Appl Microbiol Biotechnol DOI 10.1007/s00253-015-6494-4

MINI-REVIEW

Fungal volatile organic compounds and their role in ecosystems Richard Hung & Samantha Lee & Joan W. Bennett

Received: 15 January 2015 / Revised: 17 February 2015 / Accepted: 17 February 2015 # Springer-Verlag Berlin Heidelberg 2015

Abstract All odorants are volatile organic compounds (VOCs), i.e., low molecular weight compounds that easily evaporate at normal temperatures and pressure. Fungal VOCs are relatively understudied compared to VOCs of bacterial, plant, or synthetic origin. Much of the research to date on fungal VOCs has focused on their food and flavor properties, their use as indirect indicators of fungal growth in agriculture, or their role as semiochemicals for insects. In addition, research into fungal volatiles has also taken place to monitor spoilage, for purposes of chemotaxonomy, for use in biofilters and for biodiesel, to detect plant and animal disease, for Bmycofumigation,^ and with respect to plant health. As methods for the analysis of gas phase molecules have improved, it has become apparent that fungal VOC are more chemically varied and more biologically active than has generally been realized. In particular, there is increasing data that show that fungal VOCs frequently mediate interactions between organisms within and across different ecological niches. The goal of this mini review is to orchestrate data on fungal VOCs obtained from disparate disciplines as well as to draw attention to the ecological importance of fungal VOCs in signaling between different species. Technologies and approaches that are common in one area of research are often unknown in others, and the study of fungal VOCs would benefit from more cross talk between subdisciplines.

Keywords Fungal volatiles . Volatile organic compounds (VOCs) . Interspecies interactions . Mushroom alcohol (1-octen-3-ol) . Semiochemical . Sick building syndrome R. Hung (*) : S. Lee : J. W. Bennett Department of Plant Biology and Pathology, Rutgers, The State University of New Jersey, 59 Dudley Rd., New Brunswick, NJ 08901, USA e-mail: [email protected]

Introduction Volatile organic compounds (VOCs) are low molecular weight compounds that can vaporize and enter the gas phase at normal atmospheric temperatures and pressure. VOCs generally have low to medium water solubility and often have a distinctive odor (Herrmann 2010). In most studies with modern analytical equipment, growing fungi are shown to produce VOCs as a mixture of compounds of many molecular sizes in which the types, the numbers, and the amounts of individual VOCs are variable. Chemically, this gas phase mixture may contain acids, alcohols, aldehydes, aromatics, esters, heterocycles, ketones, terpenes, thiols, and so forth. Further, the complex cocktail varies temporarily and changes with temperature, substrate, and other environmental variables for each species. Over 300 distinct VOCs have been identified from fungi (Chiron and Michelot 2005, Korpi et al. 2009, Lemfack et al. 2014), and the volatile sesquiterpenoids have been the focus of particular attention (Kramer and Abraham 2012). The emissions of microbes affect atmospheric chemistry (Kesselmeier et al. 2000; Leff and Fierer, 2008; Bäck et al. 2010). There is a growing literature on VOCs of bacterial origin and their role in signaling in terrestrial environments (see, for example, Schulz and Dickschat, 2007; Junker and Tholl, 2013: Piechulla and Degenhardt 2014). However, there has been far less attention paid to the ecological role of VOCs of fungal origin (Bennett et al. 2013; Bitas et al. 2013). Most published studies on fungal VOCs are conducted for economic reasons. For example, food and flavor chemists have analyzed mushroom VOCs for their gustatory properties. Agriculturalists have used them as indicators of mold spoilage in crops. Building scientists have used them as indicators of hidden mold growth in water-damaged buildings. Entomologists study them as chemical cues that attract or repel certain insect species. Mycologists have described them as spore inhibitors and as signals for fungal development.

