Diversity and functions of fungal VOCs with special reference to the multiple bioactivities of the mushroom alcohol

ABSTRACT

Different species of fungi usually share many common pathways but they also have some unique metabolic pathways (e.g. those for specialised metabolites). It is not clear how gene expression patterns significantly contribute to the creation of diverse volatile compounds. Based on the research of most VOCs, the functions of different fungal volatile compounds are mainly as follows: inhibitory or synergistic effects on other microorganisms, promoting growth in plants or inducing a defensive response in crops, and participating in the material cycle or affecting the interactions between organisms in the ecosystem. Approximately three hundred VOCs have been identified from fungi. According to their chemical properties, the major categories of fungal VOCs are terpenoids, aromatic compounds, alcohols, alkanes, esters, aldehydes, ketones, and heterocyclic compounds. The eight-carbon alcohol (1-octen-3-ol) is one of the most characteristic fungal VOC. This abundantly produced VOC results from the breakdown of linoleic acid and causes a distinctive mushroom-like odour. Consequently, its presence has been utilised as a signal of fungal growth. It is also produced by certain plants and functions as a semiochemical for numerous arthropods. The use of Drosophila melanogaster (fruit flies) as a model for testing the toxicity of fungal VOCs showed that some VOCs delayed metamorphosis and/or caused fly death at certain concentrations. When Drosophila was cultivated in an atmosphere shared with VOC mixtures released from growing cultures of several medically important fungi, including Aspergillus fumigatus, toxicity was observed. Additionally, we propose that components of the genetic immune system of D. melanogaster are engaged in the toxicity of fungal VOCs mainly via the elicitation of the Toll pathway. The presence of 1-octen-3-ol, for example, was associated with higher levels of toxicity in the fruit fly bioassay. In this review, we summarise (1) the diversity and functions of different fungal VOCs, (2) the biosynthesis and bioactive characteristics of 1-octen-3-ol, and (3) the use of D. melanogaster as a genetic model to assess the health impacts of fungal VOCs.

GRAPHICAL ABSTRACT

1. Introduction

In recent years, fungal VOCs have received increasing attention because it has become apparent that they are bioactive and can play the role of chemical molecular signals in many environments (Morath et al. 2012; Hung et al. 2015; Pennerman et al. 2016, 2019; Inamdar et al. 2020; Lee et al. 2024). Moreover, they may cause health problems in humans when encountered at high concentrations in water-damaged (and subsequently mould-contaminated) schools, workplaces, and homes (Takigawa et al. 2012; Mølhave 2018). Aspergillus fumigatus is also one of the causal agents that resulted in hypersensitivity pneumonitis and allergy in humans (Vitte et al. 2022). In addition to Aspergillus, airborne fungi include species of Penicillium, Acremonium, Paecilomyces, Mucor, and Cladosporium and they can cause asthma and other respiratory symptoms (Kumar et al. 2021). Here, we introduce the research history, types, and functions of fungal VOCs with a special focus on the mushroom alcohol (1-octen-3-ol). A recent article on the application of bioactive compounds from the mushroom family was reported by Rani and his colleagues (Rani et al. 2023).

