Skip to main content

Effect of copper and zinc on microbial tolerance to triclosan in two soil types

Abstract

Purpose

Sewage sludge and biosolid application to land is a common approach to fertilise soils, but sewage-derived contaminants like the antimicrobial agent triclosan, and heavy metals zinc and copper, are known to affect soil microbial communities. In this study, the tolerance to triclosan was examined for soil microbial communities chronically pre-exposed to one of two heavy metals (Cu or Zn) and the antimicrobial triclosan. This was investigated in two different soil types.

Materials and methods

The impacts of chronic exposure of copper, zinc and triclosan as individual compounds or in mixtures on soil microbial communities were assessed in soils collected from two sites. The first was a Horotiu sandy loam with ample carbon and nitrogen levels and the second was a Templeton silt loam with very low carbon and nitrogen levels. The end points used to characterise the response of the soil microbial community were biomass, metabolic activity and pollution-induced community tolerance (PICT) to triclosan (using Biolog EcoPlates). In addition, metabolic activities for individual substrates were examined and those that significantly changed with the applied treatments were identified.

Results and discussion

Exposure to mixtures of both triclosan and copper in the Horotiu sandy loam reduced microbial biomass, increased metabolic activity and reduced microbial tolerance to triclosan. The decrease in soil microbial tolerance correlated with an increased metabolic activity for N-acetyl-d-glucosamine providing a potential link between triclosan exposure and nitrogen mineralisation. Exposure to both triclosan and high zinc levels decreased microbial biomass in the Horotiu sandy loam but did not have an effect on microbial tolerance to triclosan. In the finer-textured and less fertile Templeton soil, microbial tolerance to triclosan and the microbial biomass were not impacted by copper/triclosan or zinc/triclosan mixtures.

Conclusions

Mixture effects could become a cause for concern when soil microbial communities are exposed to triclosan in fertile soils with copper concentrations in excess of 50 mg kg−1 and could be especially important in the more coarsely textured soils. Current regulations for soil contaminants only consider the risk and effects of single contaminants. Greater protection of soil resources could result from considering mixture effects and soil types.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3

References

  • Al-Rajab AJ, Sabourin L, Scott A, Lapen DR, Topp E (2009) Impact of biosolids on the persistence and dissipation pathways of triclosan and triclocarban in an agricultural soil. Sci Total Environ 407:5978–5985

    CAS  Article  Google Scholar 

  • An J, Zhou Q, Sun Y, Xu Z (2009) Ecotoxicological effects of typical personal care products on seed germination and seedling development of wheat (Triticum aestivum L.). Chemosphere 76:1428–1434

    CAS  Article  Google Scholar 

  • Bååth E, Díaz-Raviña M, Frostegård Å, Campbell CD (1998) Effect of metal-rich sludge amendments on the soil microbial community. Appl Environ Microbiol 64:238–245

    Google Scholar 

  • Backhaus T, Porsbring T, Arrhenius A, Brosche S, Johansson P, Blanck H (2011) Single-substance and mixture toxicity of five pharmaceuticals and personal care products to marine periphyton communities. Environ Toxicol Chem 30:2030–2040

    CAS  Article  Google Scholar 

  • Baker-Austin C, Wright MS, Stepanauskas R, McArthur JV (2006) Co-selection of antibiotic and metal resistance. Trends Microbiol 14:176–182

    CAS  Article  Google Scholar 

  • Bedoux G, Roig B, Thomas O, Dupont V, Le Bot B (2012) Occurrence and toxicity of antimicrobial triclosan and by-products in the environment. Environ Sci Pollut Res 19:1044–1065

    CAS  Article  Google Scholar 

  • Berg J, Thorsen MK, Holm PE, Jensen J, Nybroe O, Brandt KK (2010) Cu exposure under field conditions coselects for antibiotic resistance as determined by a novel cultivation-independent bacterial community tolerance assay. Environ Sci Technol 44:8724–8728

    CAS  Article  Google Scholar 

  • Berg J, Brandt KK, Al-Soud WA, Holm PE, Hansen LH, Sørensen SJ, Nybroe O (2012) Selection for Cu-tolerant bacterial communities with altered composition, but unaltered richness, via long-term cu exposure. Appl Environ Microbiol 78:7438–7446

    CAS  Article  Google Scholar 

  • Brading MG, Cromwell VJ, Jones NM, Baldeckand JD, Marquis RE (2003) Anti-microbial efficacy and mode of action studies on a new zinc/triclosan formulation. Int Dent J 53:363–370