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Plant pathologists view them as stress metabolites. (Note: Specific literature citations to all of these topics are given in the sections below.) As a result, research on fungal VOCs is scattered over many disciplines. Although our intent is to highlight the role of fungal-derived volatiles in mediating short- and long-distance physiological effects in complex ecosystems, we also briefly introduce and consolidate representative research from apparently unrelated fields, provide references that will lead researchers to pertinent literature, and thereby hope to promote crosstalk between scientists currently separated by different disciplinary traditions utilizing somewhat different approaches and conceptual frameworks. Informative experiments have been conducted by workers in many fields ranging from analytical chemistry, developmental mycology, food and flavor research, entomology, olfaction, perfumery, and toxicology. We believe that collaborations between scientists in these disparate sub-disciplines will provide mutual benefits, accelerate the sciences involved in studying microbial volatile organic compounds, and lead to a more meaningful synthesis of our understanding of the important role that biogenic, gas phase molecules play in interorganism communication.

How do we analyze fungal VOCs? Methods In order to study fungal VOCs, they first must be isolated and characterized. Methodologies for the separation, concentration, identification, and quantification of gas phase molecules have lagged over cognate techniques for characterization of other natural products. Nevertheless, over recent decades, new analytic techniques have improved our ability to study biologically produced volatiles. With each improvement in our analytical abilities, the number of known fungal VOCs increases as does our appreciation for the challenges involved in identifying compounds that tend to be found in complex and constantly changing combinations in low to extremely low concentrations. See Zhang and Li (2010) for a useful review of analytical methods. Early studies usually were conducted using steam distillation coupled with liquid-liquid extraction, subsequent concentration, and then laborious chemical identification of individual concentrated VOCs, often with the intent of understanding mushroom aromas (see, for example, Cronin and Ward 1971). Using such traditional approaches, 1-octen-3-ol (mushroom alcohol) was identified as the main VOC aroma compound of many mushroom species such as Agaricus bisporus (Cronin and Ward 1971; Picardi and Issenbergl 1973) and mold genera such as Aspergillus and Penicillium (Kaminiski et al. 1974).

With the advent of reliable and affordable gas chromatography–mass spectrometry (GC-MS), the separation, identification, and quantification steps were linked. In general, nowadays, the VOCs are collected from a headspace, trapped on a sorptive surface such as that described in Booth et al. 2011, and separated by GC, and then the individual VOCs from complex mixtures are identified by comparisons of mass spectra with library spectra, authentic standards, and/or chromatographic retention indices. Variations on the identification protocol include proton transfer reaction–mass spectrometry (PTR-MS) that, for example, has been used in measuring volatile emissions of Muscodor albus (Ezra et al. 2004) and monitoring foodborne pathogens (Bunge et al. 2008). Another refinement is selected ion flow tube–mass spectrometry (SIFT-MS) that has been adapted for the detection of volatiles from medically important fungi such as Aspergillus fumigatus, Candida albicans, and Cryptococcus neoformans (Scotter et al. 2005). Coupling a headspace sorptive extraction technique with gas chromatography–time of flight mass spectrometry (GC-TOFMS), Wihlborg et al. (2008) were able to identify Penicillium italicum, Penicillium camemberti, and Penicillium roqueforti based on their volatile metabolite profiles. Solid phase microextraction (SPME) is an important advance. In this portable method, VOCs are concentrated on a fiber and later delivered to the input of a detector. Desorption occurs in the GC injector itself. SPME combines extraction, concentration, and introduction. Nevertheless, profiles of VOCs obtained are dependent on the fibers and extraction method used (Jeleń 2003). In one interesting application, Camara et al. (2007) compared the VOC profiles of whiskey volatiles obtained by liquid-liquid extraction with SPME analysis and found that SPME was superior. In general, SPME is well suited for taking environmental samples that are then transported back to the laboratory. Over the years, SPME technologies have progressed and improved, with lowaffinity surfaces substituted by resins or specially charged materials with a specific affinity for certain types of compounds. It has been applied, for example, to analysis of the biocontrol fungus Trichoderma (Stoppacher et al. 2010) and to detect toxigenic strains of Fusarium (Demyttenaere et al. 2004). In summary, SPME is good for determining the relative quantity of a target volatile compound in an exploratory situation or in a repetitive sampling process but is not useful for the identification of novel compounds. The Be-nose^ is a device that utilizes the unique electronic signature that different compounds produce when they interact with various electronic surfaces, and is useful for specific applications with known target VOCs. Originally applied for clinical diagnosis of bacterial human pathogens in breath (Bos et al. 2013) and for environmental monitoring of bacteria in potable water (Canhoto and Magan 2003), e-nose detection of fungal VOCs has been used to detect spoilage in stored grains

