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Biosensor-based comparison of the ecotoxicological contamination of the wastewaters of Southern Russia and Southern Germany

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Abstract

To assess the ecotoxicological and sanitary situation in two European metropolis, Rostov-on-Don (Southern Russia) and Munich (Southern Germany), wastewaters of the two cities were examined with a panel of bacterial lux-biosensors: Vibrio aquamarinus VKPM B-11245, Escherichia coli MG1655 (pXen7), E. coli MG1655 (pRecA-lux), E. coli MG1655 (pSoxS-lux), E. coli MG1655 (pKatG-lux), E. coli MG1655 (pIbpA-lux), E. coli MG1655 (GrpE-lux), E. coli MG1655 (pFabA-lux). The presence of different genotoxic compounds and substances with the oxidative and membrane-damaging effects was revealed in contaminated wastewater with the applied panel of the lux-biosensors. The integral toxicity was approximately the same in both cities but demonstrated opposite trends. The presence of genotoxicants and peroxides was higher in the majority of the Munich wastewater samples. There were also differences in the presence of individual toxicants. The presence of the genotoxic compounds might also promote development and dissemination of several antibiotic resistance traits found in microorganisms, a feature more pronounced in Rostov-on-Don wastewaters. By means of polymerase chain reaction assay, antibiotic resistance genes to such antibiotics as ermB, vim and vanB were revealed in two Munich samples. Antibiotic resistance genes were present at all Rostov samples, and genes ndm, vanA, vanB and ermB were found. Taken together, the proposed analytical approach with the application of the constructed panel of biosensors can be applied for monitoring of the ecotoxicological contamination in the wastewaters of large cities.

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References

  • Amos GCA, Zhang L, Hawkey PM, Gaze WH, Wellington EM (2014) Functional metagenomic analysis reveals rivers are a reservoir for diverse antibiotic resistance genes. Vet Microbiol 171:441–447

    Article  CAS  Google Scholar 

  • Belkin S (2003) Microbial whole-cell sensing systems of environmental pollutants. Curr Opin Microbiol 6:206–212

    Article  CAS  Google Scholar 

  • Bhalla B, Saini MS, Jha MK (2013) Effect of age and seasonal variations on leachate characteristics of municipal solid waste landfill. Int J Res Eng Technol (IJRET) 2:223–232

    Google Scholar 

  • Biran A, Yagur-Kroll S, Pedahzur R, Buchinger S, Reifferscheid G, Ben-Yoav H, Shacham-Diamand Y, Belkin S (2010) Bacterial genotoxicity bioreporters. Microb Biotechnol 3:412–427

    Article  CAS  Google Scholar 

  • Carney Almroth B, Albertsson E, Sturve J, Förlin L (2008) Oxidative stress, evident in antioxidant defences and damage products, in rainbow trout caged outside a sewage treatment plant. Ecotoxicol Environ Saf 70(3):370–378. doi:10.1016/j.ecoenv.2008.01.023

    Article  CAS  Google Scholar 

  • Choi S, Gu M (1999) A whole cell bioluminescent biosensor for the detection of membrane-damaging toxicity. Biotechnol Bioprocess Eng 4:59–62

    Article  CAS  Google Scholar 

  • Daniel R, Almog R, Ron A, Belkin S, Diamand YS (2008) Modeling and measurement of a whole-cell bioluminescent biosensor based on a single photon avalanche diode. Biosens Bioelectron 24:888–893

    Article  Google Scholar 

  • Deriabin DG, Aleshina ES (2008) Biotests for mineral waters with natural and recombinant luminescent microorganisms. Prikl Biokhim Mikrobiol 44:417–421

    CAS  Google Scholar 

  • Ding S, Wu J, Zhang M, Lu H, Mahmood Q, Zheng P (2015) Acute toxicity assessment of ANAMMOX substrates and antibiotics by luminescent bacteria test. Chemosphere 140:174–183. doi:10.1016/j.chemosphere

    Article  CAS  Google Scholar 

  • Elad T, Belkin S (2013) Broad spectrum detection and “barcoding” of water pollutants by a genome-wide bacterial sensor array. Water Res 47:3782–3790. doi:10.1016/j.watres.2013.04.011

    Article  CAS  Google Scholar 

  • Elad T, Almog R, Yagur-Kroll S, Levkov K, Melamed S, Shacham-Diamand Y, Belkin S (2011) Online monitoring of water toxicity by use of bioluminescent reporter bacterial biochips. Environ Sci Technol 45:8536–8544

    Article  CAS  Google Scholar 

  • Eltzov E, Yehuda A, Marks RS (2015) Creation of a new portable biosensor for water toxicity determination. Sens Actuators B Chem 221(31):1044–1054

