A Two-Way Street: How Are Yeasts Impacted by Pesticides and How Can They Help Solve Agrochemical Contamination Problems?

Abstract

Plant-associated yeasts play significant ecological roles within the microbiomes of soils and pollinating insects. In previous studies, we have shown that yeasts can assist pollinators in locating nectar, which is crucial for their nutrition and the reproduction of many angiosperms. Additionally, in soil, yeasts can also act as plant growth promoters. Given the importance of yeasts for plant development, this review first explores the biochemical processes underlying the ecological role of these microorganisms in soil, insects, and in direct association with plants. Based on this premise, we discuss the influence of these relationships on agricultural production, the biological mechanisms through which pesticides negatively affect yeast cells, and how these microorganisms can tolerate widely used agrochemicals. Finally, we address key studies in the literature that support the potential of these microorganisms as bioremediation agents. In this context, we emphasize different experiences with both indigenous and genetically engineered yeasts, which may display enzymes in their surfaces that convert pesticides into less harmful or nontoxic molecules. Our review indicates that yeasts can be effectively harnessed in organic agriculture to promote plant growth and bioremediate contaminated soil or food.

1. Introduction

As food production rises due to population growth, the use of chemicals in agriculture seems to be an inevitable practice. However, although these agrochemicals enhance crop productivity, they also raise significant environmental concerns, particularly regarding their persistence in the soil and food supply [1].

It is essential to consider the soil’s nutrient composition and classification to determine the destination of the residual load of these compounds. Pesticides can affect the pH, moisture levels, organic matter content, and microbial communities in various environments. On the other hand, the environment microbiota can include bacteria and fungi that are often capable of playing important roles in the biodegradation process of these residues [2].

Yeasts are among the microorganisms associated with plants that can be affected to a greater or lesser extent by the use of pesticides. These unicellular fungi play critical ecological roles, either as natural plant defenders against pathogens, plant growth promoters, or producers of volatile organic compounds (VOCs) that attract pollinators to flowers. Yeasts also play a prominent role in nutrient cycling (biogeochemical cycles) and contribute significantly to the digestive and immune systems of herbivores, pollinivores, and nectarivores [3,4].

Since the Neolithic Revolution, yeasts have become humans’ most commonly used microorganisms. It is believed that these single-celled fungi played a crucial role in transitioning from a nomadic hunting–gathering lifestyle to establishing permanent settlements and developing agriculture. Yeasts gained widespread recognition due to their use in producing beer, wine, bread, and fuel ethanol. However, their applications in industry extend far beyond these areas. In fact, yeasts contribute to a market valued at over USD 1.3 trillion annually [5].

Additionally, yeasts are easily and thus widely genetically engineered. Successful yeast transformation processes have led to significant advances in biotechnology, including the production of human insulin by yeast cells, which has been happening since the early 1980s [6,7]. Genetically modified yeasts can also be used as bioremediation agents [8], increasing their importance for environmental and agricultural purposes.

If, thousands of years ago, yeasts played a role in the early development of agriculture, recently, studies have indicated that they can enhance organic food production [9]. This is due to their innate capacity to interact with plants, other microorganisms, and various environmental abiotic factors. Moreover, the literature suggests that yeasts can degrade some pesticides commonly used in traditional agricultural practices over the past few decades. With this in mind, in the following sections we address the biochemical processes involved in the ecological roles of yeasts that benefit plant development, the harmful effects of pesticides on these microorganisms, and how their cells can act as agrochemical degraders.

The literature was reviewed based on our previous studies and experiences over the past few years. The initial searches employed the following terms in the Scopus database: “yeast AND agriculture”, “yeast AND pesticide”, “yeast AND plant growth”, “yeast AND biocontrol”, “yeast AND Indole-3-acetic acid OR IAA”, and “yeast AND agriculture AND bioremediation” (no additional filters were used in these searches). References were selected for their relevance to the subject of this study. Additionally, foundational articles were sometimes used as starting points, which led to more recent articles that cited them.

2. The Contribution of Soil Yeasts to Plant Health

For hundreds of millions of years, yeasts have evolved and established their role in the ecological balance, thriving in a wide range of environments [3]. In these habitats, these microorganisms are not merely passive; rather, they actively engage in numerous biological activities and participate in a complex mix of biochemical reactions that affect the environments they colonize [10]. A summary of the ecological services that yeasts provide to plants is illustrated in Figure 1.

One of yeasts’ most challenging habitats is the soil, which hosts several microbial species that biochemically interact and alter the environment’s physical, chemical, and biological characteristics [11]. Regarding the physical changes, the presence of yeasts contributes to soil aggregate formation and maintenance, which is crucial for enhancing soil aeration, water infiltration, and root penetration [12]. Additionally, certain soil yeasts can form biofilms, stabilizing soil particles and further improving soil structure [13]. However, the chemical and biological changes exerted by yeasts in the soil are even more significant, as examined below.

The soil’s surface layers concentrate most of this system’s organic matter and biological activity [14]. Consequently, the greatest diversity of yeast species is found in this environment [15,16]. There, in their quest for survival, these microorganisms provide essential ecological services that support the growth of other living organisms, including their development [17]. In fact, yeasts can act as plant growth promoters (

Table 1. Physiological processes through which yeasts promote plant growth.