    CAS  Article  Google Scholar 

  • Brandt KK, Frandsen RJN, Holm PE, Nybroe O (2010) Development of pollution-induced community tolerance is linked to structural and functional resilience of a soil bacterial community following a five-year field exposure to copper. Soil Biol Biochem 42:748–757

    CAS  Article  Google Scholar 

  • Brinch UC, Ekelund F, Jacobsen CS (2002) Method for spiking soil samples with organic compounds. Appl Environ Microbiol 68:1808–1816

    CAS  Article  Google Scholar 

  • Butler E, Whelan MJ, Ritz K, Sakrabani R, van Egmond R (2012) The effect of triclosan on microbial community structure in three soils. Chemosphere 89:1–9

    CAS  Article  Google Scholar 

  • Carey DE, McNamara PJ (2015) The impact of triclosan on the spread of antibiotic resistance in the environment. Front Microbiol. doi:10.3389/fmicb.2014.00780

    Google Scholar 

  • Chen J, Ahn KC, Gee NA, Gee SJ, Hammock BD, Lasley BL (2007) Antiandrogenic properties of parabens and other phenolic containing small molecules in personal care products. Toxicol Appl Pharmacol 221:278–284

    CAS  Article  Google Scholar 

  • Christian B, Lind O (2006) Key issues concerning Biolog use for aerobic and anaerobic freshwater bacterial community-level physiological profiling. Int Rev Hydrobiol 91:257–268

    Article  Google Scholar 

  • Cole EC, Addison RM, Rubino JR, Leese KE, Dulaney PD, Newell MS, Wilkins J, Gaber DJ, Wineinger T, Criger DA (2003) Investigation of antibiotic and antibacterial agent cross-resistance in target bacteria from homes of antibacterial product users and nonusers. J Appl Microbiol 95:664–676

    CAS  Article  Google Scholar 

  • DeLorenzo ME, Keller JM, Arthur CD, Finnegan MC, Harper HE, Winder VL, Zdankiewicz DL (2008) Toxicity of the antimicrobial compound triclosan and formation of the metabolite methyl-triclosan in estuarine systems. Environ Toxicol 23:224–232

    CAS  Article  Google Scholar 

  • Department of Environment UK (1989) Code of practice for the agricultural use of sewage sludge

  • European Commission Scientific Committee on Consumer Safety (2010) Opinion on triclosan—antimicrobial resistance. doi: 10:10.2772/11162

  • Foran CM, Bennett ER, Benson WH (2000) Developmental evaluation of a potential non-steroidal estrogen: triclosan. Mar Environ Res 50:153–156

    CAS  Article  Google Scholar 

  • Gee RH, Charles A, Taylor N, Darbre PD (2008) Oestrogenic and androgenic activity of triclosan in breast cancer cells. J Appl Toxicol 28:78–91

    CAS  Article  Google Scholar 

  • Gielen GJHP, Clinton PW, Van den Heuvel MR, Kimberley MO, Greenfield LG (2011) Influence of sewage and pharmaceuticals on soil microbial function. Environ Toxicol Chem 30:1086–1095

    CAS  Article  Google Scholar 

  • Giller KE, Witter E, McGrath SP (1998) Toxicity of heavy metals to microorganisms and microbial processes in agricultural soils: a review. Soil Biol Biochem 30:1389–1414

    CAS  Article  Google Scholar 

  • Girvan MS, Bullimore J, Pretty JN, Osborn AM, Ball AS (2003) Soil type is the primary determinant of the composition of the total and active bacterial communities in arable soils. Appl Environ Microbiol 69:1800–1809

    CAS  Article  Google Scholar 

  • Gomez Escalada M, Russell AD, Maillard JY, Ochs D (2005) Triclosan-bacteria interactions: single or multiple target sites? Lett Appl Microbiol 41:476–481

    CAS  Article  Google Scholar 

  • Guillén J, Bernabeu A, Shapiro S, Villalaín J (2004) Location and orientation of triclosan in phospholipid model membranes. Eur Biophys J 33:448–453

    Article  Google Scholar 

  • Heath RJ, Yu YT, Shapiro MA, Olson E, Rock CO (1998) Broad spectrum antimicrobial biocides target the FabI component of fatty acid synthesis. J Biol Chem 273:30316–30320

    CAS  Article  Google Scholar 

  • Heidler J, Halden RU (2007) Mass balance assessment of triclosan removal during conventional sewage treatment. Chemosphere 66:362–369

    CAS  Article  Google Scholar 

  • Hewitt AE (1998) New Zealand soil classification. Landcare research science series 1. Manaaki Whenua. Landcare Research New Zealand Ltd, Lincoln