    Article  CAS  Google Scholar 

  • Figueras M, Borrego JJ (2010) New perspectives in monitoring drinking water microbial quality. Int J Environ Res Public Health 712:4179–4202

    Article  Google Scholar 

  • Gaze WH, Zhang L, Abdouslam NA, Hawkey PM, Calvo-Bado L, Royle J, Brown H, Davis S, Kay P, Boxall ABA, Wellington EMH (2011) Impacts of anthropogenic activity on the ecology of class 1 integrons and integron-associated genes in the environment. ISME J 5:1253–1261. doi:10.1038/ismej.2011.15

    Article  CAS  Google Scholar 

  • Gondek K, Baran A, Kopeć M (2014) The effect of low-temperature transformation of mixtures of sewage sludge and plant materials on content, leachability and toxicity of heavy metals. Chemosphere 117:33–39. doi:10.1016/j.chemosphere.2014.05.032

    Article  CAS  Google Scholar 

  • Guillaume G, Verbrugge D, Chasseru-Libotte M-L, Moens W, Collard J (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 32:77–85

    CAS  Google Scholar 

  • Hakkila K, Green T, Leskinen P, Ivask A, Marks R, Virta MJ (2004) Detection of bioavailable heavy metals in EILATox-Oregon samples using whole-cell luminescent bacterial sensors in suspension or immobilized onto fibre-optic tips. Appl Toxicol 24:333–342

    Article  CAS  Google Scholar 

  • Halling-Sørensen B, Nors Nielsen S, Lanzky PF, Ingerslev F, Holten Lützhøft HC, Jørgensen SE (1998) Occurrence, fate and effects of pharmaceutical substances in the environment—a review. Chemosphere 36(2):357–393

    Article  Google Scholar 

  • Harwood V, Brownell M, Perusek W, Whitlock JE (2001) Vancomycin-resistant Enterococcus spp. isolated from wastewater and chicken faeces in the United States. Appl Environ Microbiol 67:4930–4933. doi:10.1128/AEM.67.10.4930-4933.2001

    Article  CAS  Google Scholar 

  • Ivask A, Rolova T, Kahru A (2009) A suite of recombinant luminescent bacterial strains for the quantification of bioavailable heavy metals and toxicity testing. BMC Biotechnol 9:41. doi:10.1186/1472-6750-9-41

    Article  Google Scholar 

  • Iversen A, Kühn I, Franklin A, Möllby R (2002) High prevalence of vancomycin-resistant enterococci in Swedish sewage. Appl Environ Microbiol 68:2838–2842

    Article  CAS  Google Scholar 

  • Ji JY, Xing YJ, Ma ZT, Cai J, Zheng P, Lu HF (2013) Toxicity assessment of anaerobic digestion intermediates and antibiotics in pharmaceutical wastewater by luminescent bacterium. J Hazard Mater 246–247:319–323. doi:10.1016/j.jhazmat.2012.12.025

    Article  Google Scholar 

  • Kokkali V, Delft W (2014) Overview of commercially available bioassays for assessing chemical toxicity in aqueous samples. Trends Analyt Chem 61:133–155

    Article  CAS  Google Scholar 

  • Korzeniewska E, Harnisz M (2013) Extended-spectrum beta-lactamase (ESBL)-positive Enterobacteriaceae in municipal sewage and their emission to the environment. J Environ Manag 128:904–911. doi:10.1016/j.jenvman.2013.06.051

    Article  CAS  Google Scholar 

  • Kümmerer K, Henninger A (2004) Promoting resistance by the emission of antibiotics from hospitals and households into effluents. Clin Microbiol Infect 9:1203–1214. doi:10.1111/j.1469-0691.2003.00739.x

    Article  Google Scholar 

  • Layton AC, Muccini M, Ghosh MM, Sayler GS (1998) Construction of a bioluminescent reporter strain to detect polychlorinated biphenyls. Appl Environ Microbiol 64(12):5023–5026

    CAS  Google Scholar 

  • Lee HJ, Gu MB (2003) Construction of a sodA:luxCDABE fusion Escherichia coli: comparison with a katG fusion strain through their responses to oxidative stresses. Appl Microbiol Biotechnol 60:577–580

    Article  CAS  Google Scholar 

  • Livingstone DR (2001) Contaminant-stimulated reactive oxygen species production and oxidative damage in aquatic organisms. Mar Pollut Bull 42:656–666

    Article  CAS  Google Scholar 

  • Lushchak VI (2011) Adaptive response to oxidative stress: bacteria, fungi, plants and animals. Comp Biochem Physiol C Toxicol Pharmacol 153:175–190

