Trophic transfer of silver nanoparticles shifts metabolism in snails and reduces food safety

Food security and sustainable development of agriculture has been a key challenge for decades. To support this, nanotechnology in the agricultural sectors increases productivity and food security, while leaving complex environmental negative impacts including pollution of the human food chains by na...

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Main Authors: Fei Dang, Chengcheng Li, Luís M. Nunes, Ronggui Tang, Junsong Wang, Shuofei Dong, Willie J.G.M. Peijnenburg, Wenxiong Wang, Baoshan Xing, Su Shiung Lam, Christian Sonne
Format: Article
Language:English
Published: Elsevier 2023-06-01
Series:Environment International
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Online Access:http://www.sciencedirect.com/science/article/pii/S0160412023002635
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author Fei Dang
Chengcheng Li
Luís M. Nunes
Ronggui Tang
Junsong Wang
Shuofei Dong
Willie J.G.M. Peijnenburg
Wenxiong Wang
Baoshan Xing
Su Shiung Lam
Christian Sonne
author_facet Fei Dang
Chengcheng Li
Luís M. Nunes
Ronggui Tang
Junsong Wang
Shuofei Dong
Willie J.G.M. Peijnenburg
Wenxiong Wang
Baoshan Xing
Su Shiung Lam
Christian Sonne
author_sort Fei Dang
collection DOAJ
description Food security and sustainable development of agriculture has been a key challenge for decades. To support this, nanotechnology in the agricultural sectors increases productivity and food security, while leaving complex environmental negative impacts including pollution of the human food chains by nanoparticles. Here we model the effects of silver nanoparticles (Ag-NPs) in a food chain consisting of soil-grown lettuce Lactuca sativa and snail Achatina fulica. Soil-grown lettuce were exposed to sulfurized Ag-NPs via root or metallic Ag-NPs via leaves before fed to snails. We discover an important biomagnification of silver in snails sourced from plant root uptake, with trophic transfer factors of 2.0–5.9 in soft tissues. NPs shifts from original size (55–68 nm) toward much smaller size (17–26 nm) in snails. Trophic transfer of Ag-NPs reprograms the global metabolic profile by down-regulating or up-regulating metabolites for up to 0.25- or 4.20- fold, respectively, relative to the control. These metabolites control osmoregulation, phospholipid, energy, and amino acid metabolism in snails, reflecting molecular pathways of biomagnification and pontential adverse biological effects on lower trophic levels. Consumption of these Ag-NP contaminated snails causes non-carcinogenic effects on human health. Global public health risks decrease by 72% under foliar Ag-NP application in agriculture or through a reduction in the consumption of snails sourced from root application. The latter strategy is at the expense of domestic economic losses in food security of $177.3 and $58.3 million annually for countries such as Nigeria and Cameroon. Foliar Ag-NP application in nano-agriculture has lower hazard quotient risks on public health than root application to ensure global food safety, as brought forward by the United Nations Sustainable Development Goals.
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spelling doaj.art-c512fe45730b492f9b8818f6fb3d72a42023-06-04T04:23:07ZengElsevierEnvironment International0160-41202023-06-01176107990Trophic transfer of silver nanoparticles shifts metabolism in snails and reduces food safetyFei Dang0Chengcheng Li1Luís M. Nunes2Ronggui Tang3Junsong Wang4Shuofei Dong5Willie J.G.M. Peijnenburg6Wenxiong Wang7Baoshan Xing8Su Shiung Lam9Christian Sonne10Key Laboratory of Soil Environment and Pollution Remediation, Institute of Soil Science, Chinese Academy of Sciences, Nanjing 210008, China; Stockbridge School of Agriculture, University of Massachusetts, 161 Holdsworth Way, Amherst, MA 01003, United StatesKey Laboratory of Soil Environment and Pollution Remediation, Institute of Soil Science, Chinese Academy of Sciences, Nanjing 210008, China; Corresponding authors at: Department of Ecoscience, Aarhus University, Frederiksborgvej 399, PO Box 358, DK-4000 Roskilde, DenmarkUniversity of Algarve, Civil Engineering Research and Innovation for Sustainability Center, Faro, PortugalKey Laboratory of Soil Environment and Pollution Remediation, Institute of Soil Science, Chinese Academy of Sciences, Nanjing 210008, ChinaCenter for Molecular Metabolism, School of Environmental and Biological Engineering, Nanjing