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(Magan and Evans 2000), hidden mold growth in indoor environments (Kuske et al. 2005), and evidence of fungal contamination on library paper (Canhoto et al. 2004). Finally, one should not underestimate the human nose as a mold detection device. The odor thresholds of the musty odorants geosmin and 1-octen-3-ol are so low that most people can smell extremely low concentrations in ambient air. Overview of fungal VOC detection and characterization Of the more than 100,000 species of described fungi, only about 100 species have been tested for their VOC production for any reason. In each case, published VOC profiles have been shown to be produced as mixtures of different chemical classes and their derivatives: alcohols, aldehydes, hydrocarbons, aromatics, nitrogen-containing compounds, sulfurcontaining compounds, terpenoids, and so forth. An extremely useful database of bacterial and fungal volatiles (mVOC) has been compiled at the University of Rostock, Germany (Lemfack et al. 2014). This searchable database can be accessed by chemical name, by certain chemical properties, by structural similarities, by species of producing microorganisms, or by a combination of search terms. Particularly useful is the Bsignature table^ that plots the emitted VOCs of a given species against the VOCs of all the other microbial species in the database. See http://bioinformatics.charite.de/mvoc/#. Several final caveats First, the analytical method used affects the VOC profile obtained. In older studies using exhaustive solvent extraction procedures and heat, some of the reported VOCs are degradation products. Artifacts can also be introduced by solid sorbents during headspace analysis. For exampling, Coeur et al. (1997) reported the degradation of pinene and sabinene on Tenax Carbowax, leading to the formation of camphene, limonene, and other terpene artifacts. Further, water from sampled air can cause problems during GC analysis. Since fungal VOCs are more likely to form under humid atmospheric conditions, this is a particular challenge to the outcome of environmental sampling. For a comprehensive review of some of the analytical challenges surrounding accurate VOC detection, see Salthammer and Uhde (2009). Second, while it is easy to assume that all the VOCs reported for a given species are metabolic products of that species, one should remember that fungi are the planet’s great degraders, producing a vast number of extracellular hydrolytic and other enzymes capable of breaking down all kinds of exogenous chemicals. Thus, many of VOCs identified as associated with a given species are not necessarily emitted by an anabolic process of fungal biosynthesis, but rather as incidental extracellular breakdown products of a given substrate. In controlled laboratory studies, it has been shown that the VOC profile of any given species is highly dependent on the

cultivation medium/substrate (Fiedler et al. 2001; Matysik et al. 2008; Polizzi et al. 2012) More studies of this kind are needed.

