Hot spots of antibiotic tolerant and resistant bacterial subpopulations in natural freshwater biofilm communities due to inevitable urban drainage system overflows☆
Graphical abstract
Introduction
The majority of urban surface waters are continuously impacted by wastewater treatment plant effluents and intermittently by combined sewer overflow discharges – a composite of sewage and storm water – due to capacity limitations of urban drainage systems. In particular, urban wastewater contains not only a large repertoire of antibiotic residues, but also antibiotic resistant bacteria and antibiotic resistance genes. The identification of antibiotic resistance genes (ARG) in wastewater treatment plant effluents had been focused (Czekalski et al., 2014; Novo et al., 2013; Rizzo et al., 2013). Investigations, which assess the impact of ARG to surface water biofilms, followed (Aubertheau et al., 2017; Guo et al., 2018; Lehmann et al., 2016; Marti et al., 2013; Proia et al., 2016). Consequently, biofilms may represent an ideal setting for the promotion and spreading of antibiotic resistance. However, studies identifying tolerant and resistant bacterial subpopulations in natural freshwater biofilm (NFB) communities due to intermittent and untreated sewage are rare. Marathe et al. (2017) investigated the impact of uncontrolled discharge of inadequately treated and untreated urban effluents; Subirats et al. (2017) even measured a more pronounced effect of raw wastewater than treated sewage.
Identifying environments where ARGs are enriched is important for the design of mitigation strategies to control antibiotic resistance (Berendonk et al., 2015). The identification of hot spots is challenging. Currently, there are two major ways of evaluation present, either the response-assessment due to toxicity tests or the determination of specific genes. The evaluation of effects due to antibiotic mixtures is another challenge: pharmaceutical cocktails shape the microbial community (Menz et al., 2017) and the three-dimensional matrix of the biofilm (Bruchmann et al., 2013). This short communication focuses the identification of hot spots of tolerant and resistant bacterial subpopulations in NFB-communities due to intermittent urban drainage overflows. The inhibition of activity due to antibiotic exposure – individually dosed and in mixture – is measured as oxygen uptake rate. This approach is appropriate to characterize effects (Friedrich et al., 2015, 2016, Kaeseberg et al., 2015, Lee et al., 2006, Spanjers and Vanrolleghem, 1995). To the best of the authors' knowledge, this is the first look at NFB-communities for a stormwater pollution aspect. The following investigations were conducted to (i) quantify the antibiotic concentrations in sewage and adjacent surface water; (ii) growth of NFB-communities attached to self-designed biofilm attachment constructions, which were placed upstream and downstream of a rainwater overflow structure respectively upstream and downstream of a combined sewer overflow structure; (iii) quantify activity inhibition of those NFB-communities due to individually dosed antibiotics and antibiotic mixtures; and (iv) identify hot spots of increased antibiotic tolerance and resistance.
Although our investigations are in an initial phase in terms of the announcement of necessary policy and management options, we highlight these findings due to ubiquitous urban drainage overflow constructions, which are state of the art in the urban drainage design.
Section snippets
Area under investigation
A brook in Germany with a mean flow (MQ) of 0.34 m3 s−1 was selected for the present study. The effluents of 6 wastewater treatment plants (WWTP), 11,500 population equivalents (PE), 3650 PE, 500 PE, 400 PE, 150 PE and 130 PE, discharge into the brook before it enters Dresden (540,000 inhabitants). The WWTP with the highest capacity treats the wastewater of a rehabilitation clinic (more than 1000 beds and 1800 employees). 8 combined sewer overflows (CSO) and 26 rain sewer overflows (RSO) of the
Antibiotics in sewage
Ciprofloxacin. The sampled concentration in sewage was 985.1 ± 547.6 ng L−1 (mean value and standard deviation), see Table 2. The median value was 814.5 ng L−1, which was 82.7% of mean concentration. The maximum detected concentration in 24-h composite samples was 2151.0 ng L−1.
Clarithromycin. The analyzed concentration in 24-h composite sewage samples was 575.5 ± 544.3 ng L−1 (mean value and standard deviation), see Table 2. The median value was 330.5 ng L−1, which was 57.4% of mean
Conclusion
Surface waters and NFB-communities are intermittently exposed to urban drainage overflow plumes and consequently antibiotic stress. Antibiotic tolerant subpopulations have survival benefits, and tolerance is the preliminary stage to resistance (Levin-Reisman et al., 2017). The increased residual activity at DSCSO,10 and even DSCSO,100 was a consequence of a severe impact of urban drainage overflows. CSO-constructions are state of the art in the urban drainage design. Consequently, adjacent
Acknowledgements
This paper is part of the research project “ANTI-Resist” (Untersuchung zu Einträgen von Antibiotika und der Bildung von Antibiotikaresistenzen im urbanen Abwasser sowie Entwicklung geeigneter Strategien, Monitoring-und Frühwarnsysteme am Beispiel Dresden), funded by the German Federal Ministry of Education and Research (Grant reference 02WRS1272A) within the Framework Concept “Risk Management of Emerging Compounds and Pathogens in the Water Cycle” and managed by the Project Management Agency
References (46)
- et al.
