CoChat
Sign Up
Cited by 70Pharmaceutical and Antibiotic Environmental ImpactsWastewater Treatment and ReuseAntibiotic Use and Resistance

The DOI matches its Crossref record; 1 of the 1 references it cites were found in a registry or an index.

Occurrence and distribution of antibiotics and corresponding antibiotic resistance genes in different soil types irrigated with treated wastewater

Seyoum, Mitiku Mihiret, Obayomi, Olabiyi, Bernstein, Nirit, Williams, Clinton F., Gillor, Osnat·2021·Science of The Total Environment
DOI 10.1016/j.scitotenv.2021.146835
Open this paper in CoChat — free account

Abstract

Diminishing freshwater (FW) supplies necessitate the reuse of treated wastewater (TWW) for various purposes, like irrigation of agricultural lands. However, there is a growing concern that irrigation with TWW may transfer antibiotic resistance genes (ARGs) to the soil and crops. We hypothesized that TWW irrigation would increase the prevalence of antibiotic residues together with the corresponding ARGs in the irrigated soil. We further predicted that soil texture, especially pH, clay content, and organic matter variabilities, would change the antibiotic residues concentrations and thus ARGs dissemination. To test our predictions, three soils types (loamy-sand, loam, and clay) were irrigated with two water types (FW and TWW), over two consecutive seasons. We monitored physico-chemical parameters, the abundance of seven antibiotic residues, and their corresponding ARGs together with class 1 integron (intI1) in 54 water and soil samples collected at the end of the field experiments. The results revealed increase in antibiotics concentrations and ARGs relative abundance in TWW than FW. Yet, in the soil ARGs relative abundances were independent of the irrigation water quality, but dependent on the soil type, especially the clay content. Further, there were no clear associations between the targeted antibiotics or the presence of heavy metals and ARGs' relative abundance in the water or soil samples. Therefore, our results question the link between the discharge of antibiotics and…

Overview

Integrity signals

Registry

Crossref · 10.1016/j.scitotenv.2021.146835

Cites

1 of 1 references verified0 citation errors · 0 not checkable

Statistics

Recomputing p-values needs the paper’s full text.

Verification

Claims the paper makes

This paper’s full text isn’t openly available, so its claims and self-check weren’t run. The registry and citation checks still apply.