    Google Scholar 

  • Hinther A, Bromba CM, Wulff JE, Helbing CC (2011) Effects of triclocarban, triclosan, and methyl triclosan on thyroid hormone action and stress in frog and mammalian culture systems. Environ Sci Technol 45:5395–5402

    CAS  Article  Google Scholar 

  • Horswell J, Prosser JA, Siggins A, van Schaik A, Ying L, Ross C, McGill A, Northcott G (2014) Assessing the impacts of chemical cocktails on the soil ecosystem. Soil Biol Biochem 75:64–72

    CAS  Article  Google Scholar 

  • Ihssen J, Egli T (2005) Global physiological analysis of carbon- and energy-limited growing Escherichia coli confirms a high degree of catabolic flexibility and preparedness for mixed substrate utilization. Environ Microbiol 7:1568–1581

    CAS  Article  Google Scholar 

  • Ishibashi H, Matsumura N, Hirano M, Matsuoka M, Shiratsuchi H, Ishibashi Y, Takao Y, Arizono K (2004) Effects of triclosan on the early life stages and reproduction of medaka Oryzias latipes and induction of hepatic vitellogenin. Aquat Toxicol 67:167–179

    CAS  Article  Google Scholar 

  • Jain PK, Ramachandran S, Shukla V, Bhakuni D, Verma SK (2009) Characterization of metal and antibiotic resistance in a bacterial population isolated from a copper mining industry. Int J Integr Biol 6:57–61

    CAS  Google Scholar 

  • Jones RD, Jampani HB, Newman JL, Lee AS (2000) Triclosan: a review of effectiveness and safety in health care settings. Am J Infect Control 28:184–196

    CAS  Article  Google Scholar 

  • Karnjanapiboonwong A, Morse AN, Maul JD, Anderson TA (2010) Sorption of estrogens, triclosan, and caffeine in a sandy loam and a silt loam soil. J Soils Sediments 10:1300–1307

    CAS  Article  Google Scholar 

  • Kemper N (2008) Veterinary antibiotics in the aquatic and terrestrial environment. Ecol Indicators 8:1–13

    CAS  Article  Google Scholar 

  • Klimek B (2012) Effect of long-term zinc pollution on soil microbial community resistance to repeated contamination. B Environ Contam Tox 88:617–622

    CAS  Article  Google Scholar 

  • Kookana RS, Ying GG, Waller NJ (2011) Triclosan: its occurrence, fate and effects in the Australian environment. Water Sci Technol 63:598–604

    CAS  Article  Google Scholar 

  • Kumar V, Chakraborty A, Kural MR, Roy P (2009) Alteration of testicular steroidogenesis and histopathology of reproductive system in male rats treated with triclosan. Reprod Toxicol 27:177–185

    CAS  Article  Google Scholar 

  • Ledder RG, Gilbert P, Willis C, McBain AJ (2006) Effects of chronic triclosan exposure upon the antimicrobial susceptibility of 40 ex-situ environmental and human isolates. J Appl Microbiol 100:1132–1140

    CAS  Article  Google Scholar 

  • Li Y, Liu B, Zhang X, Gao M, Wang J (2015) Effects of Cu exposure on enzyme activities and selection for microbial tolerances during swine-manure composting. J Hazard Mater 283:512–518

    CAS  Article  Google Scholar 

  • Lindström A, Buerge IJ, Poiger T, Bergqvist PA, Müller MD, Buser HR (2002) Occurrence and environmental behavior of the bactericide triclosan and its methyl derivative in surface waters and in wastewater. Environ Sci Technol 36:2322–2329

    Article  Google Scholar 

  • Liu F, Ying G-G, Yang L-H, Zhou Q-X (2009) Terrestrial ecotoxicological effects of the antimicrobial agent triclosan. Ecotoxicol Environ Saf 72:86–92

    CAS  Article  Google Scholar 

  • Lozano N, Rice CP, Ramirez M, Torrents A (2012) Fate of triclosan and methyltriclosan in soil from biosolids application. Environ Pollut 160:103–108

    CAS  Article  Google Scholar 

  • Macdonald CA, Singh BK, Peck JA, van Schaik AP, Hunter LC, Horswell J, Campbell CD, Speir TW (2007) Long-term exposure to Zn-spiked sewage sludge alters soil community structure. Soil Biol Biochem 39:2576–2586

    CAS  Article  Google Scholar 

  • Matsumura N, Ishibashi H, Hirano M, Nagao Y, Watanabe N, Shiratsuchi H, Kai T, Nishimura T, Kashiwagi A, Arizono K (2005) Effects of nonylphenol and triclosan on production of plasma vitellogenin and testosterone in male South African clawed frogs (Xenopus laevis). Biol Pharm Bull 28:1748–1751