University of Science and Technology, Nanjing 210094, China; Corresponding authors at: Department of Ecoscience, Aarhus University, Frederiksborgvej 399, PO Box 358, DK-4000 Roskilde, DenmarkAgilent Technologies Co. Ltd (China), No.3, Wang Jing Bei Road, Chao Yang District, Beijing 100102, ChinaInstitute of Environmental Sciences (CML), Leiden University, P.O. Box 9518, 2300 RA Leiden, the Netherlands; National Institute of Public Health and the Environment (RIVM), P.O. Box 1, Bilthoven, the NetherlandsSchool of Energy and Environment, City University of Hong Kong, Kowloon, Hong KongStockbridge School of Agriculture, University of Massachusetts, 161 Holdsworth Way, Amherst, MA 01003, United StatesHigher Institution Centre of Excellence (HICoE), Institute of Tropical Aquaculture and Fisheries (AKUATROP), Universiti Malaysia Terengganu, 21030 Kuala Nerus, Terengganu, Malaysia; School of Forestry, Henan Agricultural University, Zhengzhou 450002, ChinaSchool of Forestry, Henan Agricultural University, Zhengzhou 450002, China; Department of Ecoscience, Aarhus University, Frederiksborgvej 399, PO Box 358, DK-4000 Roskilde, Denmark; Corresponding authors at: Department of Ecoscience, Aarhus University, Frederiksborgvej 399, PO Box 358, DK-4000 Roskilde, DenmarkFood security and sustainable development of agriculture has been a key challenge for decades. To support this, nanotechnology in the agricultural sectors increases productivity and food security, while leaving complex environmental negative impacts including pollution of the human food chains by nanoparticles. Here we model the effects of silver nanoparticles (Ag-NPs) in a food chain consisting of soil-grown lettuce Lactuca sativa and snail Achatina fulica. Soil-grown lettuce were exposed to sulfurized Ag-NPs via root or metallic Ag-NPs via leaves before fed to snails. We discover an important biomagnification of silver in snails sourced from plant root uptake, with trophic transfer factors of 2.0–5.9 in soft tissues. NPs shifts from original size (55–68 nm) toward much smaller size (17–26 nm) in snails. Trophic transfer of Ag-NPs reprograms the global metabolic profile by down-regulating or up-regulating metabolites for up to 0.25- or 4.20- fold, respectively, relative to the control. These metabolites control osmoregulation, phospholipid, energy, and amino acid metabolism in snails, reflecting molecular pathways of biomagnification and pontential adverse biological effects on lower trophic levels. Consumption of these Ag-NP contaminated snails causes non-carcinogenic effects on human health. Global public health risks decrease by 72% under foliar Ag-NP application in agriculture or through a reduction in the consumption of snails sourced from root application. The latter strategy is at the expense of domestic economic losses in food security of $177.3 and $58.3 million annually for countries such as Nigeria and Cameroon. Foliar Ag-NP application in nano-agriculture has lower hazard quotient risks on public health than root application to ensure global food safety, as brought forward by the United Nations Sustainable Development Goals.http://www.sciencedirect.com/science/article/pii/S0160412023002635Nano-agricultureBiomagnificationMetabolismHuman healthFood safety
spellingShingle Fei Dang
Chengcheng Li
Luís M. Nunes
Ronggui Tang
Junsong Wang
Shuofei Dong
Willie J.G.M. Peijnenburg
Wenxiong Wang
Baoshan Xing
Su Shiung Lam
Christian Sonne
Trophic transfer of silver nanoparticles shifts metabolism in snails and reduces food safety
Environment International
Nano-agriculture
Biomagnification
Metabolism
Human health
Food safety
title Trophic transfer of silver nanoparticles shifts metabolism in snails and reduces food safety
title_full Trophic transfer of silver nanoparticles shifts metabolism in snails and reduces food safety
title_fullStr Trophic transfer of silver nanoparticles shifts metabolism in snails and reduces food safety
title_full_unstemmed Trophic transfer of silver nanoparticles shifts metabolism in snails and reduces food safety
title_short Trophic transfer of silver nanoparticles shifts metabolism in snails and reduces food safety
title_sort trophic transfer of silver nanoparticles shifts metabolism in snails and reduces food safety
topic Nano-agriculture
Biomagnification
Metabolism
Human health
Food safety
url http://www.sciencedirect.com/science/article/pii/S0160412023002635
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