Why have scientists studied fungal VOCS? An attempt to review the relevant literature on the ecological function of fungal VOCs must take into account the fact that most of what we know about these compounds comes from research outside the field of ecology, usually conducted for a practical end. The sections below introduce some of the scientific subdisciplines that have conducted research on the characterization and application of fungal VOCs, with selected references that can provide an entry into the broader literature. Olfaction and aroma In order to smell a substance, it must be in the vapor phase, or as Diane Ackerman wrote in Natural History of the Senses in 1991, BWe can smell something only when it is evaporating.^ Not surprisingly, much of the research on VOCs in general, and on fungal VOCs in particular, has been conducted by perfumers and food scientists (Berger 1995; Sell 2006). It would take an encyclopedia to cover this topic adequately; however, we here give a few examples. Fungal volatiles contribute to the desirable flavor properties of certain cheeses, sausages, beverages, Asian food products, etc., so odorant analyses have been used to monitor quality of these fermented foods (Karahadian et al. 1985; Kinderlerer 1989; Bruna et al. 2001; Karlshøj et al. 2007). Similarly, VOC profiles of gourmet macrofungi (e.g., chanterelles and truffles) have been analyzed (Fraatz and Zorn 2010). Many fungal VOCs are chemically the same as desirable plant products and are classified as Bbioidentical^ natural flavoring ingredients, thus offering a wide range of possibilities in the food industry (Lomascolo et al. 1999). One famous example is the production 6-pentyl-α-pyrone, a lactone with a characteristic coconut odor, by certain species of Trichoderma (Prapulla et al. 1992). The patent literature offers a rich source for information on the production of pleasing aroma compounds by fungi and contains many pertinent references often overlooked by academic scientists. Malodors as indicators of spoilage BOff^ flavors and odors in feeds and foodstuffs are mostly due to microbial metabolism and can be used as indirect indicators of contamination (Schnürer et al. 1999). For example, VOCs have been used to detect spoilage in a jam factory (Nieminen et al. 2008) and on bakery products (Keshri et al. 2002). Further, VOC sampling has been used to monitor the presence of fungi in stored agricultural products (Jeleń and Wasowicz

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1998), and the key volatile groups indicative of spoilage in stored grains have been summarized by Magan and Evans (2000). VOCs are also produced by Bindoor molds,^ and their detection provides a nondestructive way to find molds inside of buildings (Matysik et al. 2008). Another context in which malodorous microbial VOCs have been studied concerns efforts to prevent bad odors in compost facilities and feed lots (Fischer et al. 1999). The undesirable emanations from composting and biowaste handling facilities are suspected of being detrimental to human health (Müller et al. 2004). Fingerprinting and chemotaxonomy Fungal VOCs have been applied in chemotaxonomy. Berger et al. (1986) were able to characterize several basidiomycetes by their odors while Larsen and Frisvad (1995) showed that VOCs could be used to distinguish members of the genus Penicillium at the species level. Korpi et al. (1998) found differences in VOC profiles of Bindoor^ microbes grown on different building materials. Using volatile production, Polizzi et al. (2009) distinguished Chaetomium spp. and Epicoccum spp. from a group of 76 fungal strains. The VOC signatures of virulent and avirulent entomopathogenic species Metarrhizium anisopliae and Beauveria bassiana showed consistent patterns (Hussain et al. 2010). Different odorant profiles were found for fungi from different functional groups (ectomycorrhizal, pathogenic, and saprophytic), particularly in the pattern of sesquiterpenes, and these profiles could be used to predict members of different ecological groups (Muller et al. 2013). Biofilters and Bbiodiesel^ Fungi are not only able to create a large variety of volatile compounds; they are also able to metabolize them. This has led to their incorporation into biofilters for use in degrading volatile contaminants (Kennes and Veiga 2004; VergaraFernandez et al. 2011). Building scientists increasingly recognize that metabolic capabilities of airborne fungi warrant closer study (Fischer and Dott 2003). Fungi are well known for utilizing plant biomass, and it has been hypothesized that they could be used as sources of generating diesel-type compounds for what is variously called Bbiodiesel^ or Bmycodiesel^ (Grigoriev et al. 2011). For example, several species of Ascocoryne generated VOC mixtures including alkanes, alkenes, alcohols, ester, ketones, acids, benzene derivatives, and terpenes, some of which are similar to biofuel target molecules (Griffin et al. 2010; Mallette et al. 2014). The general potential for fungi in biofuel development has been reviewed by Morath et al. (2012), and the specific role of endophytic fungi in this context has been reviewed by Strobel (2014a, b, c).