Yeast Species	Physiological Process	References
Aureobasidium pullulans, Myriangiales sp., Occultifur brasiliensis, Candida silvae, Cryptococcus podzolicus	Nitrogen and carbon availability	[18]
Pichia kudriavzevii, Issatchenkia terricola	Phosphorus availability, IAA 1 production	[19]
Cryptococcus flavus, Candida railenensis	Phosphorus availability	[20]
Meyerozyma guilliermondii, Candida zemplinina, Candida pimensis, Lachancea lanzarotensis, Rhodotorula mucilaginosa	IAA 1 production	[17]
Kazachstania rupicola, Rhodosporidium diabovatum, Saccharomyces cerevisiae	IAA 1 production	[21]
Hannaella sinensis, Cryptococcus flavus, Rhodosporidium paludigenum, Torulaspora globosa	IAA 1, NH3, and siderophore production	[22]
Papiliotrema laurentii, Wickerhamomyces anomalus	IAA 1 and NH3 production, calcium and zinc solubilization	[23]
Rhodotorula mucilaginosa	IAA 1 and siderophore production, phosphorus solubilization	[24]
Cryptococcus flavus, Hannaella coprosmaensis, Pseudozyma aphidis, Sporisorium reilianum, Ustilago esculenta	IAA 1 production	[25]
Rhodotorula mucilaginosa, Cystobasidium sloffiae	IAA 1 production	[26]
Schwanniomyces occidentalis, Cyberlindnera saturnus, Candida tropicalis	NH3 production, phosphorus and zinc solubilization	[27]
Cryptococcus sp.	Phosphorus solubilization	[28]
Aureobasidium pullulans, Candida sp., Dothideomycetes sp., Galactomyces candidum, Hanseniaspora uvarum, Meyerozyma caribbica, Barnettozyma californica, Pseudozyma aphidis	IAA 1 and NH3 production, phosphorus and zinc solubilization	[29]

¹ Indole-acetic acid.

).

Yeasts play a prominent role in nutrient cycling by releasing enzymes that catalyze the transformation of molecules, breaking them down into smaller units (monomers) that other organisms can more easily utilize. In this context, it is worth mentioning nitrogen as one of the elements made available in the environment through the action of yeasts [12]. The proteolytic enzymes secreted by yeasts increase the availability of essential elements to other microorganisms and plants. In addition to a source of nitrogen, the availability of carbon is also vital for the growth and development of other species. Enzymes such as xylanases, amylases, pectinases, and cellulases help release more assimilable carbon sources into the environment [18].

Phosphorus-based nutrients are some of the most required by plant species. Their presence in the soil directly impacts plant growth [20]. This nutrient is often found in forms that are not available to plants; however, yeasts such as Pichia kudriavzevii and Issatchenkia terricola were found to provide this essential element in forms that are better assimilated by plants, generating an increase of 80.31% and 50.90% (respectively, with P. and I. terricola) in the growth of mung bean roots [19].

An increase in phosphorus solubilization has also been observed from the activity of other yeast species, such as Cryptococcus flavus and Candida railenensis. When inoculated into the corn rhizosphere, these yeasts induced an increase in root growth of 53% and 34%, respectively. This increase in growth was linked to improved phosphorus absorption by the plants, especially when the yeasts were inoculated in consortia with mycorrhizal fungi. Consequently, a synergistic effect among these species was observed, as the enhanced development of the plant’s aerial parts (26% increase) correlated with a 20% to 29% rise in phosphorus absorption [20].

In addition to the greater availability of nutrients, yeasts also promote plant growth by other means, such as the production and release of compounds related to plant growth stimulation, especially indole-3-acetic acid (IAA). Yeasts of the species Meyerozyma guilliermondii, Candida zemplinina, Candida pimensis, Lachancea lanzarotensis, Rhodotorula mucilaginosa [17], Pichia kudriavzevii, Issatchenkia terricola [19], Kazachstania rupicola, Rhodosporidium diabovatum, and Saccharomyces cerevisiae [21] have already been reported as good IAA producers. The yeast metabolic pathways involved in producing this important plant growth promoter are summarized in Figure 2.

IAA is a phytohormone belonging to the auxin class, responsible for stimulating both apical and lateral growth in plants through cell elongation [15]. Its presence in plant roots enhances root development, increasing the area of contact with the soil. This improvement allows plants to more effectively intercept and absorb nutrients in the soil [21], thereby boosting their ability to compete with pathogenic organisms present in the environment [19].

As mentioned, soil is a habitat for several species of microorganisms, especially in its upper layers. While phytopathogenic microorganisms are commonly found in this environment [36], wild yeast strains also play a significant role by competing with these harmful organisms. They exert pressure on the survival and establishment of phytopathogens through several mechanisms [37]. These yeasts compete for physical space [38] and nutrients [19,38,39], and they can also secrete extracellular enzymes such as β-glucanases and chitinases [37,39]. These enzymes actively contribute to plant protection [19,40], as exemplified in

Table 2. Antagonistic activities exerted by yeasts.

