The effect of sulfadiazine in manure on accumulation of sulfonamide resistance genes in freshly consumable plants

Abstract Background Antibiotic resistance genes will spread via soil fertilized with animal manure to food products. Especially plants whose harvested products can be consumed freshly are of concern. The aim of this study was to assess the impact of sulfadiazine (SDZ)-manured soil on the occurrence...

Full description

Bibliographic Details
Main Authors: Leo van Overbeek, Björn Berendsen, Stefan Aanstoot, Alex Bossers, Els Nijhuis, Lina Russ, Beatriz Andreo Jimenez
Format: Article
Language:English
Published: BMC 2023-09-01
Series:CABI Agriculture and Bioscience
Subjects:
Online Access:https://doi.org/10.1186/s43170-023-00174-2
_version_ 1797451810893463552
author Leo van Overbeek
Björn Berendsen
Stefan Aanstoot
Alex Bossers
Els Nijhuis
Lina Russ
Beatriz Andreo Jimenez
author_facet Leo van Overbeek
Björn Berendsen
Stefan Aanstoot
Alex Bossers
Els Nijhuis
Lina Russ
Beatriz Andreo Jimenez
author_sort Leo van Overbeek
collection DOAJ
description Abstract Background Antibiotic resistance genes will spread via soil fertilized with animal manure to food products. Especially plants whose harvested products can be consumed freshly are of concern. The aim of this study was to assess the impact of sulfadiazine (SDZ)-manured soil on the occurrence of sulfonamide (SA) resistance genes in freshly consumable plants. Methods Sulfadiazine-containing manure was administered via soil to lettuce and leek plants. At harvest, the rhizosphere soil, roots and leaves were investigated on the presence of SDZ-resistant bacteria and sul1 and sul2 genes via qPCR. Further, the impact of SDZ in manure on bacterial community and antibiotic resistance gene composition via amplicon sequencing and shotgun metagenomics was investigated in rhizosphere soils. Results Amendment of SDZ to manure resulted in an increase in sul2 genes in manure. However, abundances of sul genes in rhizosphere soils was strongly determined by plant growth and not by soil treatments with SDZ-manure, which was also the case for the bacterial community composition. Effects of SDZ at low or undetectable levels in leek rhizosphere soil became evident by bacterial association network and resistome analyses, and also in roots and leaves by SDZ-selective bacterial cultivation. Conclusions Antibiotic residues present in animal manure can lead to an increase in antibiotic resistances in food products. Plants play an important role in selection of antibiotic resistance genes present in manured soil. Transmission of antibiotic resistances via manure to the soil–plant ecosystem must be placed into the context of soils as vast reservoirs of ARGs.
first_indexed 2024-03-09T14:59:47Z
format Article
id doaj.art-28ccf2fd22c64ee0bccd9bec64be46b8
institution Directory Open Access Journal
issn 2662-4044
language English
last_indexed 2024-03-09T14:59:47Z
publishDate 2023-09-01
publisher BMC
record_format Article
series CABI Agriculture and Bioscience
spelling doaj.art-28ccf2fd22c64ee0bccd9bec64be46b82023-11-26T13:58:53ZengBMCCABI Agriculture and Bioscience2662-40442023-09-014111510.1186/s43170-023-00174-2The effect of sulfadiazine in manure on accumulation of sulfonamide resistance genes in freshly consumable plantsLeo van Overbeek0Björn Berendsen1Stefan Aanstoot2Alex Bossers3Els Nijhuis4Lina Russ5Beatriz Andreo Jimenez6Wageningen Plant Research (WPR), Wageningen University & ResearchWageningen Food Safety Research (WFSR), Wageningen University & ResearchWageningen Plant Research (WPR), Wageningen University & ResearchWageningen Bioveterinary Research (WBVR), Wageningen University & ResearchWageningen Plant Research (WPR), Wageningen University & ResearchWageningen Plant Research (WPR), Wageningen University & ResearchWageningen Plant Research (WPR), Wageningen University & ResearchAbstract Background Antibiotic resistance genes will spread via soil fertilized with animal manure to food products. Especially plants whose harvested products can be consumed freshly are of concern. The aim of this study was to assess the impact of sulfadiazine (SDZ)-manured soil on the occurrence of sulfonamide (SA) resistance genes in freshly consumable plants. Methods Sulfadiazine-containing manure was administered via soil