Manure and Doxycycline Affect the Bacterial Community and Its Resistome in Lettuce Rhizosphere and Bulk Soil
Manure application to agricultural soil introduces antibiotic residues and increases the abundance of antibiotic-resistant bacteria (ARB) carrying antibiotic resistance genes (ARGs), often located on mobile genetic elements (MGEs). The rhizosphere is regarded as a hotspot of microbial activity and g...
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Language: | English |
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Frontiers Media S.A.
2019-04-01
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Series: | Frontiers in Microbiology |
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Online Access: | https://www.frontiersin.org/article/10.3389/fmicb.2019.00725/full |
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author | Khald Blau Samuel Jacquiod Søren J. Sørensen Jian-Qiang Su Yong-Guan Zhu Yong-Guan Zhu Kornelia Smalla Sven Jechalke |
author_facet | Khald Blau Samuel Jacquiod Søren J. Sørensen Jian-Qiang Su Yong-Guan Zhu Yong-Guan Zhu Kornelia Smalla Sven Jechalke |
author_sort | Khald Blau |
collection | DOAJ |
description | Manure application to agricultural soil introduces antibiotic residues and increases the abundance of antibiotic-resistant bacteria (ARB) carrying antibiotic resistance genes (ARGs), often located on mobile genetic elements (MGEs). The rhizosphere is regarded as a hotspot of microbial activity and gene transfer, which can alter and prolong the effects of organic fertilizers containing antibiotics. However, not much is known about the influence of plants on the effects of doxycycline applied to soil via manure. In this study, the effects of manure spiked with or without doxycycline on the prokaryotic community composition as well as on the relative abundance of ARGs and MGEs in lettuce rhizosphere and bulk soil were investigated by means of a polyphasic cultivation-independent approach. Samples were taken 42 days after manure application, and total community DNA was extracted. Besides a pronounced manure effect, doxycycline spiking caused an additional enrichment of ARGs and MGEs. High-throughput quantitative PCR revealed an increase in tetracycline, aminoglycoside, and macrolide–lincosamide–streptogramin B (MLSB) resistance genes associated with the application of manure spiked with doxycycline. This effect was unexpectedly lower in the rhizosphere than in bulk soil, suggesting a faster dissipation of the antibiotic and a more resilient prokaryotic community in the rhizosphere. Interestingly, the tetracycline resistance gene tetA(P) was highly enriched in manure-treated bulk soil and rhizosphere, with highest values observed in doxycycline-treated bulk soil, concurring with an enrichment of Clostridia. Thus, the gene tetA(P) might be a suitable marker of soil contamination by ARB, ARGs, and antibiotics of manure origin. These findings illustrate that the effects of manure and doxycycline on ARGs and MGEs differ between rhizosphere and bulk soil, which needs to be considered when assessing risks for human health connected to the spread of ARGs in the environment. |
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issn | 1664-302X |
language | English |
last_indexed | 2024-04-12T21:43:41Z |
publishDate | 2019-04-01 |
publisher | Frontiers Media S.A. |
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spelling | doaj.art-c3d630aeddd4435885de48e4a7ad204b2022-12-22T03:15:42ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2019-04-011010.3389/fmicb.2019.00725453226Manure and Doxycycline Affect the Bacterial Community and Its Resistome in Lettuce Rhizosphere and Bulk SoilKhald Blau0Samuel Jacquiod1Søren J. Sørensen2Jian-Qiang Su3Yong-Guan Zhu4Yong-Guan Zhu5Kornelia Smalla6Sven Jechalke7Julius Kühn-Institut—Federal Research Centre for Cultivated Plants, Institute for Epidemiology and Pathogen Diagnostics, Braunschweig, GermanySection of Microbiology, Department of Biology, University of Copenhagen, Copenhagen, DenmarkSection of Microbiology, Department of Biology, University of Copenhagen, Copenhagen, DenmarkKey Lab of Urban Environment and Health, Institute of Urban