The emerging threat of human-use antifungals in sustainable and circular agriculture schemes

TY - JOUR

T1 - The emerging threat of human-use antifungals in sustainable and circular agriculture schemes

AU - Sallach, J. Brett

AU - Thirkell, Tom J.

AU - Field, Katie J.

AU - Carter, Laura J.

N1 - Funding Information: JBS was supported by funding from the European Union's Horizon 2020 research and innovation programme under the Marie Skłodowska‐Curie Grant Agreement No. 706151. KJF is supported by a Biotechnology and Biological Sciences Research Council (BBSRC) Translational Fellowship (BB/M026825/1) and the H2020 European Research Council (865225). LJC was supported by funding from a UK Research and Innovation (UKRI) Future Leaders Fellowship (Grant Number MR/S032126/1). The project also received financial support from the N8 Agrifood Pump Priming Award. Publisher Copyright: © 2021 The Authors. Plants, People, Planet published by John Wiley & Sons Ltd on behalf of New Phytologist Foundation.

PY - 2021/11/1

Y1 - 2021/11/1

N2 - Rapidly growing global populations mandate greater crop productivity despite increasingly scarce natural resources, including freshwater. The adoption of sustainable agricultural practices seek to address such issues, but an unintended consequence is the exposure of agricultural soils and associated biota to emerging contaminants including azole pharmaceutical antifungals. We show that environmentally relevant exposure to three commonly prescribed azole antifungals can reduce mycorrhizal 33P transfer from the soil into the host plant. This suggests that exposure to azoles may have a significant impact on mycorrhizal-mediated transfer of nutrients in soil-plant systems. Understanding the unintended consequences of sustainable agricultural practices is needed to ensure the security and safety of future food production systems. Summary: Sustainable farming practices are increasingly necessary to meet the demands of a growing population under constraints imposed by climate change. These practices, in particular the reuse of wastewater and amending soil with wastewater derived biosolids, provide a pathway for man-made chemicals to enter the agricultural environment. Among the chemicals commonly detected in wastewater and biosolids are pharmaceutical azole antifungals. Fungi, in particular mycorrhiza-forming fungal symbionts of plant roots, are key drivers of nutrient cycling in the soil–plant system. As such, greater understanding of the impacts of azole antifungal exposure in agricultural systems is urgently needed. We exposed wheat (Triticum aestivum L. cv. ‘Skyfall’) and arbuscular mycorrhizal fungi to environmentally relevant concentrations of three azole antifungals (clotrimazole, miconazole nitrate and fluconazole). We traced the mycorrhizal-acquired 33P from the soil into the host plant in contaminated versus non-contaminated soils and found 33P transfer from mycorrhizal fungi to host plants was reduced in soils containing antifungals. This represents a potentially major disruption to soil nutrient flows as a result of soil contamination. Our work raises the major issue of exposure of soil biota to pharmaceuticals such as azole antifungals, introduced via sustainable agricultural practices, as a potentially globally important disruptive influence on soil nutrient cycles. The impacts of these compounds on non-target organisms, beneficial mycorrhizal fungi in particular, could have major implications on security and sustainability of future food systems.

AB - Rapidly growing global populations mandate greater crop productivity despite increasingly scarce natural resources, including freshwater. The adoption of sustainable agricultural practices seek to address such issues, but an unintended consequence is the exposure of agricultural soils and associated biota to emerging contaminants including azole pharmaceutical antifungals. We show that environmentally relevant exposure to three commonly prescribed azole antifungals can reduce mycorrhizal 33P transfer from the soil into the host plant. This suggests that exposure to azoles may have a significant impact on mycorrhizal-mediated transfer of nutrients in soil-plant systems. Understanding the unintended consequences of sustainable agricultural practices is needed to ensure the security and safety of future food production systems. Summary: Sustainable farming practices are increasingly necessary to meet the demands of a growing population under constraints imposed by climate change. These practices, in particular the reuse of wastewater and amending soil with wastewater derived biosolids, provide a pathway for man-made chemicals to enter the agricultural environment. Among the chemicals commonly detected in wastewater and biosolids are pharmaceutical azole antifungals. Fungi, in particular mycorrhiza-forming fungal symbionts of plant roots, are key drivers of nutrient cycling in the soil–plant system. As such, greater understanding of the impacts of azole antifungal exposure in agricultural systems is urgently needed. We exposed wheat (Triticum aestivum L. cv. ‘Skyfall’) and arbuscular mycorrhizal fungi to environmentally relevant concentrations of three azole antifungals (clotrimazole, miconazole nitrate and fluconazole). We traced the mycorrhizal-acquired 33P from the soil into the host plant in contaminated versus non-contaminated soils and found 33P transfer from mycorrhizal fungi to host plants was reduced in soils containing antifungals. This represents a potentially major disruption to soil nutrient flows as a result of soil contamination. Our work raises the major issue of exposure of soil biota to pharmaceuticals such as azole antifungals, introduced via sustainable agricultural practices, as a potentially globally important disruptive influence on soil nutrient cycles. The impacts of these compounds on non-target organisms, beneficial mycorrhizal fungi in particular, could have major implications on security and sustainability of future food systems.

KW - antifungal

KW - arbuscular mycorrhizal fungi

KW - azole

KW - emerging contaminants

KW - nutrient cycling

KW - organic fertiliser

KW - pharmaceutical pollution

KW - wastewater reuse

UR - http://www.scopus.com/inward/record.url?scp=85113286669&partnerID=8YFLogxK

U2 - 10.1002/ppp3.10222

DO - 10.1002/ppp3.10222

M3 - Article

AN - SCOPUS:85113286669

SN - 2572-2611

VL - 3

SP - 685

EP - 693

JO - Plants People Planet

JF - Plants People Planet

IS - 6

ER -