to lettuce and leek plants. At harvest, the rhizosphere soil, roots and leaves were investigated on the presence of SDZ-resistant bacteria and sul1 and sul2 genes via qPCR. Further, the impact of SDZ in manure on bacterial community and antibiotic resistance gene composition via amplicon sequencing and shotgun metagenomics was investigated in rhizosphere soils. Results Amendment of SDZ to manure resulted in an increase in sul2 genes in manure. However, abundances of sul genes in rhizosphere soils was strongly determined by plant growth and not by soil treatments with SDZ-manure, which was also the case for the bacterial community composition. Effects of SDZ at low or undetectable levels in leek rhizosphere soil became evident by bacterial association network and resistome analyses, and also in roots and leaves by SDZ-selective bacterial cultivation. Conclusions Antibiotic residues present in animal manure can lead to an increase in antibiotic resistances in food products. Plants play an important role in selection of antibiotic resistance genes present in manured soil. Transmission of antibiotic resistances via manure to the soil–plant ecosystem must be placed into the context of soils as vast reservoirs of ARGs.https://doi.org/10.1186/s43170-023-00174-2Antibiotic resistanceFreshly consumable plantsOne healthRhizosphere soilSulfadiazineSulfonamide resistance genes
spellingShingle Leo van Overbeek
Björn Berendsen
Stefan Aanstoot
Alex Bossers
Els Nijhuis
Lina Russ
Beatriz Andreo Jimenez
The effect of sulfadiazine in manure on accumulation of sulfonamide resistance genes in freshly consumable plants
CABI Agriculture and Bioscience
Antibiotic resistance
Freshly consumable plants
One health
Rhizosphere soil
Sulfadiazine
Sulfonamide resistance genes
title The effect of sulfadiazine in manure on accumulation of sulfonamide resistance genes in freshly consumable plants
title_full The effect of sulfadiazine in manure on accumulation of sulfonamide resistance genes in freshly consumable plants
title_fullStr The effect of sulfadiazine in manure on accumulation of sulfonamide resistance genes in freshly consumable plants
title_full_unstemmed The effect of sulfadiazine in manure on accumulation of sulfonamide resistance genes in freshly consumable plants
title_short The effect of sulfadiazine in manure on accumulation of sulfonamide resistance genes in freshly consumable plants
title_sort effect of sulfadiazine in manure on accumulation of sulfonamide resistance genes in freshly consumable plants
topic Antibiotic resistance
Freshly consumable plants
One health
Rhizosphere soil
Sulfadiazine
Sulfonamide resistance genes
url https://doi.org/10.1186/s43170-023-00174-2
work_keys_str_mv AT leovanoverbeek theeffectofsulfadiazineinmanureonaccumulationofsulfonamideresistancegenesinfreshlyconsumableplants
AT bjornberendsen theeffectofsulfadiazineinmanureonaccumulationofsulfonamideresistancegenesinfreshlyconsumableplants
AT stefanaanstoot theeffectofsulfadiazineinmanureonaccumulationofsulfonamideresistancegenesinfreshlyconsumableplants
AT alexbossers theeffectofsulfadiazineinmanureonaccumulationofsulfonamideresistancegenesinfreshlyconsumableplants
AT elsnijhuis theeffectofsulfadiazineinmanureonaccumulationofsulfonamideresistancegenesinfreshlyconsumableplants
AT linaruss theeffectofsulfadiazineinmanureonaccumulationofsulfonamideresistancegenesinfreshlyconsumableplants
AT beatrizandreojimenez theeffectofsulfadiazineinmanureonaccumulationofsulfonamideresistancegenesinfreshlyconsumableplants
AT leovanoverbeek effectofsulfadiazineinmanureonaccumulationofsulfonamideresistancegenesinfreshlyconsumableplants
AT bjornberendsen effectofsulfadiazineinmanureonaccumulationofsulfonamideresistancegenesinfreshlyconsumableplants
AT stefanaanstoot effectofsulfadiazineinmanureonaccumulationofsulfonamideresistancegenesinfreshlyconsumableplants
AT alexbossers effectofsulfadiazineinmanureonaccumulationofsulfonamideresistancegenesinfreshlyconsumableplants
AT elsnijhuis effectofsulfadiazineinmanureonaccumulationofsulfonamideresistancegenesinfreshlyconsumableplants
AT linaruss effectofsulfadiazineinmanureonaccumulationofsulfonamideresistancegenesinfreshlyconsumableplants
AT beatrizandreojimenez effectofsulfadiazineinmanureonaccumulationofsulfonamideresistancegenesinfreshlyconsumableplants