Yeast Species	Pathogen	Yeast Antagonist Action	References
Papiliotrema laurentii	Pythium ultimum	β-1,3-glucanase production	[41]
Rhodotorula minuta, Candida azyma, Aureobasidium pullulans	Georichum citri-aurantii	Competition for nutrients, β-1,3-glucanase, chitinase, killer activity	[42]
Wickerhamomyces anomalus	Rhizoctonia solani, Curvularia lunata, Fusarium moniliforme	Production of VOCs, β-1,3-glucanase, and chitinase	[37]
Wickerhamomyces anomalus	Penicillium digitatum	β-glucanase production	[43]
Wickerhamomyces anomalus, Metschnikowia pulcherrima, Saccharomyces cerevisiae	Botrytis cinerea	VOC production	[44]
Debaryomyces hansenii and Wickerhamomyces anomalus	Monilinia fructigena, Monilinia fructicola	Hydrolytic enzymes, killer Toxins, and VOCs	[45]
Pichia galeiformis	Penicillium digitatum	Competition for space and nutrients, VOC production	[38]
Pseudozyma graminicola	Bullera hannae, Cryptococcus nemorosus, Dacrymyces stillatus, Neovossia setariae, Sporobolomyces singularis	Cellobiose lipid production	[46]
Candida diversa	Botrytis cinerea	Affect spore germination and germ tube	[47]
Candida intermedia	Botrytis cinerea	VOC production	[48]
Candida sake	Penicillium expansum	VOC production	[49]
Galactomyces candidum	Botrytis cinerea	VOC production	[50]

.

Indeed, different yeast species have demonstrated antagonistic activities against phytopathogens. For instance, the species Papiliotrema (Cryptococcus) laurentii has been reported to inhibit the pathogen Pythium ultimum in vitro and in vivo. This inhibition was attributed to its high lytic activity, which results from the production of large amounts of β-1,3-glucanase by this strain [41].

Similarly, strains of Rhodotorula minuta, Candida azyma, and Aureobasidium pullulans have shown significant antagonistic effects in vivo against Geotrichum citri-aurantii, a fungus responsible for citrus sour rot. These three yeasts employ multiple mechanisms simultaneously to exert their effects, including killer activity, competition for nutrients, and production of extracellular enzymes such as β-1,3-glucanase (from R. minuta) and chitinases (from both R. minuta and C. azyma), which can degrade the cell wall of pathogens [42].

This indicates that yeasts typically do not rely on a single mode of action to oppose their antagonists; instead, they activate several mechanisms at once, exerting deleterious effects on the pathogens [37,38]. Another yeast, Pseudozyma graminicola, has also shown antifungal potential against various pathogens by producing a glycolipid containing cellobiose in its saccharide portion, which acts as a fungicide [46].

Yeasts can also play a beneficial role more discreetly by acting as external sensors for plants and signaling the presence of pathogens. In this context, yeasts release compounds such as salicylic acid (SA), jasmonic acid (JA), and ethylene (ET). These substances prompt the plant to activate its own defense mechanisms, producing secondary metabolites that help repel or inhibit pathogen attacks (Figure 1). This prevents or reduces damage to the plant. This phenomenon is known as induced systemic resistance (ISR) [46,51].

When challenged by the bacterium Xanthomonas axonopodis, cells of Pseudozyma churashimaensis inoculated into pepper leaves (Capsicum annuum) drove a 4.5-fold increase in the expression of resistance inducers such as SA and JA. At the same time, ET production was found to be 15 times higher in the inoculated plants than in those not treated with the yeast [52]. Moreover, the presence of the yeast Meyerozyma (Pichia) guilliermondii in peach fruits has been shown to enhance the activity of enzymes such as glucanase and polyphenol oxidase. This increase also led to higher SA production, thereby activating plant defenses against pathogens like Rhizopus stolonifer, which causes soft rot, and Penicillium expansum, responsible for blue mold [53].

Finally, soil composition may also be altered by the presence of yeasts, as they can provide carbohydrates to the environment. Specifically, the yeasts Rhodotorula glutinis and Rhodotorula acheniorum have been reported to provide mannose, galactose, glucose, and xylose [54,55]. In this way, yeasts also impact the soil’s physical structure, enhancing its stability, maintaining the balance between micro- and macropores, and ensuring adequate air spaces and water storage for plants.

3. The Ecological Importance of Yeasts Beyond Soil

Above ground, yeasts can play several important roles. Among them, perhaps the most important and best known is their role in the pollination process of angiosperms. Present in floral nectaries, yeasts ferment nectar, releasing volatile organic compounds (VOCs) capable of attracting pollinating insects. This creates a beneficial triple symbiosis: (a) the insect is attracted to a food source, (b) the plant benefits from the pollination, continuing its propagation, and (c) the microorganism gains access to new habitats or colonizes the digestive tract of the insects during periods when there is no flowering [3].

In the gastrointestinal tract of insects, yeasts also play an important ecological role. Once internalized, they interact with the existing microorganisms and act as probiotics. This interaction helps these invertebrates by breaking down complex polymers into simpler monomers, making nutrients more easily absorbable. Additionally, yeasts contribute to their defense by producing antimicrobial substances and/or preventing the growth of pathogenic species in the guts [19,56,57,58].