VOCs are low molecular weight organic carbon substances with low water solubility and high vapour pressure (≥0.01 kPa at 20 °C). They readily vaporise at room temperature, escaping from the liquid phase to gases and entering the atmosphere (Herrmann 2011). This ability to enter the atmosphere means that VOCs can mediate inter-organismal communications in terrestrial environments (Peñuelas et al. 2014; Plaszkó et al. 2020), and there is extensive literature on VOCs serving as semiochemicals in microbe-arthropod interactions (Davis et al. 2013). Most microbial VOCs have characteristic smells (Schulz and Dickschat 2007). Some have agreeable associations for humans as components of fermented beverages and foodstuffs (Gong et al. 2024). Conversely, others create unpleasant associations, such as decayed foods, dirty socks, wastewater collection systems, and flooded buildings. Over three hundred various VOCs have been detected from the chemical profiles of microscopic or macroscopic fungi. Any given species of fungus may instantaneously release dozens of different volatiles as combinations of alcohols, ketones, esters, small alkenes, thiols, monoterpenes, cyathane diterpenes, and sesquiterpenes (Korpi et al. 2009; Liu et al. 2024). The total profile of volatiles produced by a fungus at a specific sampling time is defined as its “volatilome”, and it is general for the same VOC to be formed by dozens if not hundreds (Martinez and Bennett 2021; Minerdi et al. 2021; Ul Hassan et al. 2023). Eight-carbon volatiles are the most characteristic of the fungal VOCs and give off odours variously described as fatty, waxy, musty, or mushroom-like. The book titled “Nose Dive: A Field Guild to the World’s Smells” (McGee 2020) gives tables in which the specific odours associated with different fungal species are matched with the relevant molecules responsible for eliciting those odours. For example, geosmin, which is a major odour component in soils, is produced by lots of species of Streptomyces bacteria and cyanobacteria as well as fungi (Schulz and Dickschat 2007; Elmassry et al. 2020). An informative compendium of fungal VOC compositions and species of origin, based on articles published between 1936 and 2005, was published in French (Chiron and Michelot 2005). A database of thousands of bacterial and fungal VOCs is accessible online (Lemfack et al. 2018). An updated [third] version contains the effects caused by individual mVOC from different organisms (https://bioinformatics.charite.de/mvoc/index.php?site=home).

2. Diversity and function of fungal VOCs

The chemical compositions of VOCs produced by different fungi are diverse. The Trichoderma species produce VOCs which are associated with antifungal and promoting plant growth (Alfiky and Weisskopf 2021). Trichoderma itself also has been developed as a mycoparasite to control pests (Poveda 2021). Ascomycetes produce metabolites such as volatile hydrocarbons, alcohols, esters, aldehydes, ketones, and acids. Therefore, fungal volatiles are constituted of various components with certain concentrations that are released as products of metabolism under different growth conditions. VOC production is highly affected by a diversity of ecological factors such as temperature, pH, substrate, and oxygen. For different alcohol-based compounds, ketone-based compounds, ester-based compounds, aldehyde-based compounds, and hydrocarbon-based compounds, see Naik et al. (2024). Matsutake can produce unique volatile flavour components such as methyl cinnamate, 1-octen-3-one, 1-octen-3-ol, valeraldehyde, and decanal, while Agaricus blazei can produce benzaldehyde, cocoaldehyde, and other unique ingredients (Li et al. 2016). Truffles, as a delectable food source, emit a variety of volatile compounds, such as dimethyl sulphide, dimethyl disulphide, 1-octen-3-ol, and 2-methyl-1-propanolm, which disperse in the soil and intermediate the communications with microbes and plant roots. In nature, truffles produce volatiles to attract animal vectors to spread their spores (Allen and Bennett 2021). Practical aspects correlated to the collection of VOCs and their environmental-friendly application in agronomy were reviewed by Razo-Belman and his colleagues (Razo-Belman and Ozuna 2023). Table 1 summarises the major functions of principal VOCs.

Table 1.

The category and function of principal fungal VOCs.

