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

Abstract

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 33 P 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 33 P from the soil into the host plant in contaminated versus non-contaminated soils and found 33 P 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.

Agricultural management and pesticide use reduce the functioning of beneficial plant symbionts

“…Various mechanisms could explain the observed differences in AMF functioning between cropland and grassland soils. First, a range of studies showed that management practices associated with intensive land use, including soil tillage, pesticide and fertilizer use, reduce AMF abundance, spore abundance, AMF diversity and alter AMF community composition 37 – 39 . Our study confirmed that both microbial biomass as well as AMF richness were reduced in intensively managed croplands, and this was linked to a reduced hyphal 33 P transfer ( Table 1 ).…”

“…It further indicates that the common use of fungicides hampers the natural ability of soil organisms to provide crops with nutrients and supports the findings of Sallach et al . (2021) who showed that also fungicides applied unintentionally through wastewater or biosolids can decrease the ability of AMF to transfer P to plants 39 . Future studies under controlled conditions in the field now need to specifically test to which extent fungicides suppress the ability of AMF to support crop growth and test whether such effects are persistent.…”

Soil microbiomes and one health

“…Consequently, researchers are increasingly realizing that the role of microbial communities must be understood and incorporated to safeguard and enhance soil health 49 and there is a growing interest in the practices that can maintain healthy soils. For instance, several studies have shown that crop diversification 50,51 , a reduction of synthetic pesticides 52,53 , mineral fertilizers 35,42 and intensive tillage 54 can improve soil biodiversity and soil health.…”

Occurrence and Effects of Antimicrobials Drugs in Aquatic Ecosystems

“…Inhibits DNA synthesis Metronidazole Human and veterinary [4,21,27,28] Inhibition of polymerization of microtubules Albendazole Human and veterinary [4,21,27,28] Increased permeability of parasite to calcium Prazicuantel Human and veterinary [4,21,27,28] Antifungals Inhibits ergosterol synthesis Ketoconazole Human and veterinary [29,30] Binds to ergosterol and alteration of cytoplasmic membrane Amphotericin B Human and veterinary [29,30] Alteration of microtubules Griseofulvin Human and veterinary [29,30] Antivirals Blocks the active site of neurominidase of the influenza virus Oseltamivir Human and veterinary [31,32] Inhibits viral DNA Polymerase Acyclovir Human and veterinary [31,32] Inhibit reverse transcriptase Lamivudine Zidovudine Human [31]…”

“…For example, Belgium is the country with the highest consumption of systemic antifungals in Europe. In the United Kingdom, approximately 1.5 tons of azole antifungals and 85 and 0.5 kg of griseofulvin and amphotericin B were prescribed, respectively in 2018 [29]. On the other hand, in a hospital in Valencia, Spain, as a consequence of the COVID-19 pandemic, fungal infections increased and consequently the consumption of antifungals in intensive care units increased by 75% in 2020 compared to 2019 [40].…”