination, vol. 202, no. 1–3, pp. 326–332, 2007.
[10]
L. Domènech and D. Saurí, “A comparative appraisal of the use of rainwater harvesting in single and multi-family buildings of the Metropolitan Area of Barcelona (Spain): social experience, drinking water savings and economic costs,” Journal of Cleaner Production, vol. 19, no. 6-7, pp. 598–608, 2010.
[11]
L. M. Casanova, C. P. Gerba, and M. Karpiscak, “Chemical and microbial characterization of household graywater,” Journal of Environmental Science and Health Part A, vol. 36, no. 4, pp. 395–401, 2001.
[12]
A. Gross, N. Azulai, G. Oron, M. Arnold, A. Nejidat, and Z. Ronen, “Environmental impact and health risks associated with greywater irrigation: a case study,” Water Science and Technology, vol. 52, no. 8, pp. 161–169, 2005.
[13]
R. Birks, J. Colbourne, and R. Hobson, “Microbiological water quality in a large in-building, water recycling facility,” Water Science and Technology, vol. 50, no. 2, pp. 165–172, 2004.
[14]
B. Jefferson, A. Palmer, P. Jeffrey, R. Stuetz, and S. Judd, “Grey water characterisation and its impact on the selection and operation of technologies for urban reuse,” Water Science and Technology, vol. 50, no. 2, pp. 157–164, 2004.
[15]
E. Eriksson, H. R. Andersen, T. S. Madsen, and A. Ledin, “Greywater pollution variability and loadings,” Ecological Engineering, vol. 35, no. 5, pp. 661–669, 2009.
[16]
T. Wind, U. Werner, M. Jacob, and A. Hauk, “Environmental concentrations of boron, LAS, EDTA, NTA and Triclosan simulated with GREAT-ER in the river Itter,” Chemosphere, vol. 54, no. 8, pp. 1135–1144, 2004.
[17]
E. Eriksson, K. Auffarth, A. M. Eilersen, M. Henze, and A. Ledin, “Household chemicals and personal care products as sources for xenobiotic organic compounds in grey wastewater,” Water SA, vol. 29, no. 2, pp. 135–146, 2003.
[18]
A. I. Sch？fer, L. D. Nghiem, and N. Oschmann, “Bisphenol A retention in the direct ultrafiltration of greywater,” Journal of Membrane Science, vol. 283, no. 1-2, pp. 233–243, 2006.
[19]
M. Adolfsson-Erici, M. Pettersson, J. Parkkonen, and J. Sturve, “Triclosan, a commonly used bactericide found in human milk and in the aquatic environment in Sweden,” Chemosphere, vol. 46, no. 9-10, pp. 1485–1489, 2002.
[20]
R. U. Halden and D. H. Paull, “Co-occurrence of triclocarban and triclosan in U.S. water resources,” Environmental Science and Technology, vol. 39, no. 6, pp. 1420–1426, 2005.
[21]
H. Singer, S. Müller, C. Tixier, and L. Pillonel, “Triclosan: occurrence and fate of a widely used biocide in the aquatic environment: field measurements in wastewater treatment plants, surface waters, and lake sediments,” Environmental Science and Technology, vol. 36, no. 23, pp. 4998–5004, 2002.
[22]
L. M. McMurry, M. Oethinger, and S. B. Levy, “Overexpression of marA, soxS, or acrAB produces resistance to triclosan in laboratory and clinical strains of Escherichia coli,” FEMS Microbiology Letters, vol. 166, no. 2, pp. 305–309, 1998.
[23]
G. McDonnell and D. Pretzer, “Action and targets of triclosan,” ASM News, vol. 64, pp. 670–671, 1998.
[24]
Y. Ji, D. Yin, B. Fox, D. J. Holmes, D. Payne, and M. Rosenberg, “Validation of antibacterial mechanism of action using regulated antisense RNA expression in Staphylococcus aureus,” FEMS Microbiology Letters, vol. 231, no. 2, pp. 177–184, 2004.