Categories	Representative examples	Fungal species	Functions	References
Terpenoids	Hemiterpenes (5 carbons), monoterpenes (10 carbons), sesquiterpenes (15 carbons), etc.	Cyathus species, Ophiobolus heterostrophus, Ophiobolus miyabeanus, Aspergillus ustus, Aspergillus fumigatus, Fusidium coccineum, Pisolithus microcarpus	May show significant anti-inflammatory and anti-microbial effects, potential functions in treating skin pigmentation disorders and cancers associated with melanogenesis dysfunctions	Horváth et al. (2011); Plett et al. (2024); Trepa et al. (2024)
Alcohols	1-octen-3-ol	Penicillium paneum, P. chrysogenum, Aspergillus niger, Trichoderma species, Agaricus bisporus	Semiochemical; earthy, “mushroomy” odour, self-inhibitor, inhibition of the formation of fungal colony and growth of Aspergillus and Penicillium species; inducing conidiation of Trichoderma species; inhibiting seed germination and plant growth of Arabidopsis plants; significantly delayed the metamorphosis and toxicity of fruit flies	Chitarra et al. (2004, 2005); Nemcovic et al. (2008); Yin et al. (2015); Lee et al. (2016); Zhao et al. (2017); Pennerman et al. (2022); Rani et al. (2023)
	(Z)-3-hexen-1-ol	Trichoderma harzianum	Produced by Trichoderma harzianum, appealing to the aphid predators and decreasing the population of insect pests	Contreras-Cornejo et al. (2021)
	2-methyl-1-propanol, 3-methyl-1-butanol	Aspergillus niger, Fusarium proliferatum, Penicillium pinophilum, Mucor racemosus, Trichoderma paradoxa	Mild liquor odour, considerably caused the poisonousness in fruit flies; biocontrol of black rot in snake fruit	Zhao et al. (2017); Napitupulu et al. (2024)
	Hexan-1-ol	Penicillium commune, Paecilomyces variotü, Neofabraea vagabunda	Reducing the growth of pathogens at higher concentrations	Yin et al. (2015); Neri et al. (2019)
Acids	Isobutyric acid	Muscodor albus	Rancid cheese-like odour, antifungal activity	Braun et al. (2012); Li et al. (2024)
Esters	Isoamyl acetate	Candida maltose	Banana odour, inhibitory compounds	Ando et al. (2012); Manathunga et al. (2024)
Aldehydes	Benzyl aldehyde	Polyporus tuberaster, Agaricus bisporus	Almond odour, antimicrobial activity	Kawabe and Morita (1994); Xie et al. (2024)
Ketones	6-pentyl-a-pyrone	Trichoderma species	Coconut odour, control of plant pathogens	Mendoza-Mendoza et al. (2024)
	2-heptanone	Penicillium roqueforti	Cheese odour, antifungal activity	Gehrig and Knight (1961); Wu et al. (2019)
Heterocyclic compounds	β-caryophyllene	Cytospora species, Fusarium solani	Woody-spicy odour, promoting the growth of plants	Li et al. (2017); Ana et al. (2020)
	1,8-cineole	Hypoxylon species	Camphor-like odour, antifungal activity	Shaw et al. (2015); Yelboğa and Karakuş (2023)