Disease detection Odorants can be used to detect disease (Casalinuovo et al. 2006) and have been employed by both plant pathologists and medical mycologists. An illustration from the plant world is the powdery mildew fungus Uncinula necator that causes a serious vineyard infection. Darriet et al. (2002) detected several distinctive odorants from diseased grapes including 1-octen-3-one (mushroom-like), (Z)-1,5-octadien-3one (geranium-like), and an unidentified fishy odor. An illustration from the world of human disease is the common mold Aspergillus fumigatus, which can cause invasive pulmonary aspergillosis, a condition associated with high mortality in immunocompromised patients. When grown in vitro, Aspergillus fumigatus produces farnesene, and it was suggested that terpene volatiles could be used for early detection of invasive aspergillosis (Bazemore et al. 2012; Heddergott et al. 2014). The compound 2-pentylfuran was detected in the breath of patients with Aspergillus fumigatus infections (Chambers et al. 2009).

Ecological role of VOCs and interspecies interactions Fungi and other microorganisms do not live alone. Rather, they form complex, multi-species networks, alliances, and symbioses. In seeking the chemical basis by which microbes form these communities, most of the emphasis of past research has been placed on the role of soluble secondary metabolites in determining the distribution and interspecific interactions within ecological niches. More recently, there has been growing awareness that the blends of VOCs produced by fungi and other microbes during their growth also play a role in the formation and regulation of symbiotic associations and in the distribution of saprophytic, mycorrhizal, and pathogenic organisms. They are involved in host recognition, defense, and competition. They mediate interactions in soil environments (Effmert et al. 2012) and in terrestrial habitats; they are carriers of various aerial signals (Morath et al. 2012). A list of a few representative fungal VOCs that are known to have interspecific effects, with selected references to the relevant literature, is given in Table 1. Sections below highlight major areas that inform our understanding that VOCs can serve as ecologically important signaling molecules. The examples in the table and in the text are illustrative of the diversity of VOC functionalities but are far from comprehensive. Effects on plants It has been known for many years that beneficial rhizosphere bacteria produce VOCs that enhance plant growth (Lugtenberg and Kamilova 2009; Blom et al. 2011). Similarly, volatile mixtures emitted from the biocontrol fungus Trichoderma viride

Appl Microbiol Biotechnol Table 1

Illustrative examples of fungal volatiles and their functionalities

Compound

Producing species Geotrichum candidum

Functionality

Reference(s)

Self-inhibition

Robinson et al. 1989

Anti-fungal against: Bulmeria graminis Fusarium oxysporum Colletotrichum fragarie Botrytis cinerea

Koitabashi et al. 2004

Complete inhibition of: Pythium ultimum Rhizoctonia solani Tapesia yallundae Xylaria sp.

Strobel et al. 2001

Self-inhibition of mycelial development

Hornby et al. 2001

Apoptosis in Aspergillus nidulans

Semighini et al. 2006

Altered morphology and reduced fitness in Fusarium graminearum

Semighini et al. 2008

Apoptosis in malignant mammalian cells

Joo and Jetten 2010

Microbe detection in Drosophila

Stensmyr et al. 2012

Functionality

Reference

Fungal spore production, inhibition, induction

Berendsen et al. 2013 Chitarra et al. 2004

Insect attractant, repellant

Davis et al. 2013

Trimethylamine

Irpex lacteus 5-Pentyl-2-furaldehyde

Muscodor albus 3-Methyl-acetate

Candida albicans (Hornby et al. 2001) Farnesol

Botrytis cinerea (La Guerche et al. 2005) Penicillium expansum (La Guerche et al. 2005) Geosmin (4S,4aS,8aR)-4,8a-Dimethyl-1,2,3,4,5,6,7,8-octahydronaphthalen-4a-ol

Compound

Producing species Most fungi 1-octen-3-ol Trichoderma viride Trichoderma harzianum

Phytotoxicity during seedling formation. Seedling blight suppression

El-Hasan and Buchenauer 2009

6-Pentyl-α-pyrone Schiestl et al. 2006 Epichloe sp. Chokol K.