[25]
S. B. Levy, “Antibacterial household products: cause for concern,” Emerging Infectious Diseases, vol. 7, no. 3, pp. 512–515, 2001.
[26]
S. B. Levy, “Factors impacting on the problem of antibiotic resistance,” Journal of Antimicrobial Chemotherapy, vol. 49, no. 1, pp. 25–30, 2002.
[27]
L. Biro？ová and M. Mikulá？ová, “Development of triclosan and antibiotic resistance in Salmonella enterica serovar Typhimurium,” Journal of Medical Microbiology, vol. 58, no. 4, pp. 436–441, 2009.
[28]
Y. Chen, B. Pi, H. Zhou, N. Yu, and L. Li, “Triclosan resistance in clinical isolates of Acinetobacter baumannii,” Journal of Medical Microbiology, vol. 58, no. 8, pp. 1086–1091, 2009.
[29]
J. L. Copitch, R. N. Whitehead, and M. A. Webber, “Prevalence of decreased susceptibility to triclosan in Salmonella enterica isolates from animals and humans and association with multiple drug resistance,” International Journal of Antimicrobial Agents, vol. 36, no. 3, pp. 247–251, 2010.
[30]
B. F. G. Pycke, A. Crabbé, W. Verstraete, and N. Leys, “Characterization of triclosan-resistant mutants reveals multiple antimicrobial resistance mechanisms in rhodospirillum rubrum S1H,” Applied and Environmental Microbiology, vol. 76, no. 10, pp. 3116–3123, 2010.
[31]
A. D. Russell, “Biocide use and antibiotic resistance: the relevance of laboratory findings to clinical and environmental situations,” The Lancet Infectious Diseases, vol. 3, no. 12, pp. 794–803, 2003.
[32]
A. D. Russell, “Whither triclosan?” Journal of Antimicrobial Chemotherapy, vol. 53, no. 5, pp. 693–695, 2004.
[33]
R. G. Ledder, P. Gilbert, C. Willis, and A. J. McBain, “Effects of chronic triclosan exposure upon the antimicrobial susceptibility of 40 ex-situ environmental and human isolates,” Journal of Applied Microbiology, vol. 100, no. 5, pp. 1132–1140, 2006.
[34]
A. Cottell, S. P. Denyer, G. W. Hanlon, D. Ochs, and J. Y. Maillard, “Triclosan-tolerant bacteria: changes in susceptibility to antibiotics,” Journal of Hospital Infection, vol. 72, no. 1, pp. 71–76, 2009.
[35]
H. Almqvist and J. Han？us, “Organic hazardous substances in graywater from Swedish households,” Journal of Environmental Engineering, vol. 132, no. 8, pp. 901–908, 2006.
[36]
G. G. Ying and R. S. Kookana, “Triclosan in wastewaters and biosolids from Australian wastewater treatment plants,” Environment International, vol. 33, no. 2, pp. 199–205, 2007.
[37]
M. Ricart, H. Guasch, M. Alberch et al., “Triclosan persistence through wastewater treatment plants and its potential toxic effects on river biofilms,” Aquatic Toxicology, vol. 100, no. 4, pp. 346–353, 2010.
[38]
J. L. Wu, N. P. Lam, D. Martens, A. Kettrup, and Z. Cai, “Triclosan determination in water related to wastewater treatment,” Talanta, vol. 72, no. 5, pp. 1650–1654, 2007.
[39]
Z. Li, F. Boyle, and A. Reynolds, “Rainwater harvesting and greywater treatment systems for domestic application in Ireland,” Desalination, vol. 260, no. 1–3, pp. 1–8, 2010.
[40]
M. Kraume, R. Scheumann, A. Baban, and B. El Hamouri, “Performance of a compact submerged membrane sequencing batch reactor (SM-SBR) for greywater treatment,” Desalination, vol. 250, no. 3, pp. 1011–1013, 2010.