Fruit fly larvae (Drosophila melanogaster) with their gastric system inoculated with Saccharomyces cerevisiae showed faster growth and better development, resulting in larger insects when compared to non-inoculated ones [59]. Similarly, the presence of the yeast Yarrowia lipolytica in the digestive system of beetles from the species Nicrophorus vespilloides enhanced the metabolism of proteins and lipids. This improvement was attributed to the secretion of proteases, lipases, and enzymes associated with the β-oxidation of fatty acids by the yeast cells [56].

In plants, yeasts can also develop an endophytic symbiosis, occupying the plant’s intercellular spaces. In this relationship, yeasts help the plant absorb essential nutrients such as iron, phosphorus, and zinc [60]. Additionally, yeasts enhance the plant’s resistance to pathogens by producing glycosyl hydrolases (as already mentioned) and VOCs that act antagonistically against other microorganisms [37]. As an example, in tomato plants, Fernandez-San Millan et al. [61] demonstrated that the yeast Wickerhamomyces anomalus significantly antagonized pathogenic species such as Fusarium oxysporum, which causes fusarium wilt, and Verticillium dahliae, responsible for verticillium wilt in tomatoes.

This antagonistic effect is observed not only in endophytic yeasts but also in species that inhabit floral nectaries. These species compete with pathogenic organisms for both physical space and nutrients in this microenvironment [3]. Additionally, they produce and release substances with antimicrobial properties. Notably, this action protects not only the plants but also pollinators, as it prevents the establishment of pathogens that could attack insects visiting the flowers [10].

Therefore, it is possible that these yeasts’ presence in agricultural environments can provide various ecological services, benefiting soil, plants, and the insects that pollinate them. This relationship helps maintain a balance between biodiversity and plant production. Changes in the yeast population can result in reduced pollination of plant species and negatively impact insect life [10]. At the same time, a loss of yeast biodiversity may increase the likelihood of plant and invertebrate attacks by pathogenic organisms [58].

The negative effects of pesticides on yeast cells may occur through various mechanisms. The biochemical pathways influenced by these compounds and how yeast may develop resistance are discussed in more detail in the following sections.

4. Impacts of Pesticides on Yeast Microbiota

After the Second World War, the use of synthetic molecules in agriculture increased significantly to protect and maintain crop health [62]. However, the action of these pesticides is not restricted to target organisms; they are mostly broad-spectrum products that also impact non-target organisms, thereby harming local biodiversity [63].

Repeated use of products with similar mechanisms of action leads to resistance in target organisms. As a result, these pathogens are no longer affected by the chemicals, rendering them ineffective. This also harms beneficial organisms, leaving crops vulnerable to resistant pathogens [64].

Many pesticides used in agriculture have systemic action, meaning they can penetrate the leaf tissue, passing through the plant’s vascular system. This allows them to reach areas of the plants that were not directly exposed to the pesticide, such as the floral nectary [63]. The presence of these molecules in such locations alters the biological dynamics of the yeasts present there, causing indirect problems related to pollinators’ attraction, decreased crop productivity, and reduced food availability [10].

An example of this undesirable effect occurs with fungicides, which are used extensively in conventional agriculture to reduce the population of disease-causing fungi. However, these pesticides also decrease the number of non-target organisms [65]. Many of them are beneficial, particularly during the post-harvest process. The loss of these organisms negatively impacts local biodiversity and disrupts the production chain that relies on their activities [66].

The impacts caused by these practices affect industry, especially the fermented beverage sector. It is well recognized that molecules such as penconazole, benomyl, and pyrimethanil can persist in grapes, which are the primary raw material for wine production. Once present in grape must, pyrimethanil impairs the fermentation process and alters the pace of beverage production. This molecule inhibits the growth of the wild yeast Hanseniaspora uvarum, giving space for greater growth of the yeast S. cerevisiae. This shift accelerates S. cerevisiae’s involvement in the anaerobic fermentation of the must, ultimately impacting the organoleptic characteristics of the final product [67].

Similarly, the cell growth of yeasts present in wheat grains is highly affected by the use of fungicides, which disrupts the balance among native microorganisms, such as Aureobasidium pullulans, Candida albicans, Candida sake, Debaryomyces hansenii, Candida famata, Metschnikowia (Candida) pulcherrima, and Rhodotorula glutinis, which are present on the external and internal part of the grains. This compromises bakery products’ rheological and organoleptic characteristics from wheat grains containing native yeasts [66].

Besides fungicides, other molecules widely used in the global agricultural environment also impact yeasts, whether they are at recommended concentrations or even in residues below legally permitted levels [68]. In 2022, approximately 2000 tons of herbicides were applied globally in agricultural settings. Brazil was the leading country in synthetic pesticide usage, consuming nearly 500 tons of herbicides that year [62].

Products containing 2,4-dichlorophenoxyacetic acid (2,4-D) are extremely useful in conventional agriculture as they selectively target dicotyledonous plants [69]. However, 2,4-D also poses harmful effects beyond the Kingdom Plantae. It readily interacts with cell membranes, allowing it to penetrate yeast cells and render them nonviable [68].