Insect attractant

Steinebrunner et al. 2008

(1R*,2S*,3R*)-1,2-dimethyl-3-(6-methylhepta-1,5-dien-2-yl)cyclopentanol

enhanced growth of Arabidopsis (Hung et al. 2013), and volatiles of Cladosporium cladosporioides enhanced growth of tobacco plants (Paul and Park 2013). In lettuce, VOCs emitted from a consortium of Fusarium oxysporum and bacteria also promoted growth (Minerdi et al. 2009). Fungal volatiles induce systemic resistance in plants (Naznin et al. 2014), affect barley root morphology (Fiers et al. 2013), inhibit Arabidopsis seed germination (Hung et al. 2014a,b), and promote starch accumulation in leaves of several plant species (Ezquer et al. 2010). Finally, although it is beyond the scope of this review, there is considerable research on the way that the gaseous hormone ethylene controls many aspects of plant growth and development (Zipfel, 2013).

The unique gustatory and olfactory qualities of truffles (gourmet macrofungi in the genus Tuber) have attracted attention from food connoisseurs for centuries (Brillat-Savarin 1825). More recently, it has become apparent that these subterranean fungi emit VOCs that may inhibit plant growth (Splivallo et al. 2007; Tarkka and Piechulla 2007). Thus, chemical ecologists have joined food scientists in their focus on the VOCs of these fascinating fungi. Between 1980 and 2010, approximately 30 papers were published on truffle VOCs, spanning identification, variability, their interactions with other organisms, and biosynthesis. (For a comprehensive review of these papers, see Splivallo et al. 2011.) There is increasing evidence that communities of

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bacteria (Barbieri et al. 2007) and yeast (Buzzini et al. 2005) contribute to the delectable aroma profile of truffles. In fact, in Tuber borchii, the characteristic thiophene volatiles are produced by bacteria resident on the truffle by biotransformation of nonvolatile precursors. These resident bacteria are important in the interactions between truffles, their plant symbionts, and other members of these complex communities (Splivallo et al. 2014). Although individual fungal VOCs tested to date tend to have fewer known effects on plants than mixtures, in some trials, low concentrations of 1-hexanol, a truffle volatile, had a growth-promoting effect (Blom et al. 2011). However, when tested at a higher concentration, 1-hexanol had a growthinhibiting effect (Splivallo et al. 2007) illustrating the importance of volatile concentration. Low concentrations of 2methyl-1-butanol yielded a small but significant increase in fresh weight in Arabidopsis while 2-ethylhexanal inhibited spore germination and growth of 2-week-old vegetative plants (Hung et al. 2014b). The endophytic fungi that live within plants produce many metabolites that benefit the host plant, including VOCs. For example, a Phoma sp. isolated from creosote bush produces VOCs hypothesized to contribute to the ability of this shrub to survive harsh desert habitats (Strobel et al. 2011). Other fungal endophytes make volatiles that defend against pathogens of their host plants (Macías-Rubalcava et al. 2010) (see below). Effects on fungi and other microbes VOCs mediate interactions between bacteria and fungi in the rhizosphere and in aerial environments, often in multipartite niches that include plants, insects, and other life-forms (Wheatley 2002; Effmert et al. 2012). Muscodor albus, an endophyte originally isolated from a cinnamon tree, is a good case in point. It produces blends of VOC with antibiotic properties. When grown in pure culture, the VOCs emitted by Muscodor albus can kill a range of microbial pathogens in a process dubbed Bmycofumigation^ (Strobel 2012). The endophyte Muscodor crispans also produces a mixture of VOCs that inhibit a wide range of plant pathogens, including the fungus Mycosphaerella fijiensis (the black sigatoka pathogen of bananas), and the bacterium Xanthomonas axonopodis pv. citri (a pathogen of citrus) (Mitchell et al. 2010). Muscodor sutura produces a large number of compounds with known antifungal properties including thujopsene, chamigrene, and isocaryophyllene (Kudalkar et al. 2012). A virulent strain of F. oxysporum inhibits growth of its nonvirulent form, permitting only the plant pathogenic fungi to grow (Minerdi et al. 2009). The VOCs of Oxyporus latemarginatus, an endophyte isolated from red peppers, also had a negative effect on the mycelial growth of several plant pathogens (Ezra and Strobel 2003; Atmosukarto et al. 2005; Lee et al. 2009). The VOCs emitted by Muscodor albus, the first species in which mycofumigation was described, were recently analyzed in an