3. Production of 1-octen-3-ol

A meta-analysis of known biogenic VOCs from published databases showed that only certain VOCs are largely characteristics of fungi. These include 1-octen-3-ol, 3-octanone, and 2-pentylfuran, all of which are degradation products of linoleic acid. 1-octen-3-ol is a particularly typical VOC generated by a wide scope of both macroscopic and microscopic fungi and is nearly ubiquitous in both mushrooms and moulds (Combet et al. 2006; Elmassry et al. 2020). It is also called “mushroom alcohol” or “matsutake alcohol”, and it is responsible for much of the specific odour associated with fungi (Dijkstra and Wikén 1976; Tressl et al. 1982). 1-octen-3-ol (CAS Registry Number: 3391-86-4) boils at 180 °C at 101.3 kPa, a vapour pressure of 71 Pa at 25 °C, and an octanol: water partition coefficient (log_Kow) of 2.60. It has a representative fungal order (Pyysalo 1976) and has been recommended as a marker of fungal growth in the indoor environment (Fischer et al. 1999). From an industrial perspective, 1-octen-3-ol is a principal natural flavouring compound and has the capacity as a fungal growth regulator (Mau et al. 1992a, 1992b). It is one of the main fungal VOCs emitted by moulds usually found in water-damaged construction (Kaminski et al. 1974; Moularat et al. 2008). Because this molecule includes a chiral carbon, it can be existent as two optical enantiomers: (R)-(-)-1-octen-3-ol and (S)-(+)-1-octen-3-ol. (R)-(-)-1-octen-3-ol displays the classic aroma of fresh mushrooms, while (S)-(+)-1-octen-3-ol is often depicted as mouldy, grassy, or fusty (Combet et al. 2006). Both compounds are derivatives of the enzymatic breakdown of linoleic acid by enzymes produced from several fungal species (Wurzenberger and Grosch 1984). The reaction is involved by a lipoxygenase and a hydroperoxide lyase, producing 1-octen-3-ol and 10-oxo-trans-8-decenoic acid (ODA). In the progressive reaction, the first step is the combination of molecular oxygen into the pentadienyl moiety of the linoleic acid, giving off the intermediate 10-hydroperoxy-trans-8-cis-12-octadecadienoic acid (10-HPOD), followed by the cleavage of the 10-HPOD producing 1-octen-3-ol and ODA (Wurzenberger and Grosch 1984). A crude homogenate of Agaricus bisporus can be utilised to synthesise 1-octen-3-ol with 10-hydroperoxide as an intermediate (Matsui et al. 2003; Morawicki and Beelman 2008). The lipoxygenase – hydroperoxide lyase enzymatic pathway is activated when mushroom tissue is wounded (Yin et al. 2019; Tao et al. 2024). As a result, it is hypothesised that this reaction is the fraction of a protection mechanism in fungi. This hypothesis is reinforced by the point that 1-octen-3-ol and ODA both have antimicrobic properties (Okull et al. 2003). A flow chart depicting the biosynthetic pathway of 1-octen-3-ol is shown in Figure 1.

Figure 1.

A flow chart depicted the biosynthetic pathway of 1-octen-3-ol. The red colour unit denoted the active group.

Several breakdown products of linoleic acid hinder the filamentous growth of Penicillium expansum at concentrations of 1.25 mmol/L or higher (Okull et al. 2003). The compounds are often described as “auto-inhibitors” of fungal germination because they are inclined to boost conidiation in established colonies but reversibly restrain spore germination. At certain concentrations, 1-octen-3-ol is associated with the “overcrowding consequence”, which precludes the germination of spores at high concentrations (Barrios-González et al. 1989; Chitarra et al. 2004, 2005; Miyamoto et al. 2014). In some Penicillium strains, great concentrations of R-1-octen-3-ol and S-1-octen-3-ol decrease both germination and growth of fungi (Yin et al. 2019). However, naturally, these inhibitory concentrations are rarely encountered. When tested in Aspergillus flavus, more than 100-fold more 1-octen-3-ol was required to hinder germination than is present in dense spore suspensions. Therefore, Miyamoto and co-workers concluded that it was not the chief molecule that is accountable for the experimental inhibition (Miyamoto et al. 2014).