    CAS  Article  Google Scholar 

  • McAvoy DC, Schatowitz B, Jacob M, Hauk A, Eckhoff WS (2002) Measurement of triclosan in wastewater treatment systems. Environ Toxicol Chem 21:1323–1329

    CAS  Article  Google Scholar 

  • McBain AJ, Ledder RG, Sreenivasan P, Gilbert P (2004) Selection for high-level resistance by chronic triclosan exposure is not universal. J Antimicrob Chemoth 53:772–777

    CAS  Article  Google Scholar 

  • McClellan K, Halden RU (2010) Pharmaceuticals and personal care products in archived U.S. biosolids from the 2001 EPA national sewage sludge survey. Water Res 44:658–668

    CAS  Article  Google Scholar 

  • McMurry LM, Oethinger M, Levy SB (1998) Triclosan targets lipid synthesis. Nature 394:531–532

    CAS  Article  Google Scholar 

  • Mininni G, Blanch AR, Lucena F, Berselli S (2015) EU policy on sewage sludge utilization and perspectives on new approaches of sludge management. Environ Sci Pollut Res 22:7361–7374

    CAS  Article  Google Scholar 

  • New Zealand Water and Wastes Association (2003) Guidelines for the safe application of biosolids to land in New Zealand. Wellington, New Zealand

    Google Scholar 

  • Northcott GL (2014) Disappearance and transformation of the antimicrobial chemical triclosan in 2 New Zealand soils. In: New Zealand Society of Soil Science Conference “Soil Science for Future Generations”, The University of Waikato, Hamilton, 1-4 December 2014

  • Piotrowska-Seget Z, Cycoń M, Kozdrój J (2005) Metal-tolerant bacteria occurring in heavily polluted soil and mine spoil. Appl Soil Ecol 28:237–246

    Article  Google Scholar 

  • Rayment GE, Lyons DJ (2011) Soil chemical methods: Australasia Australian soil and land survey handbooks, 3. CSIRO Publishing, Collingwood

    Google Scholar 

  • Reiss R, Lewis G, Griffin J (2009) An ecological risk assessment for triclosan in the terrestrial environment. Environ Toxicol Chem 28:1546–1556

    CAS  Article  Google Scholar 

  • Rutgers M, Van’t Verlaat IM, Wind B, Posthuma L, Breure AM (1998) Rapid method for assessing pollution-induced community tolerance in contaminated soil. Environ Toxicol Chem 17:2210–2213

    Article  Google Scholar 

  • Schmitt H (2005) The effects of veterinary antibiotics on soil microbial communities. Institute for Risk Assessment Sciences, Utrecht University, ISBN 90-8559-056-6

  • Seaman PF, Ochs D, Day MJ (2007) Comment on: Triclosan resistance in methicillin-resistant Staphylococcus aureus expressed as small colony variants: a novel mode of evasion of susceptibility to antiseptics. J Antimicrob Chemoth 60:175–176

    CAS  Article  Google Scholar 

  • Shareef A, Egerer S, Kookana R (2009) Effect of triclosan and triclocarban biocides on biodegradation of estrogens in soils. Chemosphere 77:1381–1386

    CAS  Article  Google Scholar 

  • Sparling GP, Lilburne L, Vojvodic-Vukovic M (2008) Provisional targets for soil quality indicators in New Zealand. https://sindi.landcareresearch.co.nz/. Landcare Research Science Series no. 34. Manaaki Whenua Press, Lincoln, New Zealand

  • Speir T, Northcott GL (2006) Organic residues in sewage biosolids: summary of the New Zealand CDRP Project results. Paper presented at the Australian Water Association. Biosolids Specialty Conference, Melbourne, Victoria, Australia, 2-8 June 2006

  • Speir TW, van Schaik AP, Hunter LC, Ryburn JL, Percival HJ (2007) Attempts to derive EC50 values for heavy metals from land-applied Cu-, Ni-, and Zn-spiked sewage sludge. Soil Biol Biochem 39:539–549

    CAS  Article  Google Scholar 

  • Stasinakis AS, Petalas AV, Mamais D, Thomaidis NS, Gatidou G, Lekkas TD (2007) Investigation of triclosan fate and toxicity in continuous-flow activated sludge systems. Chemosphere 68:375–381

    CAS  Article  Google Scholar 

  • Stevens KJ, Kim SY, Adhikari S, Vadapalli V, Venables BJ (2009) Effects of triclosan on seed germination and seedling development of three wetland plants: Sesbania herbacea, Eclipta prostrata, and Bidens frondosa. Environ Toxicol Chem 28:2598–2609