[41]
A. Gross, O. Shmueli, Z. Ronen, and E. Raveh, “Recycled vertical flow constructed wetland (RVFCW)-a novel method of recycling greywater for irrigation in small communities and households,” Chemosphere, vol. 66, no. 5, pp. 916–923, 2007.
[42]
A. Gross, D. Kaplan, and K. Baker, “Removal of chemical and microbiological contaminants from domestic greywater using a recycled vertical flow bioreactor (RVFB),” Ecological Engineering, vol. 31, no. 2, pp. 107–114, 2007.
[43]
B. O. Clarke and S. R. Smith, “Review of ‘emerging’ organic contaminants in biosolids and assessment of international research priorities for the agricultural use of biosolids,” Environment International, vol. 37, no. 1, pp. 226–247, 2011.
[44]
A. J. Al-Rajab, L. Sabourin, A. Scott, D. R. Lapen, and E. Topp, “Impact of biosolids on the persistence and dissipation pathways of triclosan and triclocarban in an agricultural soil,” Science of the Total Environment, vol. 407, no. 23, pp. 5978–5985, 2009.
[45]
J. Cha and A. M. Cupples, “Detection of the antimicrobials triclocarban and triclosan in agricultural soils following land application of municipal biosolids,” Water Research, vol. 43, no. 9, pp. 2522–2530, 2009.
[46]
D. R. Lapen, E. Topp, C. D. Metcalfe et al., “Pharmaceutical and personal care products in tile drainage following land application of municipal biosolids,” Science of the Total Environment, vol. 399, no. 1–3, pp. 50–65, 2008.
[47]
J. Cha and A. M. Cupples, “Triclocarban and triclosan biodegradation at field concentrations and the resulting leaching potentials in three agricultural soils,” Chemosphere, vol. 81, no. 4, pp. 494–499, 2010.
[48]
G. G. Ying, X. Y. Yu, and R. S. Kookana, “Biological degradation of triclocarban and triclosan in a soil under aerobic and anaerobic conditions and comparison with environmental fate modelling,” Environmental Pollution, vol. 150, no. 3, pp. 300–305, 2007.
[49]
X. Chen, U. Pauly, S. Rehfus, and K. Bester, “Personal care compounds in a reed bed sludge treatment system,” Chemosphere, vol. 76, no. 8, pp. 1094–1101, 2009.
[50]
G. Guillaume, D. Verbrugge, M. L. Chasseur-Libotte, W. Moens, and J. M. Collard, “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 Microbiology Ecology, vol. 32, no. 1, pp. 77–85, 2000.
[51]
H. Insam and M. Goberna, “Use of Biolog？ for the community level physiological profiling (CLPP) of environmental samples,” in Molecular Microbial Ecology: Manual, pp. 853–860, Kluwer Academic Publishers, Dordrecht, The Netherlands, 2nd edition, 2004.
[52]
J. C. Zak, M. R. Willig, D. L. Moorhead, and H. G. Wildman, “Functional diversity of microbial communities: a quantitative approach,” Soil Biology and Biochemistry, vol. 26, no. 9, pp. 1101–1108, 1994.
[53]
M. Stachowiak, S. E. Clark, R. E. Templin, and K. H. Baker, “Tetracycline-resistant Escherichia coli in a small stream receiving fish hatchery effluent,” Water, Air, and Soil Pollution, vol. 211, no. 1–4, pp. 251–259, 2010.
[54]
D. I. Harrow and K. H. Baker, “Triclosan in greywater: implications for reuse,” in World Environmental and Water Resources Congress 2010: Challenges of Change. EWRI/ASCE Providence, Providence, RI, USA, May 2010.
[55]
W. R. Cookson, A. J. O'Donnell, C. D. Grant, P. F. Grierson, and D. V. Murphy, “Impact of ecosystem management on microbial community level physiological profiles of postmining forest rehabilitation,” Microbial Ecology, vol. 55, no. 2, pp. 321–332, 2008.