Environment, Chinese Academy of Sciences, Xiamen, ChinaKey Lab of Urban Environment and Health, Institute of Urban Environment, Chinese Academy of Sciences, Xiamen, ChinaState Key Lab of Urban and Regional Ecology, Research Center for Eco-Environmental Sciences, Chinese Academy of Sciences, Beijing, ChinaJulius Kühn-Institut—Federal Research Centre for Cultivated Plants, Institute for Epidemiology and Pathogen Diagnostics, Braunschweig, GermanyJulius Kühn-Institut—Federal Research Centre for Cultivated Plants, Institute for Epidemiology and Pathogen Diagnostics, Braunschweig, GermanyManure application to agricultural soil introduces antibiotic residues and increases the abundance of antibiotic-resistant bacteria (ARB) carrying antibiotic resistance genes (ARGs), often located on mobile genetic elements (MGEs). The rhizosphere is regarded as a hotspot of microbial activity and gene transfer, which can alter and prolong the effects of organic fertilizers containing antibiotics. However, not much is known about the influence of plants on the effects of doxycycline applied to soil via manure. In this study, the effects of manure spiked with or without doxycycline on the prokaryotic community composition as well as on the relative abundance of ARGs and MGEs in lettuce rhizosphere and bulk soil were investigated by means of a polyphasic cultivation-independent approach. Samples were taken 42 days after manure application, and total community DNA was extracted. Besides a pronounced manure effect, doxycycline spiking caused an additional enrichment of ARGs and MGEs. High-throughput quantitative PCR revealed an increase in tetracycline, aminoglycoside, and macrolide–lincosamide–streptogramin B (MLSB) resistance genes associated with the application of manure spiked with doxycycline. This effect was unexpectedly lower in the rhizosphere than in bulk soil, suggesting a faster dissipation of the antibiotic and a more resilient prokaryotic community in the rhizosphere. Interestingly, the tetracycline resistance gene tetA(P) was highly enriched in manure-treated bulk soil and rhizosphere, with highest values observed in doxycycline-treated bulk soil, concurring with an enrichment of Clostridia. Thus, the gene tetA(P) might be a suitable marker of soil contamination by ARB, ARGs, and antibiotics of manure origin. These findings illustrate that the effects of manure and doxycycline on ARGs and MGEs differ between rhizosphere and bulk soil, which needs to be considered when assessing risks for human health connected to the spread of ARGs in the environment.https://www.frontiersin.org/article/10.3389/fmicb.2019.00725/fullmanurebulk soillettuce rhizosphereresistance genesprokaryotic communityhigh-throughput quantitative polymerase chain reaction |
spellingShingle | Khald Blau Samuel Jacquiod Søren J. Sørensen Jian-Qiang Su Yong-Guan Zhu Yong-Guan Zhu Kornelia Smalla Sven Jechalke Manure and Doxycycline Affect the Bacterial Community and Its Resistome in Lettuce Rhizosphere and Bulk Soil Frontiers in Microbiology manure bulk soil lettuce rhizosphere resistance genes prokaryotic community high-throughput quantitative polymerase chain reaction |
title | Manure and Doxycycline Affect the Bacterial Community and Its Resistome in Lettuce Rhizosphere and Bulk Soil |
title_full | Manure and Doxycycline Affect the Bacterial Community and Its Resistome in Lettuce Rhizosphere and Bulk Soil |
title_fullStr | Manure and Doxycycline Affect the Bacterial Community and Its Resistome in Lettuce Rhizosphere and Bulk Soil |
title_full_unstemmed | Manure and Doxycycline Affect the Bacterial Community and Its Resistome in Lettuce Rhizosphere and Bulk Soil |
title_short | Manure and Doxycycline Affect the Bacterial Community and Its Resistome in Lettuce Rhizosphere and Bulk Soil |
title_sort | manure and doxycycline affect the bacterial community and its resistome in lettuce rhizosphere and bulk soil |
topic | manure bulk soil lettuce rhizosphere resistance genes prokaryotic community high-throughput quantitative polymerase chain reaction |
url | https://www.frontiersin.org/article/10.3389/fmicb.2019.00725/full |
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