    CAS  Article  Google Scholar 

  • Svenningsen H, Henriksen T, Priemé A, Johnsen AR (2011) Triclosan affects the microbial community in simulated sewage-drain-field soil and slows down xenobiotic degradation. Environ Pollut 159:1599–1605

    CAS  Article  Google Scholar 

  • Thompson A, Griffin P, Stuetz R, Cartmell E (2005) The fate and removal of triclosan during wastewater treatment. Water Environ Res 77:63–67

    CAS  Article  Google Scholar 

  • Tkachenko O, Shepard J, Aris VM, Joy A, Bello A, Londono I, Marku J, Soteropoulos P, Peteroy-Kelly MA (2007) A triclosan-ciprofloxacin cross-resistant mutant strain of Staphylococcus aureus displays an alteration in the expression of several cell membrane structural and functional genes. Res Microbiol 158:651–658

    CAS  Article  Google Scholar 

  • Vance ED, Brookes PC, Jenkinson DS (1987) An extraction method for measuring soil microbial biomass C. Soil Biol Biochem 19:703–707

    CAS  Article  Google Scholar 

  • Veldhoen N, Skirrow RC, Osachoff H, Wigmore H, Clapson DJ, Gunderson MP, Van Aggelen G, Helbing CC (2006) The bactericidal agent triclosan modulates thyroid hormone-associated gene expression and disrupts postembryonic anuran development. Aquat Toxicol 80:217–227

    CAS  Article  Google Scholar 

  • Villalaín J, Mateo CR, Aranda FJ, Shapiro S, Micol V (2001) Membranotropic effects of the antibacterial agent triclosan. Arch Biochem Biophys 390:128–136

    Article  Google Scholar 

  • Waller NJ, Kookana RS (2009) Effect of triclosan on microbial activity in Australian soils. Environ Toxicol Chem 28:65–70

    CAS  Article  Google Scholar 

  • Wardle DA (1992) A comparative assessment of factors which influence microbial biomass carbon and nitrogen levels in soil. Biol Rev 67:321–358

    Article  Google Scholar 

  • Webber MA, Coldham NG, Woodward MJ, Piddock LJV (2008a) Proteomic analysis of triclosan resistance in Salmonella enterica serovar Typhimurium. J Antimicrob Chemoth 62:92–97

    CAS  Article  Google Scholar 

  • Webber MA, Randall LP, Cooles S, Woodward MJ, Piddock LJV (2008b) Triclosan resistance in Salmonella enterica serovar Typhimurium. J Antimicrob Chemoth 62:83–91

    CAS  Article  Google Scholar 

  • Xu J, Wu L, Chang AC (2009) Degradation and adsorption of selected pharmaceuticals and personal care products (PPCPs) in agricultural soils. Chemosphere 77:1299–1305

    CAS  Article  Google Scholar 

  • Xue J, Kimberley MO, Ross C, Gielen G, Tremblay LA, Champeau O, Horswell J, Wang H (2015) Ecological impacts of long-term application of biosolids to a radiata pine plantation. Sci Total Environ 530–531:233–240

    Article  Google Scholar 

  • Ying G-G, Yu X-Y, Kookana RS (2007) Biological degradation of triclocarban and triclosan in a soil under aerobic and anaerobic conditions and comparison with environmental fate modelling. Environ Pollut 150:300–305

    CAS  Article  Google Scholar 

  • Zuckerbraun HL, Babich H, May R, Sinensky MC (1998) Triclosan: cytotoxicity, mode of action, and induction of apoptosis in human gingival cells in vitro. Eur J Oral Sci 106:628–636

    CAS  Article  Google Scholar 

Download references

Acknowledgments

We thank the New Zealand Ministry of Business, Innovation and Employment (MBIE) for funding, Alexandra McGill, Jacqui van der Waals, Marie Dennis and Ruth Falshaw for their valued contributions and Rod Ball and Mark Kimberly for providing statistical support to this study.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Gerty J. H. P. Gielen.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Responsible editor: Jizheng He

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Gielen, G.J.H.P., van Schaik, A.P., Northcott, G. et al. Effect of copper and zinc on microbial tolerance to triclosan in two soil types. J Soils Sediments 16, 1944–1959 (2016). https://doi.org/10.1007/s11368-016-1389-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11368-016-1389-2

Keywords

  • Copper
  • Microbial tolerance
  • Mixtures
  • Soil
  • Triclosan
  • Zinc