Azole antifungal contaminants disrupt mycorrhizal function and risk agricultural sustainability

Societal Impact Statement Global food production is increasingly threatened by soil degradation, climate change and the rising costs of synthetic fertilisers. Circular agriculture, which promotes resource reuse, is a promising solution, but using treated wastewater and biosolids in farming introduces risks from emerging contaminants like pharmaceutical residues. Our study examined how common antifungal drugs affect beneficial soil fungi that support plant growth. We found that these contaminants significantly reduced fungal health and impaired nutrient uptake in crops. These findings highlight the urgent need for stronger regulations to protect soil ecosystems, ensuring the long-term sustainability of agriculture and global food security.

Summary Circular agriculture promotes waste reduction and resource reuse. However, integrating treated wastewater and biosolids into food production systems introduces emerging contaminants, including pharmaceuticals, with unknown consequences for soil health and function. We examined the impacts of commonly detected azole antifungal pharmaceuticals (clotrimazole, miconazole nitrate, fluconazole) on arbuscular mycorrhizal (AM) fungi, in lettuce and spring onion. Spring onion and lettuce were grown in AM fungi-inoculated soil with/without antifungal azoles; isotope tracers (15N, 33P, 14C) were used to quantify nutrient exchange and C flow; AM fungal colonisation and soil hyphae were assessed microscopically; plant tissues were analysed for isotope uptake and biomass; root and soil DNA was sequenced (16S/ITS) and analysed in R for microbial community profiling. Azole antifungal exposure significantly impaired AM structures in both species, reducing soil AM hyphal densities by approximately 70% (P < 0.05 and P < 0.001 in spring onion and lettuce, respectively) and AM fungal root colonisation by approximately 72–82% (P < 0.001 for both species). AM function was also negatively impacted, evidenced by a complete shutdown of AM-mediated phosphorus (P) acquisition, in terms of shoot 33P concentration (P < 0.001), and a significant decline in soil fungal diversity in spring onion-AM systems (Shannon's diversity: P < 0.05; Simpson diversity: P < 0.01). Interestingly, the effects were nutrient-dependent, as only AM-mediated P acquisition (33P concentration) was reduced. As such, the concentration of total P in shoot tissues significantly declined under azole exposure for both plant hosts (spring onion: P < 0.01; lettuce: P < 0.05), while N was, again, not impacted (spring onion: P = 0.0798; lettuce: P = 0.577). Our findings highlight the context-dependent nature of soil microbial responses to emerging contaminants and underscore the urgent need for further research. Such research is essential to inform improved regulations aimed at mitigating the unintended impacts of these contaminants on soil microbiomes and agricultural sustainability.