    Article  Google Scholar 

  • Lyngberg OK, Stemke DJ, Schottel JL, Flickinger MC (1999) A single-use luciferase-based mercury biosensor using Escherichia coli HB101 immobilized in a latex copolymer film. J Ind Microbiol Biotechnol 23:668–676

    Article  CAS  Google Scholar 

  • Ma XY, Wang XC, Ngo HH, Guo W, Wu MN, Wang N (2014) Bioassay based luminescent bacteria: interferences, improvements, and applications. Sci Total Environ 468–469:1–11. doi:10.1016/j.scitotenv.2013.08.028

    Article  Google Scholar 

  • Maniatis T, Fritsch EF, Sambrook J (1982) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory, New York

    Google Scholar 

  • Methods of Rapid Determination of Integrated Chemical Toxicity of Drinking Water, Surface Water, Groundwater, Wastewater and Treated Wastewater Using Bacterial Test “Ecolum”: Guidelines (Metodika ekspressnogo opredeleniya integral’noy khimicheskoy toksichnosti pit’evykh, poverkhnostnykh, gruntovykh, stochnykh i ochishchennykh stochnykh vod s pomoshch’yu bakterial’nogo testa “Ekolyum”: Metodicheskie rekomendatsii). (2007) Moscow

  • Munir M, Wong K, Xagoraraki I (2011) Release of antibiotic resistant bacteria and genes in the effluent and biosolids of five wastewater utilities in Michigan. Water Res 45:681–693. doi:10.1016/j.watres.2010.08.033

    Article  CAS  Google Scholar 

  • Palchetti I, Mascini M (2008) Nucleic acid biosensors for environmental pollution monitoring. Analyst 133:846–854. doi:10.1039/b802920m

    Article  CAS  Google Scholar 

  • Palma P, Alvarenga P, Palma V, Matos C, Fernandes RM, Soares A, Barbosa IR (2010) Evaluation of surface water quality using an ecotoxicological approach: a case study of the Alqueva Reservoir (Portugal). Environ Sci Pollut Res Int 17:703–716. doi:10.1007/s11356-009-0143-3

    Article  CAS  Google Scholar 

  • Park CJ, Ahn HM, Cho SC, Kim TH, Oh JM, Ahn HK, Chun SH, Gye MC (2014) Developmental toxicity of treated municipal wastewater effluent on Bombina orientalis (Amphibia: Anura) embryos. Environ Toxicol Chem 33:954–961. doi:10.1002/etc.2519

    Article  CAS  Google Scholar 

  • Paxéus N (1996) Paper Organic pollutants in the effluents of large wastewater treatment plants in Sweden. Water Res 30(5):1115–1122

    Article  Google Scholar 

  • Poma HR, Gutiérrez D, Garcé B, Gonzo EE, Rajal VB (2012) Towards a rational strategy for monitoring of microbiological quality of ambient waters. Sci Total Environ 433:98–109

    Article  CAS  Google Scholar 

  • Prasse C, Stalter D, Schulte-Oehlmann U, Oehlmann J, Ternes TA (2015) Spoilt for choice: a critical review on the chemical and biological assessment of current wastewater treatment technologies. Water Res 87:237–270. doi:10.1016/j.watres.2015.09.023

    Article  CAS  Google Scholar 

  • Ptitsyn LR, Horneck G, Komova O, Kozubec S, Krasavin EA, Bonev M, Rettberg PA (1997) biosensor for environmental genotoxin screening based on an SOS lux assay in recombinant Escherichia coli cells. Appl Environ Microbiol 63:4377–4384

    CAS  Google Scholar 

  • Ren S (2004) Assessing wastewater toxicity to activated sludge: recent research and developments. Environ Int 30(8):1151–1164

    Article  CAS  Google Scholar 

  • Rodrigues ES, Umbuzeiro Gde A (2011) Integrating toxicity testing in the wastewater management of chemical storage terminals—a proposal based on a ten-year study. J Hazard Mater 186(2–3):1909–1915. doi:10.1016/j.jhazmat.2010.12.083

    Article  CAS  Google Scholar 

  • Sahlström L, Rehbinder V, Albihn A, Aspan A, Bengtsson B (2009) Vancomycin resistant enterococci (VRE) in Swedish sewage sludge. Acta Vet Scand 51:24. doi:10.1186/1751-0147-51-24

    Article  Google Scholar 

  • Sazykin IS, Sazykina MA, Kudeevskaya EM, Sazykina MI (2014) The strain Vibrio aquamarinus, a method for determining the toxicity of samples with it and test culture to determine the toxicity of samples. Russian Federation Patent number 2534819. IPC C12N1 / 20 C12R1 / 63, C12Q1 / 02. Bulletin 34