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Citations

Cites

Show all 1 references

Research works printed but not linked: 58

  1. Adegoke, 2018, Epidemiological evidence and health risks associated with agricultural reuse of partially treated and untreated wastewater: a review, Front. Public Health, 6, 337, 10.3389/fpubh.2018.00337 · DOI
  2. Allaire, 2006, Sorption kinetics of chlortetracyline and tylosin on sandy loam and heavy clay soils, J. Environ. Qual., 35, 969, 10.2134/jeq2005.0355 · DOI
  3. Américo-Pinheiro, 2021, Monitoring microbial contamination of antibiotic resistant Escherichia coli isolated from the surface water of urban park in southeastern Brazil, Environmental Nanotechnology, Monitoring & Management, 15, 100438, 10.1016/j.enmm.2021.100438 · DOI
  4. Becerra-Castro, 2015, Wastewater reuse in irrigation: a microbiological perspective on implications in soil fertility and human and environmental health, Environ. Int., 75, 117, 10.1016/j.envint.2014.11.001 · DOI
  5. Bengtsson-Palme, 2016, Elucidating selection processes for antibiotic resistance in sewage treatment plants using metagenomics, Sci. Total Environ., 572, 697, 10.1016/j.scitotenv.2016.06.228 · DOI
  6. Bilal, 2020, Perspectives on the Feasibility of Using Enzymes for Pharmaceutical Removal in Wastewater, 10.1007/698_2020_661 · DOI
  7. Bilal, M., Barceló, D., & Iqbal, H. M. N. (2020b). Persistence, ecological risks, and oxidoreductases-assisted biocatalytic removal of triclosan from the aquatic environment. In Science of the Total Environment (Vol. 735, p. 139194). Elsevier B.V. doi:https://doi.org/10.1016/j.scitotenv.2020.139194. · DOI
  8. Cacace, 2019, Antibiotic resistance genes in treated wastewater and in the receiving water bodies: a pan-European survey of urban settings, Water Res., 162, 320, 10.1016/j.watres.2019.06.039 · DOI
  9. Carey, 2009, Contribution of wastewater treatment plant effluents to nutrient dynamics in aquatic systems: a review, Environ. Manag., 44, 205, 10.1007/s00267-009-9309-5 · DOI
  10. Cerqueira, 2020, Effects of prescription antibiotics on soil- and root-associated microbiomes and resistomes in an agricultural context, J. Hazard. Mater., 400, 123208, 10.1016/j.jhazmat.2020.123208 · DOI
  11. Christou, 2017, The potential implications of reclaimed wastewater reuse for irrigation on the agricultural environment: the knowns and unknowns of the fate of antibiotics and antibiotic resistant bacteria and resistance genes – a review, Water Res., 123, 448, 10.1016/j.watres.2017.07.004 · DOI · Paper page
  12. Conde-Cid, 2019, Competitive adsorption of tetracycline, oxytetracycline and chlortetracycline on soils with different pH value and organic matter content, Environ. Res., 178, 108669, 10.1016/j.envres.2019.108669 · DOI
  13. Cycoń, 2019, Antibiotics in the soil environment—degradation and their impact on microbial activity and diversity, Front. Microbiol., 10, 338, 10.3389/fmicb.2019.00338 · DOI
  14. Fahrenfeld, 2013, Reclaimed water as a reservoir of antibiotic resistance genes: distribution system and irrigation implications. Frontiers in Microbiology, 4
  15. Gao, 2012, Correlation of tetracycline and sulfonamide antibiotics with corresponding resistance genes and resistant bacteria in a conventional municipal wastewater treatment plant, Sci. Total Environ., 421–422, 173, 10.1016/j.scitotenv.2012.01.061 · DOI
  16. Ghaly, 2020, The peril and promise of integrons: beyond antibiotic resistance, Trends Microbiol., 28, 455, 10.1016/j.tim.2019.12.002 · DOI
  17. Gillings, 2015, Using the class 1 integron-integrase gene as a proxy for anthropogenic pollution, ISME J., 9, 1269, 10.1038/ismej.2014.226 · DOI
  18. Gudda, 2020, Antibiotic-contaminated wastewater irrigated vegetables pose resistance selection risks to the gut microbiome, Environ. Pollut., 264, 114752, 10.1016/j.envpol.2020.114752 · DOI
  19. Han, 2018, Antibiotic resistance genes and associated bacterial communities in agricultural soils amended with different sources of animal manures, Soil Biol. Biochem., 126, 91, 10.1016/j.soilbio.2018.08.018 · DOI
  20. Heuer, 2011, Antibiotic resistance gene spread due to manure application on agricultural fields, Curr. Opin. Microbiol., 14, 236, 10.1016/j.mib.2011.04.009 · DOI · Paper page
  21. Huang, 2019, Occurrence and distribution of antibiotics and antibiotic resistant genes in water and sediments of urban rivers with black-odor water in Guangzhou, South China, Sci. Total Environ., 670, 170, 10.1016/j.scitotenv.2019.03.168 · DOI
  22. Ji, 2012, Antibiotic resistance gene abundances associated with antibiotics and heavy metals in animal manures and agricultural soils adjacent to feedlots in Shanghai; China, J. Hazard. Mater., 235–236, 178, 10.1016/j.jhazmat.2012.07.040 · DOI
  23. Kantiani, 2009, Fully automated analysis of β-lactams in bovine milk by online solid phase extraction-liquid chromatography-electrospray-tandem mass spectrometry, Anal. Chem., 81, 4285, 10.1021/ac9001386 · DOI
  24. Lambirth, 2018, Microbial community composition and antibiotic resistance genes within a North Carolina urban water system, Water, 10, 1539, 10.3390/w10111539 · DOI
  25. Lamm, 2009, Detection of amoxicillin-diketopiperazine-2′, 5′ in wastewater samples, J. Environ. Sci. Health A, 44, 1512, 10.1080/10934520903263306 · DOI
  26. Liu, 2019, Occurrence and fate of antibiotics and antibiotic resistance genes in typical urban water of Beijing, China, Environ. Pollut., 246, 163, 10.1016/j.envpol.2018.12.005 · DOI
  27. Manaia, 2018, Antibiotic resistance in wastewater treatment plants: tackling the black box, Environ. Int., 10.1016/j.envint.2018.03.044 · DOI
  28. Marano, R.B.M., Zolti, A., Jurkevitch, E., Cytryn, E., 2019. Antibiotic resistance and class 1 integron gene dynamics along effluent, reclaimed wastewater irrigated soil, crop continua: elucidating potential risks and ecological constraints. Water Research 164. doi:https://doi.org/10.1016/j.watres.2019.114906. · DOI
  29. Munir, 2011, Release of antibiotic resistant bacteria and genes in the effluent and biosolids of five wastewater utilities in Michigan, Water Res., 45, 681, 10.1016/j.watres.2010.08.033 · DOI