Chitarra et al. (2005) studied 1-octen-3-ol as a volatile self-inhibitor in Penicillium paneum after veridiction that dense suspensions of conidia indicated poor germination. Self-inhibitors can limit spore germination reversibly and influence other fungal processes. In an inhibitory assay, adding 4 mmol/L 1-octen-3-ol to the media contributed a germination frequency of 2% after 7 h, while 83% of the conidia were germinated in the control. VOCs produced at high concentrations also deterred the growth of other fungal species belonging to a diversity of genera, revealing a broad range of efficacy. It was further concluded that 1-octen-3-ol has slight effects on the plasma membrane, but delays the essential metabolic processes, such as enlarging and germination of the conidia, in a reversible manner (Chitarra et al. 2004, 2005). Some VOCs generated by Agaricus bisporis restrained the primordium formation and 1-octen-3-ol had the highest effect (Noble et al. 2009). In a feasible application, 1-octen-3-ol was also used in white button mushrooms to decrease dry bubble disease (Berendsen et al. 2013). They found that low concentrations of 1-octen-3-ol could prevent the germination of the causal organism, Lecanicillium fungicola, and at greater concentrations could successfully control the malady. It also impedes the mycelial growth of Pseudogymnoascus destructans, which causes white-nose syndrome in bats (Padhi et al. 2017). While it was indicated to restrain the mycelial growth in Penicillium expansum (Okull et al. 2003) and Penicillium chrysogenum (Yin et al. 2019), it also raises patulin production (Pennerman et al. 2019). Another study described that 1-octen-3-ol, 3-octanol, and 3-octanone could provoke conidiation in dark-grown cultures of some Trichoderma species, but when vapours of these compounds were assayed individually ranging from 0.1 µmol/L to 1,000 µmol/L, researchers found that 1-octen-3-ol at higher concentrations (500 µmol/L or great) significantly hindered both conidiation and growth (Nemcovic et al. 2008). 1-octen-3-ol has been proven to augment α-amylase excretion in Aspergillus flavus that was associated with dose-dependent changes in growth, conidiation, and sclerotium production in fungi (Singh et al. 2020). It should be noticed that Aspergillus flavus has the capability to naturally produce its own 1-octen-3-ol when grown on diverse substrates (Moore and Lloyd 2023).

4. Representative examples of diverse biological activities associated with 1-octen-3-ol

1-octen-3-ol is also marketed as an active ingredient of certain commercial pesticides because it appeals to biting insects for instance mosquitoes. The element itself does not kill insects but is exploited as bait (Cilek et al. 2011). The odorant receptor (AaegOR8) found on the maxillary palps was investigated in a heterologic system and confirmed to be selectively susceptible to (R)-(-)-1-octen-3-ol, one of the two enantiomeric forms. Reduced responses were promoted by the (S)-(+)-1-octen-3-ol and numerous structural analogues, displaying the significance of particular structural features in the sensitivity of neuronal responsiveness. In particular, chain length, location of unsaturation, functional units, and the enantiomeric constitution are critical in stimulating responses from the peripheral system (Grant and Dickens 2011). 1-octen-3-ol is recorded in two formulas as a pesticide: (a) the racemic combination that contains all isomers of this substance, and (b) (R)-(-)-1-octen-3-ol that is an alone single isomer of the racemic mixture. It is generally produced in the breath and sweat of animals, most notably cows, for whose olfactory odorant-binding protein it is the natural ligand (Ramoni et al. 2001). Both 1-octen-3-ol and 3-octanone have indicated promise for usage in crop protection where they have been confirmed as biopesticides (Tonks et al. 2023). When oyster mushrooms are infected by nematodes, they manufacture 1-octen-3-ol, which displays paralytic toxin against the roundworms (Lee et al. 2023). Several plant species belonging to the orders Fabales and Lamiales have been testified to give 1-octen-3-ol in reaction to herbivore damages and mechanical wounding (Ozawa et al. 2000; Kigathi et al. 2009; Seo and Baek 2009). For more research on the physical effects of 1-octen-3-ol on arthropods and fungi, see El Jaddaoui et al. (2023).

5. Drosophila melanogaster as a genetic model

As an important biological model, D. melanogaster (i.e. the fruit fly) reproduced rapidly at a high rate. They have been broadly exploited in genetic and developmental research. This “mini-model” has a completely sequenced and noted genome, which made the application of genome microarrays and the construction of RNA interface libraries more easily (Lionakis and Kontoyiannis 2012). Because it also has a well-documented immune system and a remarkable genetic conservation of biochemical pathways with humans and other animals, it is well suited for exploring pathogenesis (Hamilos et al. 2012).