Escherichia coli knock out library, and exhibited a number of toxigenic properties, including DNA alkylation, raising possible questions about the safety of the mycofumigation process (Alpha et al. 2015). The eight-carbon volatile 1-octen-3-ol, also known as Bmushroom alcohol,^ acts as a self-inhibitor of spore germination in Penicillium paneum (Chitarra et al. 2004, 2005), Aspergillus nidulans (Herrero-Garcia et al. 2011), and Lecanicillium fungicola (Berendsen et al. 2013). The mushroom Sarcodon scabrosus produces two diterpenoid compounds that inhibit the growth of several bacteria (Ezquer et al. 2010), and Pleurotus ostreatus produces VOCs with strong antibacterial activity (Beltran-Garcia et al. 1997). Exposure to VOCs from bacteria and yeast have caused changes in pigmentation of sapstain fungi (Bruce et al. 2003) and changes to the VOC production of other microbes (Evans et al. 2008). In addition, biostatic effects have been observed when sapstain fungi were exposed to VOCs produced by Lactobacillus plantarum (El-Fouly et al. 2011). Effects on arthropods Entomologists have led the way in the study of signaling compounds that function in extremely low concentrations. Many of these so-called Bsemiochemicals^ or Binfochemicals^ are microbial volatiles (Bennett et al. 2013). The field of chemical ecology is replete with research about the way in which insects interact with odorants emitted by plants, fungi, and other volatile sources. Greatly to oversimplify, many fungal VOCs attract or repel insects, serve as aggregation pheromones and oviposition stimulants, and/or are important in host location and attraction to food resources (Davis et al. 2013). Olfaction has been well studied in the mosquitoes that act as vectors for malaria and yellow fever (Takken, 1991). In particular, the abundant eight-carbon alcohol, 1-octen-3-ol, has been identified as a mosquito attractant and can be used as a lure in traps for species of medical and veterinary importance (French and Kline 1989; Kline et al. 1991). It also serves as an attractant for midges (Blackwell et al. 1996). By the same token, the volatile profile of the entomopathogenic fungal species B. bassiana has been studied for its potential use in entomological biocontrol (Crespo et al. 2008), and there is evidence that B. bassiana can be used as an effective biocide for mosquitoes (George et al. 2013). In another interesting example, fungal volatiles produced on pine weevil frass protect weevil eggs and affect the pine weevil host-odor search (Azeem, et al, 2015). The entomological literature on volatile phase semiochemicals is vast (Davis et al. 2013). VOCs and indoor air quality Most people spend most of their time indoors, and there has been growing awareness that buildings, their contents, and