  30. Negreanu, 2012, Impact of treated wastewater irrigation on antibiotic resistance in agricultural soils, Environ. Sci. Technol., 46, 4800, 10.1021/es204665b · DOI
  31. Nguyen, B. A. T., Chen, Q. L., He, J. Z., & Hu, H. W. (2020). Microbial regulation of natural antibiotic resistance: understanding the protist-bacteria interactions for evolution of soil resistome. In Science of the Total Environment (Vol. 705, p. 135882). Elsevier B.V. doi:https://doi.org/10.1016/j.scitotenv.2019.135882. · DOI
  32. Nguyen, 2019, Association between heavy metals and antibiotic-resistant human pathogens in environmental reservoirs: a review, Front. Environ. Sci. Eng., 13, 46, 10.1007/s11783-019-1129-0 · DOI
  33. Obayomi, 2019, Importance of soil texture to the fate of pathogens introduced by irrigation with treated wastewater, Sci. Total Environ., 653, 886, 10.1016/j.scitotenv.2018.10.378 · DOI
  34. Obayomi, 2020, Soil texture and properties rather than irrigation water type shape the diversity and composition of soil microbial communities, Appl. Soil Ecol., 161, 103834, 10.1016/j.apsoil.2020.103834 · DOI
  35. Oliveira, 2020, The environmental contribution to the dissemination of carbapenem and (fluoro)quinolone resistance genes by discharged and reused wastewater effluents: the role of cellular and extracellular DNA, Water Res., 182, 116011, 10.1016/j.watres.2020.116011 · DOI
  36. Orlofsky, 2016, Comparable levels of microbial contamination in soil and on tomato crops after drip irrigation with treated wastewater or potable water, Agric. Ecosyst. Environ., 215, 140, 10.1016/j.agee.2015.08.008 · DOI
  37. Paranychianakis, 2015, Water reuse in EU states: necessity for uniform criteria to mitigate human and environmental risks, Crit. Rev. Environ. Sci. Technol., 45, 1409, 10.1080/10643389.2014.955629 · DOI
  38. Pärnänen, K.M.M., Narciso-da-Rocha, C., Kneis, D., Berendonk, T.U., Cacace, D., Do, T.T., Elpers, C., Fatta-Kassinos, D., Henriques, I., Jaeger, T., Karkman, A., Martinez, J.L., Michael, S.G., Michael-Kordatou, I., O'Sullivan, K., Rodriguez-Mozaz, S., Schwartz, T., Sheng, H., Sørum, H., Stedtfeld, R.D., Tiedje, J.M., Giustina, S.V.D., Walsh, F., Vaz-Moreira, I., Virta, M., Manaia, C.M., 2019. Antibiotic resistance in European wastewater treatment plants mirrors the pattern of clinical antibiotic resistance prevalence. Sci. Adv. 5, eaau9124. doi:https://doi.org/10.1126/sciadv.aau9124. · DOI
  39. Parra-Saldivar, 2020, Sources of Pharmaceuticals in Water, 10.1007/698_2020_623 · DOI
  40. Payment, P., Plante, R., Cejka, P., 2001. Removal of indicator bacteria, human enteric viruses, Giardia cysts, and Cryptosporidium oocysts at a large wastewater primary treatment facility. Canadian Journal of Microbiology 47, 188–193. · DOI
  41. Pepper, I.L., Brooks, J.P. and Gerba, C.P., 2018. Antibiotic resistant bacteria in municipal wastes: is there reason for concern? Environmental Science & Technology, 52(7), pp.3949-3959. · DOI
  42. Pruden, 2006, Antibiotic resistance genes as emerging contaminants: studies in Northern Colorado, Environ. Sci. Technol., 40, 7445, 10.1021/es060413l · DOI
  43. Riaz, 2018, Fluoroquinolones (FQs) in the environment: a review on their abundance, sorption and toxicity in soil, Chemosphere., 10.1016/j.chemosphere.2017.10.092 · DOI
  44. Rizzo, 2020, Best available technologies and treatment trains to address current challenges in urban wastewater reuse for irrigation of crops in EU countries, Sci. Total Environ., 710, 136312, 10.1016/j.scitotenv.2019.136312 · DOI · Paper page
  45. Santiago, 2016, Effects of soil moisture depletion on vegetable crop uptake of pharmaceuticals and personal care products (PPCPs), Environ. Sci. Pollut. Res., 23, 20257, 10.1007/s11356-016-7194-z · DOI
  46. Schweizer, 2019, Soil microaggregate size composition and organic matter distribution as affected by clay content, Geoderma, 355, 113901, 10.1016/j.geoderma.2019.113901 · DOI
  47. Seiler, 2012, Heavy metal driven co-selection of antibiotic resistance in soil and water bodies impacted by agriculture and aquaculture, Front. Microbiol., 3, 399, 10.3389/fmicb.2012.00399 · DOI · Paper page
  48. Smalla, 2018, Environmental dimensions of antibiotic resistance: assessment of basic science gaps, FEMS Microbiol. Ecol., 94, 1, 10.1093/femsec/fiy195 · DOI
  49. Subirats, 2019, High-quality treated wastewater causes remarkable changes in natural microbial communities and intI1 gene abundance, Water Res., 167, 114895, 10.1016/j.watres.2019.114895 · DOI
  50. Sui, 2019, Fate of microbial pollutants and evolution of antibiotic resistance in three types of soil amended with swine slurry, Environ. Pollut., 245, 353, 10.1016/j.envpol.2018.11.003 · DOI
  51. Tolls, 2001, Sorption of veterinary pharmaceuticals in soils: a review, Environ. Sci. Technol., 35, 3397, 10.1021/es0003021 · DOI
  52. Wegst-Uhrich, 2014, Assessing antibiotic sorption in soil: a literature review and new case studies on sulfonamides and macrolides, Chemistry Central Journal, 8, 5, 10.1186/1752-153X-8-5 · DOI
  53. Wickham, 2016, Getting started with ggplot2, 10.1007/978-3-319-24277-4_2 · DOI
  54. Zammit, 2020, Changes in antibiotic resistance gene levels in soil after irrigation with treated wastewater: a comparison between heterogeneous photocatalysis and chlorination, Environ. Sci. Technol., 54, 7677, 10.1021/acs.est.0c01565 · DOI · Paper page
  55. Zhang, 2018, Soil types influence the fate of antibiotic-resistant bacteria and antibiotic resistance genes following the land application of sludge composts, Environ. Int., 118, 34, 10.1016/j.envint.2018.05.029 · DOI
  56. Zhang, 2018, Distribution of ARGs and MGEs among glacial soil, permafrost, and sediment using metagenomic analysis, Environ. Pollut., 234, 339, 10.1016/j.envpol.2017.11.031 · DOI
  57. Zhang, 2018, Sub-inhibitory concentrations of heavy metals facilitate the horizontal transfer of plasmid-mediated antibiotic resistance genes in water environment, Environ. Pollut., 237, 74, 10.1016/j.envpol.2018.01.032 · DOI · Paper page
  58. Zhao, 2019, Evidence for co-selection of antibiotic resistance genes and mobile genetic elements in metal polluted urban soils, Sci. Total Environ., 656, 512, 10.1016/j.scitotenv.2018.11.372 · DOI · Paper page