Even at doses recommended for agricultural use, exposure to 2,4-D can acidify the intracellular pH of yeast cells. This acidification also triggers oxidative stress in the cells, which inhibits cell growth and increases their latency period [68,70]. The oxidative stress intensity varies according to the amount of the active ingredient (AI) administered. Yeast cells exposed to increasing doses of AI showed the formation of hydroxyl radicals. During the adaptation period, S. cerevisiae exposed to the herbicide showed an increase in the enzymatic activity of cytosolic catalase (Cttp1p), CuZn-superoxide (Sod1p), glutathione-dithiols, and glutathione reductoxins (Grx1p and Grx2p), evidencing an increase in the antioxidant defense mechanisms in the yeast cells [71].

Glyphosate is another herbicide commonly used in conventional agriculture, and it has a strong inhibitory effect on yeast cell growth [72]. This is because it inhibits the enzyme 5-enolpyruvylshikimate-3-phosphate synthase (EPSP synthase), thus disrupting the shikimate pathway [69]. Consequently, shikimate accumulates, preventing the synthesis of the aromatic amino acids tryptophan, phenylalanine, and tyrosine, which are essential precursors for various important compounds in yeast cells [73].

Confronted with the challenges posed by human activities in rural environments, yeasts adapt to coexist with stressors, ultimately developing resistance to certain active ingredients [71]. The repeated and indiscriminate use of these products in agriculture leads to an artificial selection of resistant organisms [73]. This was demonstrated by Barney et al. [72], who compared the effects of glyphosate on yeast strains isolated from agricultural environments both before and after the herbicide’s commercial launch. Strains that had never been exposed to glyphosate demonstrated greater susceptibility to the product, while those previously exposed exhibited increased resistance.

In addition to the active ingredients, commercial products often contain other substances known as “inerts”, which enhance the effectiveness of the AI. However, these inerts are also responsible for negative effects on yeast growth [74]. The deleterious impact of inerts was demonstrated in an environment where yeasts were not dependent on the shikimate pathway for cellular respiration. However, in this case, the commercial product still inhibited yeast growth to the same degree [75].

The negative impacts of pesticides on yeast cells and the subsequent implications on related economic activities are summarized in Figure 3. It is worth noting, though, that these microorganisms can remarkably adapt and mitigate environmental damage. In the following section, we explore the potential of yeasts in the bioremediation of contaminated soils.

5. Yeasts as Potential Bioremediators

As previously mentioned, yeasts not only play several roles in industry but also serve several essential ecological functions. From this point on, we also emphasize the potential of these microorganisms in bioremediation, an important process for promoting sustainable agriculture [76]. Bioremediation involves removing and degrading chemical contaminants with variable chemical structures, which requires specific biochemical processes for effective degradation [77].

The chemical structures of the compounds discussed below are depicted in Figure 4. Beginning with 2,4-D, it is important to recognize that this herbicide’s continual application poses significant toxicological challenges to the environment and contributes to weed resistance. A study revealed that, in addition to resistant plants, yeasts can also adapt to 2,4-D by developing a plasma membrane that is unaffected by the herbicide. The cells of these yeasts can grow in the presence of different concentrations of the herbicide. These adapted yeasts display an increased proportion of saturated and monounsaturated fatty acids in their membranes. They achieve this by downregulating the gene that encodes a fatty acid desaturase. As a result, the herbicide’s entry into the cells is impeded, enabling the proper maintenance of cellular functions [68,78]. Additionally, increased expression of other genes associated with cell integrity has also been identified as a tolerance mechanism to 2,4-D in yeast. Specifically, the upregulation of genes such as MTL1, ROM1, and MKK2, which are involved in stress signaling in the cell wall, and genes related to chitin synthesis (a component of the cell wall), such as SHC1 and ECM38, supports the importance of preserving and restoring cell wall integrity for tolerating 2,4-D [79].

Different metabolic pathways degrade 2,4-D. Most bacteria start by cleaving the side chain, whereas fungi typically use hydroxylation of the aromatic ring. Monooxygenase enzymes, specifically hydroxylases, introduce hydroxyl groups (–OH) into the aromatic ring, forming metabolites such as 2,4-dichloro-5-hydroxyphenoxyacetic acid and 2,5-dichloro-4-hydroxyphenoxyacetic acid. Furthermore, the hydroxylation of 2-chlorophenoxyacetic acid (2-CPA) generates 2-chloro-4-hydroxyphenoxyacetic and 2-hydroxyphenoxyacetic acids, indicating that dichlorination occurs along with replacement of chlorine by hydroxyl groups. Understanding these enzymatic processes and their metabolites is crucial for optimizing the bioremediation of herbicide-contaminated environments [51,81].

As the most widely used herbicide in conventional agriculture, glyphosate merits careful consideration (refer to its structure in Figure 4). As previously mentioned, glyphosate inhibits the EPSP synthase enzyme, which disrupts the synthesis of amino acids that are essential precursors for vital compounds such as alkaloids, flavonoids, and benzoic acids. In the soil, microorganisms can degrade glyphosate through two primary pathways. The first pathway involves the conversion of glyphosate into sarcosine, facilitated by the bacteria Agrobacterium radiobacter and Enterobacter aerogenes, using the enzyme C-P lyase. Then, sarcosine can be metabolized further by other microorganisms, including yeasts. The second most common route transforms glyphosate into amino-methyl phosphonic acid (AMPA) [82]. In this case, though, glyoxylate is also produced, making this route the preferred one within the Kingdom Fungi [83].