The life cycle of the fruit flies has four main phases and takes 10–12 days to complete the life cycle, which depends on the temperature (25–29 ℃). The first life phase is the egg, which grows into the embryo after one day. The second phase is the larval period, which has three substages or instars. Around the fifth day, the third instar larvae (mature larvae) metamorphose into the pupal life stage. Development in the pupal stage is such that most tissues in the larvae, and their replacements, rearrange over four days. The subsequent proliferation and discrepancy of cells form adult structures. During initial embryogenesis, imaginal discs create most of the specific structures of adults for instance the wings, legs, eyes, and genitalia (Hartwell et al. 2004). In addition to its utility in genetics, as well as in cell and developmental biology, Drosophila has been adapted for toxicological studies (Rand 2010), including the assessment of volatile toxicity (Singh et al. 2011; Inamdar et al. 2012; Almaliki et al. 2023).

6. 1-octen-3-ol disruption of neurodegeneration and dopamine packaging

Parkinson’s disease is the most common movement disorder in humans. Even though the precise causes are unidentified, the epidemiological and experimental reports point out that more than a few environmental agents, including several synthetic chemicals, may be significant risk factors. In previous reports, it has been demonstrated that 1-octen-3-ol can disrupt dopamine packaging and elicit neurodegeneration in the Drosophila model, thereby implicating it as a possible causal agent in Parkinson’s disease (Inamdar et al. 2013). In addition, it causes cytotoxicity to human embryonic stem cells, with (S)-(+)-1-octen-3-ol being more poisonous than (R)-(-)-1-octen-3-ol (Inamdar et al. 2012). In laboratory tests with human volunteers, a 2-h exposure to minimal concentrations of 1-octen-3-ol can trigger grave effects such as nasal, eye, and throat irritation (Walinder et al. 2008). Indoor concentrations of 1-octen-3-ol were up to 10 µg/m³ in buildings having problems with dampness or water damage (Walinder et al. 2008; Sahlberg et al. 2013). In summary, a combination of hereditary, chemical, and immunologic investigations showed that 1-octen-3-ol triggered the dopamine neuron degeneration in D. melanogaster (Inamdar et al. 2012). By over-expressing the vesicular monoamine transporter (VMAT), it reduced the dopamine toxicity and neurodegeneration, however, mutations reduced both the toxicity worsened by VMAT and tyrosine hydroxylase. Moreover, 1-octen-3-ol restrained the uptake of dopamine in human cell lines expressing the human plasma membrane dopamine transporter and human VMAT2. These records suggested that 1-octen-3-ol exerted toxicity by interruption of dopamine homoeostasis and could denote a naturally happening environmental means implicated in parkinsonism (Inamdar et al. 2012, 2013).

7. 1-octen-3-ol may activate the Toll pathway in Drosophila melanogaster

By using immunologically wild-type white-eyed (y¹w^1,118) 3^rd instar larvae, one study used an eclosion assay to assess the toxicity of VOCs from actively developing fungal cultures, along with distinct chemical criteria of fungal VOCs, and established that 1-octen-3-ol were toxic at the lower concentrations (Bennett and Inamdar 2015; Yin et al. 2015). Additionally, while wild-type fruit flies were subjected to the VOCs emitted by Aspergillus species, substantial developmental delays and death were observed (AL-Maliki et al. 2017; Zhao et al. 2017). It is well-known that two autonomous signal transduction pathways are implicated in triggering the immune response in D. melanogaster, including the Toll pathway, which is involved in establishing dorsoventral polarity in fruit fly embryos and in the defence against fungi (Hashimoto et al. 1988; Brennan and Anderson 2004; Chamy et al. 2008; Valanne et al. 2011). Because one can often answer questions in biology by studying different genotypes of model organisms, Drosophila flies were also tested that had loss-of-function mutations for these pathways in their innate immune systems. With a mutation in either immune pathway, the developmental delays and toxic effects were diminished (Almaliki et al. 2023). The specific eight-carbon VOCs 1-octen-3-ol, 3-octanone, and 3-octanol at 0.1 µmol/mL were less poisonous to Toll mutants. Based on this research, it was proposed that constituents of the innate immune system of D. melanogaster have participated in the toxicity of fungal VOCs. In other words, an overreaction of the immune response may turn fly immune cells against the body they are meant to protect (Figure 2). Therefore, a signalling pathway for fungal VOCs may be on the verge of being discovered in D. melanogaster. Analogous immune defence pathways may be targeted in plants and fungi by these VOCs. For 1-octen-3-ol effects on different arthropods, see El Jaddaoui et al. (2023).