Cited by

Sorted by citations

Metadata

Authors
Seyoum, M. M., Obayomi, O., Bernstein, N., Williams, C. F., & Gillor, O.
Affiliations
  • Ben-Gurion University of the Negev (IL)
  • Agricultural Research Organization (IL)
  • U.S. Arid Land Agricultural Research Center (US)
Corresponding author
Gillor, Osnat
ORCID
Venue
Science of The Total Environment
Publisher
Elsevier BV
Published
2021-08
Volume
782
Pages
146835
ISSN
0048-9697 (ISSN-L)
DOI
10.1016/j.scitotenv.2021.146835
OpenAlex
W3142397710
Cited by
70
References
1
Citations by year
2026: 14 · 2025: 14 · 2024: 11 · 2023: 12 · 2022: 16 · 2021: 3
FWCI
2.62
Type
journal article
Language
en
Open access
closed
Licence
Locations
  • The Science of The Total Environment (publishedVersion)
  • PubMed (publishedVersion)
Funders
Israel Ministry of Agriculture and Rural Development
Topics
  • Physical Sciences › Environmental Science › Pollution › Pharmaceutical and Antibiotic Environmental Impacts
  • Physical Sciences › Environmental Science › Waste Management and Disposal › Wastewater Treatment and Reuse
  • Health Sciences › Medicine › Infectious Diseases › Antibiotic Use and Resistance
Keywords
antibiotic residues, antibiotic resistance genes, treated wastewater irrigation, soil contamination, soil texture, clay content, class 1 integron, heavy metals, soil organic matter, irrigation water quality
MeSH terms
Anti-Bacterial Agents, Drug Resistance, Microbial, Genes, Bacterial, Soil, Soil Microbiology, Agricultural Irrigation, Wastewater

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review