In addition to herbicides, studies on the biodegradation of other agrochemicals, such as insecticides, are also relevant. One noteworthy example is carbofuran (Figure 4b), a broad-spectrum agrochemical that falls under the carbamate class. It serves as an acaricide, insecticide, and nematicide. Commercially introduced in 1967, its specific use increased rapidly in the following years. The half-life of carbofuran in the soil varies between thirty and one hundred and twenty days, depending on the soil type. In sandy soils, the half-life is approximately thirty days, while in clayey soils it is around forty days. In muddy soils, the half-life extends to about eighty days [84].

These two pesticides (glyphosate and carbofuran) were tested for degradation using yeasts. Candida tropicalis and Trichosporon cutaneum exhibited good growth in media containing glyphosate as the sole carbon source. Candida tropicalis degraded 76% of the initial glyphosate in 192 h, demonstrating notable biodegradation efficiency. Both yeasts also grew normally in rich medium (YEPD) with carbofuran, but the growth of T. cutaneum slowed significantly in synthetic minimal medium (YNB without amino acids) containing carbofuran above 0.3 g/L. Nevertheless, this yeast demonstrated almost complete biodegradation of carbofuran in 192 h, with the detection of intermediate metabolites such as carbofuran-7-phenol and pyruvate during cultivation [77].

Another widely used herbicide is pendimethalin (Figure 4d). Its unique combination of atoms makes it easily adsorbed by the soil but very difficult to desorb. Fortunately, certain fungi can oxidize its amine groups and benzene ring through enzymes such as pendimethalin monooxygenase and pendimethalin peroxidase. These oxidative processes render the molecule nontoxic and enhance its degradation by the soil microbial community. Moreover, microbial esterases, including pendimethalin hydrolase, also play a role in its breakdown [85]. Notably, the yeast Clavispora lusitaniae has shown significant efficacy in degrading pendimethalin. Han et al. [86] demonstrated that the ability of this yeast’s degradation efficiency is inversely related to the pH of the growth medium: as the pH decreases, its ability to degrade pendimethalin improves.

Yeast has also proven effective in degrading the herbicide atrazine (Figure 4e), a member of the triazine class. A Pichia kudriavzevii strain was shown to degrade this herbicide in both liquid media and soil. The study demonstrated that the strain Atz-EN-01 could completely degrade atrazine within 7 days, exhibiting a degradation rate of 31% per day, following the first-order kinetic model. The half-life of the degradation process was 2.2 days under optimum conditions, which included a pH of 7, a temperature of 30 °C, an inoculum size of 3% (v/v), and agitation of 120 rpm. The identified degradation products were hydroxyatrazine, N-isopropylammelide, and cyanic acid, with the enzyme atrazine chlorohydrolase exhibiting maximum activity during the degradation process [87].

It is interesting to note that some yeast species, unlike most living beings, can switch between respiration and fermentation, regardless of the presence of oxygen. This switch depends on the availability of a carbon source and/or the need imposed by the environment. As a result, yeasts are less susceptible to agrochemicals of the dinitrophenol class, which are recognized as uncoupling agents of oxidative phosphorylation, thus inhibiting the generation of ATP after the respiratory chain. Therefore, the resistance of yeasts to these toxic conditions represents a significant advantage in the biodegradation process of dinitrophenols, as detailed in the study by Marius et al. [88]. These researchers analyzed the use of yeasts for biodegradation, specifically in solutions containing dinitrophenol-based agrochemicals. The results indicated a decrease in the toxicity of the remaining solutions after treatment with yeasts, which were subsequently used in wheat seed germination experiments.

When exploring the potential of yeasts as bioremediators, issues surrounding the source of microbial cells and the costs associated with producing enough cells for large-scale contamination treatment may arise. However, an alternative to overcome this potential problem may be found in the study by Szpyrka et al. [2]. These authors tested three commercial yeast strains (of the species Saccharomyces cerevisiae, Yarrowia lipolytica, and Debaryomyces hansenii) against four herbicides and demonstrated that they can fulfill additional roles beyond their industrial applications. In their findings, fluazifop-P-butyl was the most effectively degraded herbicide, with up to 71.2% degradation observed after four days. This was followed by metribuzin (20%), propyzamide (13.4%), and pendimethalin (5.3%). Moreover, when shell pea (Pisum sativum L.) seeds were sown in soils treated with yeasts, there was a notable enhancement in plant development: growth increased by 22% and seed germination capacity improved by 30%. Therefore, these findings suggest that yeast cell biomasses could serve an additional role after their industrial use, degrading harmful environmental compounds and stimulating plant growth and germination.

A summary of the degradation processes discussed above is presented in

Table 3. Examples of pesticide degradation processes performed by yeasts.