  • Schwartz T, Kohnen T, 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 43:325–335. doi:10.1111/j.1574-6941.2003.tb01073.x

    Article  CAS  Google Scholar 

  • Sorensen SJ, Burmolle M, Hansen LH (2006) Making bio-sense of toxicity: new developments in whole-cell biosensors. Curr Opin Biotechnol 17:11–16

    Article  CAS  Google Scholar 

  • Stadler LB, Ernstoff AS, Aga DS, Love NG (2012) Micropollutant fate in wastewater treatment: redefining “removal”. Environ Sci Technol 46(19):10485–10486

    Article  CAS  Google Scholar 

  • Sturve J, Almroth BC, Förlin L (2008) Oxidative stress in rainbow trout (Oncorhynchus mykiss) exposed to sewage treatment plant effluent. Ecotoxicol Environ Saf 70(3):446–452. doi:10.1016/j.ecoenv.2007.12.004

    Article  CAS  Google Scholar 

  • Szczepanowski R, Linke B, Krahn I, Gartemann KH, Gützkow T, Eichler W, Pühler A, Schlüter A (2009) Detection of 140 clinically relevant antibiotic-resistance genes in the plasmid metagenome of wastewater treatment plant bacteria showing reduced susceptibility to selected antibiotics. Microbiology 155:2306–2319

    Article  CAS  Google Scholar 

  • Tang JYM, McCarty S, Glenn E, Neale PA, Warne MSJ, Escher BI (2013) Mixture effects of organic micropollutants present in water: towards the development of effect-based water quality trigger values for baseline toxicity. Water Res 47(10):3300–3314

    Article  CAS  Google Scholar 

  • Valavanidis A, Vlahogianni T, Dassenakis M, Scoullos M (2006) Molecular biomarkers of oxidative stress in aquatic organisms in relation to toxic environmental pollutants. Ecotoxicol Environ Saf 64:178–189

    Article  CAS  Google Scholar 

  • Van Dyk TK, Majarian WR, Konstantinov KB, Young RM, Dhurjati PS, Larossa RA (1994) Rapid and sensitive pollutant detection by induction of heat shock gene-bioluminescence gene fusions. Appl Environ Microbiol 60:1414–1420

    Google Scholar 

  • Van Dyk TK, Reed TT, Vollmer AC, LaRossa RA (1995) Synergistic induction of the heat shock response in Escherichia coli by simultaneous treatment with chemical inducers. J Bacteriol 177:6001–6004

    Google Scholar 

  • Vollmer AC, Belkin S, Smulski DR, VanDyk TK, LaRossa RA (1997) Detection of DNA damage by use of Escherichia coli carrying recA’:lux, uvrA’:lux, or alkA’:lux reporter plasmids. Appl Environ Microbiol 63:2566–2571

    CAS  Google Scholar 

  • Woutersen M, Belkin S, Brouwer B, van Wezel AP, Heringa MB (2011) Are luminescent bacteria suitable for online detection and monitoring of toxic compounds in drinking water and its sources? Anal Bioanal Chem 400:915–929. doi:10.1007/s00216-010-4372-6

    Article  CAS  Google Scholar 

  • Zavilgelsky GB, Kotova VYu, Manukhov IV (2007) Action of 1,1–dimethylhydrazine on bacterial cells is determined by hydrogen peroxide. Mutat Res 634:172–176

    Article  CAS  Google Scholar 

  • Zhang D, Ding A, Cui S, Hu C, Thornton SF, Dou J, Sun Y, Huang WE (2013) Whole cell bioreporter application for rapid detection and evaluation of crude oil spill in sea water caused by Dalian oil tank explosion. Water Res 47:1191–1200

    Article  CAS  Google Scholar 

  • Zhao J, Chen X, Zhao J, Lin F, Bao Z, He Y, Wang L, Shi Z (2015) Toxicity in different molecular-weight fractions of sludge treating synthetic wastewater containing 4-chlorophenol. Int Biodeterior Biodegrad 104:251–257

    Article  CAS  Google Scholar 

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Acknowledgments

This study was funded by the Southern Federal University (Grant No. 213.01-07-2014/12 PChVG). This research was performed with the use of the equipment of Collective Using Center of the Southern Federal University “Biotechnology, Biomedicine and Environmental Monitoring.”

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Correspondence to M. A. Sazykina.

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Sazykin, I.S., Sazykina, M.A., Khmelevtsova, L.E. et al. Biosensor-based comparison of the ecotoxicological contamination of the wastewaters of Southern Russia and Southern Germany. Int. J. Environ. Sci. Technol. 13, 945–954 (2016). https://doi.org/10.1007/s13762-016-0936-0

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