Long-term application of Swedish sewage sludge on farmland does not cause clear changes in the soil bacterial resistome

The widespread practice of applying sewage sludge to arable land makes use of nutrients indispensable for crops and reduces the need for inorganic fertilizer, however this application also provides a potential route for human exposure to chemical contaminants and microbial pathogens in the sludge. A...

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Main Authors: Carolin Rutgersson, Stefan Ebmeyer, Simon Bo Lassen, Antti Karkman, Jerker Fick, Erik Kristiansson, Kristian K. Brandt, Carl-Fredrik Flach, D.G. Joakim Larsson
Format: Article
Language:English
Published: Elsevier 2020-04-01
Series:Environment International
Online Access:http://www.sciencedirect.com/science/article/pii/S016041201931788X
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language English
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author Carolin Rutgersson
Stefan Ebmeyer
Simon Bo Lassen
Antti Karkman
Jerker Fick
Erik Kristiansson
Kristian K. Brandt
Carl-Fredrik Flach
D.G. Joakim Larsson
spellingShingle Carolin Rutgersson
Stefan Ebmeyer
Simon Bo Lassen
Antti Karkman
Jerker Fick
Erik Kristiansson
Kristian K. Brandt
Carl-Fredrik Flach
D.G. Joakim Larsson
Long-term application of Swedish sewage sludge on farmland does not cause clear changes in the soil bacterial resistome
Environment International
author_facet Carolin Rutgersson
Stefan Ebmeyer
Simon Bo Lassen
Antti Karkman
Jerker Fick
Erik Kristiansson
Kristian K. Brandt
Carl-Fredrik Flach
D.G. Joakim Larsson
author_sort Carolin Rutgersson
title Long-term application of Swedish sewage sludge on farmland does not cause clear changes in the soil bacterial resistome
title_short Long-term application of Swedish sewage sludge on farmland does not cause clear changes in the soil bacterial resistome
title_full Long-term application of Swedish sewage sludge on farmland does not cause clear changes in the soil bacterial resistome
title_fullStr Long-term application of Swedish sewage sludge on farmland does not cause clear changes in the soil bacterial resistome
title_full_unstemmed Long-term application of Swedish sewage sludge on farmland does not cause clear changes in the soil bacterial resistome
title_sort long-term application of swedish sewage sludge on farmland does not cause clear changes in the soil bacterial resistome
publisher Elsevier
series Environment International
issn 0160-4120
publishDate 2020-04-01
description The widespread practice of applying sewage sludge to arable land makes use of nutrients indispensable for crops and reduces the need for inorganic fertilizer, however this application also provides a potential route for human exposure to chemical contaminants and microbial pathogens in the sludge. A recent concern is that such practice could promote environmental selection and dissemination of antibiotic resistant bacteria or resistance genes. Understanding the risks of sludge amendment in relation to antibiotic resistance development is important for sustainable agriculture, waste treatment and infectious disease management. To assess such risks, we took advantage of an agricultural field trial in southern Sweden, where land used for growing different crops has been amended with sludge every four years since 1981. We sampled raw, semi-digested and digested and stored sludge together with soils from the experimental plots before and two weeks after the most recent amendment in 2017. Levels of selected antimicrobials and bioavailable metals were determined and microbial effects were evaluated using both culture-independent metagenome sequencing and conventional culturing. Antimicrobials or bioavailable metals (Cu and Zn) did not accumulate to levels of concern for environmental selection of antibiotic resistance, and no coherent signs, neither on short or long time scales, of enrichment of antibiotic-resistant bacteria or resistance genes were found in soils amended with digested and stored sewage sludge in doses up to 12 metric tons per hectare. Likewise, only very few and slight differences in microbial community composition were observed after sludge amendment. Taken together, the current study does not indicate risks of sludge amendment related to antibiotic resistance development under the given conditions. Extrapolations should however be done with care as sludge quality and application practices vary between regions. Hence, the antibiotic concentrations and resistance load of the sludge are likely to be higher in regions with larger antibiotic consumption and resistance burden than Sweden. Keywords: Digested sludge, Antibiotic resistance, Agricultural soil, Metagenome sequencing, Bioavailable metals, Bacterial community composition
url http://www.sciencedirect.com/science/article/pii/S016041201931788X