Agrochemical	Yeast	Degradation	Action Mechanism	Degradation Conditions	Resulting Metabolites	References
Glyphosate	Candida tropicalis and Trichosporon cutaneum	76% (C. tropicalis) and 58% (T. cutaneum) in 192 h	Conversion of glyphosate into methylglycine and glycine	Use of glyphosate as a carbon source	Methylglycine, glycine	[77]
Carbofuran	C. tropicalis and T. cutaneum	Almost 100% (T. cutaneum) and 23.4% (C. tropicalis) in 192 h	Biotransformation of carbofuran to carbofuran-7-phenol and pyruvate	Normal growth on rich medium; significant reduction on minimal medium	Carbofuran-7-phenol pyruvic acid	[77]
Pendimethalin	Clavispora lusitaniae	74% in 8 days	Oxidation of amine groups	Optimal pH between 4.5 and 5, with maximum degradation at 30 °C	1,2-dimethyl-3,5-dinitro-4-N(buta-1,3-dien 2-yl)-dinitrobenzenamine-N-oxide and 1,2-dimethyl-3,5-dinitro-4-N(prop-1-en-2-yl)-dinitrobenzenamine-N oxide	[86]
Atrazine	Pichia kudriavzevii	100% in 7 days	Dechlorination and hydrolysis	pH 7.0, temperature 30 °C, inoculum size 3% (v/v) and shaking at 120 rpm	hydroxyatrazine, N-isopropylamylidene, and cyanuric acid	[87]
Dinitrophenol (DNOC, DNG, DNPED, Dinocap)	Saccharomyces cerevisiae	In 1 week: partial degradation for DNOC and Dinocap; DNPED completely degraded. Pesticide concentration: 10−3 M.	Not specified	Yeast suspensions at 5 g/L for 1 week in a batch system	Not specified	[88]
Fluazifop-P-butyl	Saccharomyces cerevisiae, Yarrowia lipolytica and Debaryomyces hansenii	Up to 71.2% in 7 days	Not specified	Horticultural soil, temperature at 21 °C, and humidity between 70 and 71%.	Not specified	[2]

. In light of this information, it is reasonable to conclude that the scientific community has accumulated sufficient knowledge to implement the use of yeasts as effective pesticide degradation tools. However, successful bioremediation efforts with yeasts extend beyond the use of wild yeasts. The following section highlights other significant advancements achieved with genetically modified strains.

6. Engineering Yeasts for Pesticide Degradation

The first eukaryote to have its genome sequenced was a yeast—the strain S. cerevisiae S288c. This demonstrates the scientific community’s interest in these fast-growing microorganisms, which can be cultivated in simple and inexpensive culture media. In fact, yeasts have been successfully used for decades in many molecular studies and as biofactories generated from gene editing techniques [5].

Therefore, using genetic engineering tools, yeasts can be modified to perform numerous functions, such as removing toxic waste. In this context, they can act as biocatalysts (hosting different degradation enzymes within their cells) or as biosensors to detect the presence of toxic waste in the environment. Although the successful application of yeast genetic engineering has a history spanning over 40 years, the recent advent of CRISPR (clustered regularly interspaced short palindromic repeats) has propelled the functional capabilities of yeasts to new heights, further increasing their potential as bioremediators in areas affected by pesticide contamination [89].

Interestingly, the CRISPR-Cas technique is derived from the adaptive immune system of prokaryotes, which consists of a set of clustered regularly interspaced short palindromic repeats (CRISPR) and associated proteins (Cas). In bacteria, transcription of the CRISPR locus generates CRISPR RNA (crRNA), which forms a complex with the Cas nuclease. This complex recognizes specific DNA sequences through complementary base pairing, enabling Cas-mediated cleavage of exogenous DNA, such as that from invading bacteriophages [90]. In adapting the CRISPR-Cas system for genome editing, a single guide RNA (sgRNA) can be designed to be complementary to a target DNA sequence that is to be modified. Within the cellular environment, transcription of sgRNA, combined with the expression of Cas nuclease, allows the formation of a complex that precisely directs the nuclease to the target DNA, inducing a double-strand break at the designated site. After this cleavage, natural DNA repair mechanisms allow the insertion or deletion of genetic material, resulting in the desired genomic alteration [91]. The high accuracy of the CRISPR-Cas system in target recognition and cleavage has made it a robust and versatile tool for gene editing in several fields, including agriculture [92,93].

One notable example of yeast genetic engineering for bioremediation purposes involves the CYP72A18 gene, which is present in rice and encodes an enzyme from the cytochrome P450 superfamily. This enzyme catalyzes the (ω-1)-hydroxylation of the herbicide pelargonic acid, reducing its toxicity in the environment. Through genetic engineering, this gene was heterologously expressed in yeast cells, allowing them to degrade this pesticide [94]. Additionally, even human isoforms of P450 have been tested in yeast with the aim of degrading agrochemicals. In one study, the CYP 1A1 and CYP 1A2 isoforms demonstrated significant effectiveness against the herbicides chlortoluron and atrazine. These enzymes were evaluated both individually and fused to the NADPH–cytochrome P450 oxidoreductase of the transformed yeast strain. Remarkably, this fusion increased enzymatic activity [95].

Other genes that encode enzymes related to cytochrome P450 have also been expressed in yeast to induce herbicide degradation. Markedly, the monooxygenase CYP71A12 from Arabidopsis thaliana has demonstrated potential in metabolizing the herbicide pyrazoxyfen when expressed in yeast. Hayashi et al. [96] reported that this enzyme catalyzes the transformation of this agrochemical into less toxic metabolites that are more readily degradable by other microorganisms in the environment. This process involves N-demethylation reactions on the pyrazole ring and hydroxylation on the dichlorobenzene ring of pyrazoxyfen. Specifically, N-demethylation removes a methyl group (CH₃) from the pyrazole ring, while hydroxylation adds a hydroxyl group (OH) to the dichlorobenzene ring.