Occurrence and spatial distribution of 158 pharmaceuticals, drugs of abuse and related metabolites in offshore seawater
Sci. Total Environ.
(2016) - et al.
Impact of wastewater treatment plant discharge on the contamination of river biofilms by pharmaceuticals and antibiotic resistance
Sci. Total Environ.
(2017) - et al.
Highway runoff and potential for removal of heavy metals in an infiltration pond in Portugal
Sci. Total Environ.
(1999) - et al.
Validation and uncertainty estimation of a multiresidue method for pharmaceuticals in surface and treated waters by liquid chromatography-tandem mass spectrometry
J. Chromatogr. A
(2013) - et al.
Evaluation of pharmaceuticals in surface water: reliability of PECs compared to MECs
Environ. Int.
(2014) - et al.
Determination of antibiotic compounds in water by on-line SPE-LC/MSD
Chemosphere
(2007) - et al.
Occurrence and risk assessment of antibiotics in river water in Hong Kong
Ecotoxicol. Environ. Saf.
(2016) - et al.
Physiological adaptation of growth kinetics in activated sludge
Water Res.
(2015) - et al.
Occurrence of pharmaceuticals in a municipal wastewater treatment plant: mass balance and removal processes
Chemosphere
(2012) - et al.
Seasonal changes in antibiotics, antidepressants/psychiatric drugs, antihistamines and lipid regulators in a wastewater treatment plant
Chemosphere
(2014)
Biofilms as a sink for antibiotic resistance genes (ARGs) in the Yangtze Estuary
Water Res.
Total resistance of native bacteria as an indicator of changes in the water environment
Environ. Pollut.
Abiotic, biotic and photolytic degradation affinity of 14 antibiotics and one metabolite – batch experiments and a model framework
Environ. Pollut.
Sewer sediment-bound antibiotics as a potential environmental risk: adsorption and desorption affinity of 14 antibiotics and one metabolite
Environ. Pollut.
Standardized tests fail to assess the effects of antibiotics on environmental bacteria
Water Res.
Trace levels of sewage effluent are sufficient to increase class 1 integron prevalence in freshwater biofilms without changing the core community
Water Res.
Untreated urban waste contaminates Indian river sediments with resistance genes to last resort antibiotics
Water Res.
Antimicrobial activity of pharmaceutical cocktails in sewage treatment plant effluent - an experimental and predictive approach to mixture risk assessment
Environ. Pollut.
Antibiotic resistance, antimicrobial residues and bacterial community composition in urban wastewater
Water Res.
Presence of pharmaceuticals in the Lis river (Portugal): sources, fate and seasonal variation
Sci. Total Environ.
Occurrence and persistence of antibiotic resistance genes in river biofilms after wastewater inputs in small rivers
Environ. Pollut.
Urban wastewater treatment plants as hotspots for antibiotic resistant bacteria and genes spread into the environment: a review
Sci. Total Environ.
Simultaneous determination of most prescribed antibiotics in multiple urban wastewater by SPE-LC–MS/MS
J. Chromatogr. B
Cited by (22)
Transformation trend of nitrogen and phosphorus in the sediment of the sewage pipeline and their distribution along the pipeline
2023, Science of the Total EnvironmentNon-corresponding contaminants in marine surface sediments as a factor of ARGs spread in the Sea of Azov
2022, Marine Pollution BulletinCharacteristics of overflow pollution from combined sewer sediment: Formation, contribution and regulation
2022, ChemosphereCitation Excerpt :As a result, creatures in the water are poisoned (Schertzinger et al., 2018). Therefore, sewer sediments have a high contribution to the overflow pollution of channels, and they should be treated as one of the main sources of CSOs pollutants (Kaeseberg et al., 2018; Meng et al., 2020; Xu et al., 2018). During overflow, the sediment is resuspended by the water flow and discharged into the water body (David et al., 2013; Liu et al., 2021).
Migration and transformation of nitrogen in sediment–water system within storm sewers
2021, Journal of Environmental Management
- ☆
This paper has been recommended for acceptance by Klaus Kummerer.