[56]
X. Wang, M. Song, C. Gao et al., “Carbendazim induces a temporary change in soil bacterial community structure,” Journal of Environmental Sciences, vol. 21, no. 12, pp. 1679–1683, 2009.
[57]
S. M. Ndaw, A. C. Gama-Rodrigues, E. F. Gama-Rodrigues, K. R. N. Sales, and A. S. Rosado, “Relationships between bacterial diversity, microbial biomass, and litter quality in soils under different plant covers in northern Rio de Janeiro State, Brazil,” Canadian Journal of Microbiology, vol. 55, no. 9, pp. 1089–1095, 2009.
[58]
E. Slabbert, R. Y. Kongor, K. J. Esler, and K. Jacobs, “Microbial diversity and community structure in Fynbos soil,” Molecular Ecology, vol. 19, no. 5, pp. 1031–1041, 2010.
[59]
A. M. Derry, W. J. Staddon, and J. T. Trevors, “Functional diversity and community structure of microorganisms in uncontaminated and creosote-contaminated soils as determined by sole-carbon-source-utilization,” World Journal of Microbiology and Biotechnology, vol. 14, no. 4, pp. 571–578, 1998.
[60]
D. E. Lewis, J. R. White, D. Wafula et al., “Soil functional diversity analysis of a bauxite-mined restoration chronosequence,” Microbial Ecology, vol. 59, no. 4, pp. 710–723, 2010.
[61]
J. A. H. Anderson, M. J. Hooper, J. C. Zak, and S. B. Cox, “Characterization of the structural and functional diversity of indigenous soil microbial communities in smelter-impacted and nonimpacted soils,” Environmental Toxicology and Chemistry, vol. 28, no. 3, pp. 534–541, 2009.
[62]
M. Farré, D. Asperger, L. Kantiani, S. González, M. Petrovic, and D. Barceló, “Assessment of the acute toxicity of triclosan and methyl triclosan in wastewater based on the bioluminescence inhibition of Vibrio fischeri,” Analytical and Bioanalytical Chemistry, vol. 390, no. 8, pp. 1999–2007, 2008.
[63]
O. R. Price, R. J. Williams, R. van Egmond, M. J. Wilkinson, and M. J. Whelan, “Predicting accurate and ecologically relevant regional scale concentrations of triclosan in rivers for use in higher-tier aquatic risk assessments,” Environment International, vol. 36, no. 6, pp. 521–526, 2010.
[64]
J. Kim, J. Park, P. G. Kim, C. Lee, K. Choi, and K. Choi, “Implication of global environmental changes on chemical toxicity—effect of water temperature, pH, and ultraviolet B irradiation on acute toxicity of several pharmaceuticals in Daphnia magna,” Ecotoxicology, vol. 19, no. 4, pp. 662–669, 2010.
[65]
L. Canesi, C. Ciacci, L. C. Lorusso et al., “Effects of Triclosan on Mytilus galloprovincialis hemocyte function and digestive gland enzyme activities: possible modes of action on non target organisms,” Comparative Biochemistry and Physiology Part C, vol. 145, no. 3, pp. 464–472, 2007.
[66]
R. Oliveira, I. Domingues, C. K. Grisolia, and A. M. V. M. Soares, “Effects of triclosan on zebrafish early-life stages and adults,” Environmental Science and Pollution Research, vol. 16, no. 6, pp. 679–688, 2009.
[67]
D. Lin, Q. Zhou, X. Xie, and Y. Liu, “Potential biochemical and genetic toxicity of triclosan as an emerging pollutant on earthworms (Eisenia fetida),” Chemosphere, vol. 81, no. 10, pp. 1328–1333, 2010.
[68]
F. Liu, G. G. Ying, L. H. Yang, and Q. X. Zhou, “Terrestrial ecotoxicological effects of the antimicrobial agent triclosan,” Ecotoxicology and Environmental Safety, vol. 72, no. 1, pp. 86–92, 2009.