As observed in the previous cases, it is noteworthy that enzymes from agriculturally significant plants can be expressed in yeast to alleviate the harmful effects of pesticides on the environment. For glyphosate, for example, it was found that the overexpression of two glutathione-S-transferases from a tea plant (Camellia sinensis) in S. cerevisiae allowed the cells to grow efficiently even at a concentration of 1 g/L of the herbicide [97]. Given the advantages of using yeast as biofactories (as pointed out before), the heterologous production of these enzymes within these microbial cells can substantially increase their use as catalysts for the degradation of agrochemicals.

In the context of engineered yeasts for bioremediation, a successful approach involves the expression of degradation enzymes on the cell surfaces of these microorganisms (Figure 5). This strategy allows yeasts to degrade compounds without needing to internalize them, which is particularly effective for high-molecular-weight substances. The so-called whole-cell yeast biocatalysts also prove efficient by eliminating the transportation barrier across the plasma membrane and dismissing any enzyme preparation and purification steps, ultimately reducing the cost. In addition, the cell surface display strategy enhances the potential for biocatalyst recycling in various processes [89,98,99].

The cell-surface strategy has been notedly studied for the degradation of organophosphorus pesticides. Takayama et al. [100] succeeded in expressing up to 14 × 10⁴ molecules of an organophosphorus hydrolase (OPH) from Flavobacterium sp. on the cell surface of S. cerevisiae. To anchor this enzyme to the yeast surface, the authors fused an α-agglutinin with a glycosylphosphatidylinositol (GPI) signal sequence to the OPH’s C-terminal region, enabling the cells to efficiently hydrolyze paraoxon. The same research group has also expressed this OPH in S. cerevisiae through the Flo1p anchor system. In this case, the authors attached the anchor protein to OPH’s N-terminal region and achieved eight times higher OPH activity than the GPI approach [101]. In any case, though, they found significantly higher activities with these yeast-surface display methods than with a similar strategy that employed bacterial cells instead [100,101]. Indeed, as eukaryotes, yeasts harbor more sophisticated pathways for secreting or displaying proteins on their surfaces than bacteria (which are prokaryotes) [99]. Figure 5 depicts how these anchor systems can work in yeasts.

7. Yeasts for Sustainable Agriculture: Challenges and Avenues

Yeasts have been employed in the production of food and beverages since the Neolithic Revolution, leading to their selection and adaptation within agricultural environments over millennia [5]. Furthermore, as discussed in this review, yeasts can benefit the health and development of plants in several ways, either by protecting them against pathogens or stimulating their growth. Therefore, they may be favored over filamentous fungi or bacteria in organic or agroecological agriculture practices. Additionally, yeasts possess the potential for bioremediation in areas contaminated by conventional pesticides. In this case, they would first help to “clean” the environment and subsequently facilitate the cultivation of new crops from an organic perspective.

Fortunately, this premise has gained considerable traction in recent years. Our bibliometric analysis in the Scopus database revealed a significant increase in studies focusing on the use of yeasts in agriculture, particularly regarding their role in bioremediation, over the past two decades (Figure 6). This search used the terms “yeast AND agriculture AND bioremediation” to identify articles published between 2004 and 2024.

However, some questions are yet to be answered. The literature, for example, lacks studies that have tested yeasts in large-scale agricultural experiments—most research has been carried out in greenhouses or laboratory settings. Additionally, only a few studies have examined how yeast microbiota change over extended periods under the influence of pesticide use. In this regard, it would be valuable to investigate how different seasons or climate zones might affect yeast adaptation. The same holds true for soil types: it is still unclear how (or if) soil features contribute to developing tolerance in yeasts toward agrochemicals. Finally, science would benefit from more studies on yeasts isolated from environments in the vicinity of farms that use agrochemicals. In these areas, the presence of pesticides, although in lower concentrations, could drive an artificial selection of microorganisms.

In addition to the need for more studies, it is important to consider the logistical challenges of effectively incorporating yeasts into agricultural systems, especially for large-scale applications. From this perspective, “on-farm” production (producing inputs for personal use on the agricultural property) could be an advantageous solution. However, using yeasts as biocontrol agents, plant growth promoters, or bioremediators requires careful management of environmental factors (such as temperature, pH, and oxygen levels) to ensure these organisms maintain high metabolic activity and efficiency in degrading contaminants. In addition, obtaining and multiplying yeast cultures implies significant costs, especially when using genetically modified strains, which require rigorous safety assessments to avoid negative impacts on the agricultural ecosystem [102,103].

8. Conclusions

The trend observed in Figure 6 underscores the growing concern for sustainability and the pursuit of alternatives that mitigate the negative environmental impacts of conventional agriculture. In this context, yeasts hold significant importance, owing to both the inherent potential of various species in nature and the biotechnological innovations surrounding their genetic engineering. This review aimed to systematically present these potentials to spark interest within the scientific community for developing practical processes based on the ideas discussed. It is imperative to acknowledge the harm that agrochemical usage inflicts on the environmental microbiota and its broader implications for wildlife. Additionally, the microorganisms we aim to preserve may provide solutions to the challenges created by human activities. In this two-way street, further studies on yeast physiological processes are highly desired.