Nectar yeasts of theMetschnikowiaclade are highly susceptible to azole antifungals widely used in medicine and agriculture

Abstract

The widespread use of azole antifungals in medicine and agriculture and the resulting long-persistent residues could potentially affect beneficial fungi. However, there is very little information on the tolerance of non-target environmental fungi to azoles. In this study, we assessed the susceptibility of diverse plant- and insect-associated yeasts from the Metschnikowia clade, including several ecologically important species, to widely used medical and agricultural azoles (epoxiconazole, imazalil, ketoconazole and voriconazole). A total of 120 strains from six species were tested. Minimum inhibitory concentrations (MICs) were determined by the EUCAST broth microdilution procedure after some necessary modifications were made. The majority of species tested were highly susceptible to epoxiconazole, ketoconazole and voriconazole (>95% of strains showed MICs ≤ 0.125 mg l(-1)). Most strains were also very susceptible to imazalil, although MIC values were generally higher than for the other azoles. Furthermore, certain Metschnikowia reukaufii strains displayed a 'trailing' phenotype (i.e. showed reduced but persistent growth at antifungal concentrations above the MIC), but this characteristic was dependent on test conditions. It was concluded that exposure to azoles may pose a risk for ecologically relevant yeasts from the Metschnikowia clade, and thus could potentially impinge on the tripartite interaction linking these fungi with plants and their insect pollinators.

Non‐target effects of fungicides on nectar‐inhabiting fungi of almond flowers

“…Numerous fungi, largely pathogenic taxa, develop resistance to multiple fungicides utilized in agricultural systems (Brent and Hollomon, 1998;Ma and Michailides, 2005;Price et al, 2015). Alvarez-P erez et al (2016) observed that some Metschnikowia strains display a "trailing" phenotype (reduced, but persistent growth) at concentrations above the noted minimum inhibitory concentration observed for synthetic fungicides tested in their study. While this "trailing" phenotype may be a consequence of the assay procedure, it may also suggest inter-and intra-specific variation in susceptibility, which could allow for evolution of resistance.…”

“…Both metconazole (triazole) and penthiopyrad (carboxamide) are broad‐spectrum fungicides effective against many fungal pathogens that target fruit, vegetable, and nut crops. Recently, a suite of synthetic fungicides widely used in agriculture have also been shown to reduce the performance of nectar‐inhabiting yeasts under laboratory conditions (Álvarez‐Pérez et al ., ; Bartlewicz et al ., ), including numerous members of the Metschnikowia clade. Moreover, experimental application of these fungicides to the flowering plant Linaria vulgaris revealed that these effects can also occur in‐situ (Bartlewicz et al ., ).…”

“…For instance, exposure to and consumption of fungicides can have detrimental effects on beneficial macroorganisms such as bees, affecting larval development (Mussen et al, 2004), foraging behavior (Sprayberry et al, 2013), and driving mortality through both direct and indirect pathways (Pettis et al, 2013;Bernauer et al, 2015). Although evidence is mounting on the detrimental effects of agrochemicals on macroorganisms, less attention has been paid to non-target microorganisms that may also benefit crop yield (but see Alvarez-P erez et al, 2016;Bartlewicz et al, 2016).…”

Changes in Phenylpropanoid and Trichothecene Production by Fusarium culmorum and F. graminearum Sensu Stricto via Exposure to Flavonoids

“…However, the efficacy of azoles for disease control often remains contradictory, presumably due to the difficulty of timing and targeting fungicides to heads [ 3 ] and the apparently increased resistance of fungi to this fungicide class [ 4 ]. In addition, azole residues can disperse and persist in the environment due to repeated use of these fungicides [ 5 , 6 , 7 ], which have a considerable impact on ecosystem health and functionality [ 8 ].…”

Characterization of a novel yeast species Metschnikowia persimmonesis KCTC 12991BP (KIOM G15050 type strain) isolated from a medicinal plant, Korean persimmon calyx (Diospyros kaki Thumb)

“…The genus Metschnikowia of the family Metschnikowiaceae (Order Saccharromycetales ) comprises single-celled species that reproduce via budding of vegetative cells and is characterized by the presence of one or two needle-shaped ascospores on elongated asci (Mendonca-Hagler et al 1993 ; Pretorius 2000 ; Marinoni et al 2006 ; Kuan et al 2016 ). A total of 35 Metschnikowia species have been described to date in a wide range of hosts, including flowers, fruits, flower-pollinating insects, and lacewings (Mendonca-Hagler et al 1993 ; Lachance et al 2005 ; Guzmán et al 2013 ; De Vega et al 2014 ; Kuan et al 2016 ; Álvarez-Pérez et al 2016 ). Yeasts provide a variety of unique bioactive metabolites that have medicinal importance (Mager and Winderickx 2005 ; VanderMolen et al 2013 ).…”