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their microbial flora are important to human health. Damp buildings in particular tend to support complex microbial ecosystems that may include Bblooms^ of molds and mildews. These indoor fungi have been implicated in the etiology of a poorly defined health problem called Bsick building syndrome,^ Bdamp building syndrome,^ or Bdamp-building-related illnesses^ (Kuhn and Ghannoum, 2003; Carey et al. 2012). There is no consistent definition of this condition, which consists of a group of nonspecific symptoms (fatigue, respiratory distress, skin problems, eye irritation, and so forth). The Boffgassing^ of industrial solvents and airborne particulates and the biogenic production of mold toxins (mycotoxins) have been implicated as causes of this elusive syndrome (Straus, 2009). Moreover, it has been hypothesized that in addition to mycotoxins, mold VOCs may be involved in sick building syndrome (Mølhave et al. 1993; Mølhave 2009). It is known that many biogenic VOCs are cytotoxic in mammalian tissue culture systems (Korpi et al. 2009), and some researchers have linked fungal VOCs to the symptomology of damp-building-related illness (Araki et al. 2010, 2012; Takigawa et al. 2009). Major authoritative reviews on the topic of indoor air quality, human health, and fungal exposure have been conducted by the Institute of Medicine (2004) and the World Health Organization (WHO 2009). Neither meta-review was able to find a definitive link between building-related illness and the presence of molds or their metabolites. Nevertheless, public concern remains high. Our laboratory has developed a Drosophila melanogaster model for studying the toxigenic potential of fungal VOCs (Inamdar et al. 2010, 2012). We have found that exposure to chemical standards of several eight-carbon fungal VOCs can cause neurotoxic symptoms in flies that can be dissected at the molecular level using GFP-linked markers, confocal microscopy, and mutant analysis (Inamdar et al. 2010). In particular, low concentrations of 1-octen-3-ol caused parkinsonian symptoms, reduced dopamine levels, and were associated with dopaminergic neuron degeneration, while overexpression of the vesicular monoamine transporter (VMAT) rescued the dopamine toxicity and neurodegeneration (Inamdar et al. 2013). Similarly, 1-octen-3-ol stimulated a NO-mediated inflammatory response in nervous and respiratory tissues of D. melanogaster (Inamdar and Bennett 2014). We also have confirmed the toxicity of 1-octen-3-ol in human cell culture using both embryonic stem lines (Inamdar et al. 2012) and cell lines that express the human plasma membrane dopamine transporter (Inamdar et al. 2013).

Conclusion In this mini-review, we have attempted to orchestrate data obtained from widely disparate scientific fields with the intent of highlighting the fact that fungal VOCs are ubiquitous and

have biotechnological utility and that they mediate numerous interactions between organisms within and across different ecological niches. Most of the best known examples of interkingdom signaling involve the study of nonvolatile natural products (secondary metabolites) and their chemical interactions. However, we believe that the advances in analytical and genomics techniques will generate many cognate multidisciplinary collaborations focused on gas phase organic molecules. Why do fungi emit odorants? Because so much of the research has been conducted with practical intent or for a commercial end, the vast majority of the existing published literature does not address the question of why these compounds are made in nature. Theodosius Dobzhansky’s famous 1973 aphorism is worth quoting: BIn biology, nothing makes sense except in the light of evolution.^ Fungal VOCs surely have evolved for adaptive reasons, to facilitate communication within terrestrial environments, to act as developmental signals, to aid in reproduction, to attract and repulse other organisms, and for many other functional roles. Reviews, by their very nature, require compression and simplification. Given the scattered nature of the research on fungal volatiles, we are aware that we have run the risk of oversimplifying the studies on ecology, while perhaps overemphasizing what is known about their role as useful aroma compounds and their concomitant use as indicators of fungal growth. Thus, in closing, we remind readers that we barely have begun to explore this important biological frontier. As scientists learn more about the complex microbiomes—both bacterial and fungal—that live with all forms of Bhigher^ life, no doubt we will discover that volatile-mediated, interorganism cross talk is far more common and more complex than we now recognize. We hope that this mini-review will encourage researchers to explore the way in which fungi and other microbes use gas phase molecules to transmit molecular signals. Acknowledgments We are very grateful to Arati Inamdar, Shannon Morath, Sally Padhi, Prakash Masurekar, David Pu, Jason Richardson, and Guohua Yin for stimulating discussions and to Rutgers University and the National Science Foundation Graduate Research Fellowship Program under Grant No. (0937373) for research support.

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