Figure 2.

A model of the Drosophila melanogaster immune system responding to the toxicity of microbial VOCs. This diagram shows the IMD and Toll pathways in fruit flies that are involved in VOC responses. The genes spz⁶ and spz⁴ of the Toll pathway may detect fungal VOCs “at a distance” (i.e. without physical contact) and trigger an overactive immune response that causes fly toxicity. Lack-of-function mutants exhibit modulated or absent toxicity. The coloured circles represent different fungal VOCs. NOS: Nitrate oxide synthase; Rel: Relish enzyme; spz: Spätzle; tube: Protein tube; Drosal/Dif: Dorsal-related immunity factor; drm: Drumstick protein; dpt: Diptericin. The red colour unit denoted the active group.

These studies also have possible consequences for human health. Fungi have long been implicated in the so-called “sick building syndrome”, an ill-defined group of negative symptoms experienced by people who spend extended amounts of time in damp and mouldy spaces. Many studies from the late 1990s and early 2000s hypothesised that mycotoxins, especially trichothecenes, were the causative agents in sick-building syndrome (Cooley et al. 1998; Schwab and Straus 2004; Straus 2009), while other studies denied any association of the syndrome with fungal exposure and indoor health problems (Borchers et al. 2006, 2017). Nevertheless, there is growing proof that non-mycotoxin metabolites, including fungal structural components and volatiles, may be involved. For example, Finnish research correlated multiple chemical sensitivities, after prolonged exposure, to indoor moulds and suggested that mould hypersensitivity is associated with dysregulation of the immune system (Tuuminen 2018). The increasingly voluminous literature on the biological potency of volatile phase metabolites, including 1-octen-3-ol, has demonstrated that minute quantities of biogenic VOCs can elicit many interspecific biological responses including toxicity. Nonetheless, a general problem concerning the physiological role of VOCs is that we do not know how they work at the molecular level. The hypothesis we present here suggests that future investigations ought to link VOC research more closely with immunological studies.

8. Conclusions

The overall literature on volatiles is enormous but fragmented. VOCs have been studied for their odour properties, taxonomic characters, and as indirect assays of food spoilage, disease detection, and other instances when it is hard to directly spot fungal growth. Moreover, in recent years, fungal VOCs have received increasing attention in the scientific community because it has become apparent that many of them serve as intracellular, intercellular, and interspecific signalling molecules. For example, several of them have been implicated in the negative consequences associated with time spent in mould-damaged schools, homes, or workplaces. In summary, fungal VOCs are a diverse group of compounds with multifaceted roles in ecosystems, agriculture, and potentially human health. Their study has expanded from an early focus on odour formation and mycotoxin production to encompass their broader ecological and biotechnological potential. This review has emphasised the efficiency of Drosophila melanogaster as a useful tool for studying volatile toxicity because the innate immune systems of the wild-type Drosophila flies display toxicological responses to many fungal VOCs, and because flies with loss-of-function mutations in their immune pathways have mitigated responses. Therefore, it would make sense for future research to put increasing emphasis on studying the function of the natural immune system in mediating VOC toxicity.

Funding Statement

This work was supported by the Research Program of Qilu Institute of Technology [QIT23TP009] for Guohua Yin, while research in the Bennett laboratory has been supported by a cooperative agreement from the U.S. Department of Agriculture and a grant from the Eppley Foundation.

Disclosure statement

No potential conflict of interest was reported by the author(s).