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spelling doaj-7e03ed7e11574c9b8c674367c928702f2020-11-25T00:29:19ZengElsevierEnvironment International0160-41202020-04-01137Long-term application of Swedish sewage sludge on farmland does not cause clear changes in the soil bacterial resistomeCarolin Rutgersson0Stefan Ebmeyer1Simon Bo Lassen2Antti Karkman3Jerker Fick4Erik Kristiansson5Kristian K. Brandt6Carl-Fredrik Flach7D.G. Joakim Larsson8Centre for Antibiotic Resistance Research (CARe) at the University of Gothenburg, Guldhedsgatan 10A, 413 46 Gothenburg, Sweden; Department of Infectious Diseases, Institute of Biomedicine, The Sahlgrenska Academy at the University of Gothenburg, Guldhedsgatan 10A, 413 46 Gothenburg, SwedenCentre for Antibiotic Resistance Research (CARe) at the University of Gothenburg, Guldhedsgatan 10A, 413 46 Gothenburg, Sweden; Department of Infectious Diseases, Institute of Biomedicine, The Sahlgrenska Academy at the University of Gothenburg, Guldhedsgatan 10A, 413 46 Gothenburg, SwedenDepartment of Plant and Environmental Sciences, University of Copenhagen, Thorvaldsensvej 40, 1871 Frederiksberg C, Denmark; Sino-Danish Center for Education and Research (SDC), University of Chinese Academy of Sciences, 380 Huaibeizhuang, Beijing, ChinaCentre for Antibiotic Resistance Research (CARe) at the University of Gothenburg, Guldhedsgatan 10A, 413 46 Gothenburg, Sweden; Department of Infectious Diseases, Institute of Biomedicine, The Sahlgrenska Academy at the University of Gothenburg, Guldhedsgatan 10A, 413 46 Gothenburg, Sweden; Department of Microbiology, University of Helsinki, P.O. Box 56, 00014, Helsinki, FinlandDepartment of Chemistry, Umeå University, Linnaeus väg 6, 901 87 Umeå, SwedenCentre for Antibiotic Resistance Research (CARe) at the University of Gothenburg, Guldhedsgatan 10A, 413 46 Gothenburg, Sweden; Department of Mathematical Sciences, Chalmers University of Technology, 412 96 Gothenburg, SwedenDepartment of Plant and Environmental Sciences, University of Copenhagen, Thorvaldsensvej 40, 1871 Frederiksberg C, DenmarkCentre for Antibiotic Resistance Research (CARe) at the University of Gothenburg, Guldhedsgatan 10A, 413 46 Gothenburg, Sweden; Department of Infectious Diseases, Institute of Biomedicine, The Sahlgrenska Academy at the University of Gothenburg, Guldhedsgatan 10A, 413 46 Gothenburg, SwedenCentre for Antibiotic Resistance Research (CARe) at the University of Gothenburg, Guldhedsgatan 10A, 413 46 Gothenburg, Sweden; Department of Infectious Diseases, Institute of Biomedicine, The Sahlgrenska Academy at the University of Gothenburg, Guldhedsgatan 10A, 413 46 Gothenburg, Sweden; Corresponding author at: Department of Infectious Diseases, Institute of Biomedicine, The Sahlgrenska Academy, University of Gothenburg, Guldhedsgatan 10, SE-413 46 Gothenburg, Sweden.The widespread practice of applying sewage sludge to arable land makes use of nutrients indispensable for crops and reduces the need for inorganic fertilizer, however this application also provides a potential route for human exposure to chemical contaminants and microbial pathogens in the sludge. A recent concern is that such practice could promote environmental selection and dissemination of antibiotic resistant bacteria or resistance genes. Understanding the risks of sludge amendment in relation to antibiotic resistance development is important for sustainable agriculture, waste treatment and infectious disease management. To assess such risks, we took advantage of an agricultural field trial in southern Sweden, where land used for growing different crops has been amended with sludge every four years since 1981. We sampled raw, semi-digested and digested and stored sludge together with soils from the experimental plots before and two weeks after the most recent amendment in 2017. Levels of selected antimicrobials and bioavailable metals were determined and microbial effects were evaluated using both culture-independent metagenome sequencing and conventional culturing. Antimicrobials or bioavailable metals (Cu and Zn) did not accumulate to levels of concern for environmental selection of antibiotic resistance, and no coherent signs, neither on short or long time scales, of enrichment of antibiotic-resistant bacteria or resistance genes were found in soils amended with digested and stored sewage sludge in doses up to 12 metric tons per hectare. Likewise, only very few and slight differences in microbial community composition were observed after sludge amendment. Taken together, the current study does not indicate risks of sludge amendment related to antibiotic resistance development under the given conditions. Extrapolations should however be done with care as sludge quality and application practices vary between regions. Hence, the antibiotic concentrations and resistance load of the sludge are likely to be higher in regions with larger antibiotic consumption and resistance burden than Sweden. Keywords: Digested sludge, Antibiotic resistance, Agricultural soil, Metagenome sequencing, Bioavailable metals, Bacterial community compositionhttp://www.sciencedirect.com/science/article/pii/S016041201931788X