Introduction
1. Introduction :
1.1. Volatile organic compounds (VOCs):
Volatile organic compounds (VOCs) are low molecular weight compounds that can
vaporize and enter the gas phase at normal atmospheric temperatures and pressure. Most are
lipids and thus have low water solubility (Herrmann, 2010 and Werner et al., 2016).
Compound groups included under this classification have various structural characteristics
and chemical properties that include: Alcohols, halogenated hydrocarbons, aromatics, nitriles,
sulfides and ethers (Hung et al., 2015).
Volatile organic compounds come from many sources: a) Anthropogenic source: Paints
and coatings, Chlorofluorocarbons and chlorocarbons, Fossil fuels, Benzene and
Formaldehyde and b) Biologically sources: plants and microorganisms (Fungi and bacteria)
(Goldstein and Galbally, 2007).
These molecules can be used as health indicator that can be sampled quickly and noninvasively from breath, urine or other bodily fluids (Fig. 1). Particular patterns of VOC
biomarkers are characteristic of specific disease processes, because their production is linked
directly to metabolic activity in the body. Changes in the concentrations of VOCs occur at the
very earliest stages of disease; detecting these VOC biomarkers can therefore allow for disease
diagnosis before other physical symptoms have become apparent. Early diagnosis is critical in
the successful treatment of cancer, as well as infectious and inflammatory diseases (Sethi et al.,
2013).
Fig. (1): Non-invasive patient sampling in urine or breath.
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1.2. Fungal volatile organic compounds (FVOCs):
Over 300 VOCs have been identified from fungi where they occur as mixtures of
simple hydrocarbons, heterocycles, aldehydes, ketones, alcohols, phenols, thioalcohols,
thioesters and their derivatives, including, among others, benzene derivatives, and
cyclohexanes. Fungal VOCs are derived from both primary and secondary metabolism
pathways, and because VOCs can diffuse through the atmosphere and soil, they are ideal
“infochemicals” with distinctive and characteristic odors (Table 1) (Korpi et al., 2009 and
Lemfack et al., 2014).
Table (1): Structures, functions and odors of selected common volatile compounds
produced by fungi.
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A single review cannot do justice to the enormous scientific literature that has contributed
to our current knowledge about fungal VOCs (Fig. 2). Therefore, this research will focus on
recent improvements in our ability to isolate and identify VOCs, as well as on provocative new
findings in toxicology and biocontrol from the study of endophytes that highlight the
physiological potency of these small gas-phase molecules and their potential for exploitation in
biotechnology. For an overview of the contributions of fungal VOCs to food and flavor
research see fig. 2 (Fraatz and Zorn, 2010 and Styger et al., 2011).
Fig. (2): Subdisciplines that have contributed to our knowledge of fungal VOCs.
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Characterization of FVOCs
2. Characterization of FVOCs :
2.1. Extraction, Separation and Identification of FVOCs :
The two main methods for the isolation of volatile organic compounds from liquids
are the purge & trap method and headspace-solid phase microextraction method (HSSPME (Mallia et al., 2005). These are described below:
(1) Purge and Trap Method (P&T)
This method, also known as the dynamic headspace method, removes (separates)
volatile compounds from the sample matrix (culture sample) by passing an inert gas
such as helium or nitrogen through the matrix (purging) as shown in fig. 3. The target,
volatile compounds are desorbed from the aqueous phase to the gas phase (purged) and
are then separated from the stream of gas (trapped) by adsorbent filters. The adsorbent
material is then heated in a stream of GC carrier gas (usually pure helium). This releases
the trapped substances into the carrier gas, the target analytes are introduced to GC, and
analysed. Typical trapping (adsorbent) materials are porous polymer beads, activated
charcoal, tenax, silica gel, other GC column packing materials, or combinations of such
materials (Fig. 3) (Mallia et al., 2005).
Fig. (3): Experimental design used for purge-and-trap analysis of culture samples.
(2) HS-SPME:
This method is less sensitive compared to the purge & trap method, but operation is
simple, easily automated. SPME is a method used to both extract and concentrate
organic compounds in which a fiber needle attachment which has been chemically
coated with a fused silica equivalent to a GC liquid phase, is dipped directly into liquid
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samples, or exposed to the headspace vapors from liquid or solid samples (Fig. 4) (Mallia
et al., 2005 and Morath et al., 2012).
Fig. (4): Solid phase microextraction component.
With the advent of reliable and affordable gas chromatography–mass spectrometry (GCMS), 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 (Fig. 5).
Fig. (5): Diagram of analysis with (SPME– GC-MS).
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2.2. Development of the first database of FVOCs :
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 “signature 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/ (Fig 6).
Fig. (6): Microbial VOCs database website.
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Applications of FVOCs
3. Applications of FVOCs :
3.1. Biomarkers of fungal diseases:
Odorants can be used to detect disease and have been employed by both plant pathologists
and medical mycologists (Casalinuovo et al., 2006). 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 1octen-3-one (mushroom-like), (Z)-1, 5-octadien-3-one (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 .The compound 2-pentylfuran was detected in the breath of
patients with Aspergillus fumigatus infections and these diseases can be detected by electric
nose (Bazemore et al., 2012 and Heddergott et al., 2014).
3.2. 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, ‘‘we 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. It would take an encyclopedia to cover
this topic adequately; however, we here give a few examples. (Sell, 2006 and Hung et al.,
2015).
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 (Karlshøj et al., 2007). Similarly, VOC profiles of gourmet
macrofungi (e.g., chanterelles and truffles) have been analyzed. Many fungal VOCs are
chemically the same as desirable plant products and are classified as ‘bioidentical’ natural
flavoring ingredients, thus offering a wide range of possibilities in the food industry. One
famous example is the production 6-pentyl-α-pyrone, a lactone with a characteristic coconut
odor by certain species of Trichoderma (Fraatz and Zorn, 2010).
3.3. Malodors as indicators of spoilage
‘‘Off’’ flavors and odors in feeds and foodstuffs are mostly due to microbial metabolism
and can be used as indirect indicators of contamination. For example, VOCs have been used to
detect spoilage in a jam factory and on bakery products (Keshri et al., 2002 and Nieminen et
al., 2008). Further, VOC sampling has been used to monitor the presence of fungi in stored
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agricultural products, and the key volatile groups indicative of spoilage in stored grains have
been summarized by Magan and Evans (2000). VOCs are also produced by ‘‘indoor molds’’
and their detection provides a nondestructive way to find molds inside of buildings (Matysik et
al., 2008 and 2009).
Another context in which malodorous microbial VOCs have been studied concerns efforts
to prevent bad odors in compost facilities and feed lots. The undesirable emanations from
composting and bio-waste handling facilities are suspected of being detrimental to human
health (Müller et al., 2004).
3.4. 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.
Oliveira et al. (2015) use FVOC as a Chemotaxonomic Tool of the Botryosphaeriaceae
Family. 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 a
virulent 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).
3.5. Biofilters and Biodiesel :
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. Building scientists increasingly recognize that metabolic capabilities of airborne
fungi warrant closer study (Fischer and Dott, 2003 and Vergara-Fernandez et al., 2011).
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
‘‘biodiesel’’ or ‘‘mycodiesel’’ (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 and 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).
3.6. Ecological role of VOCs and interspecies interactions:
Fungi and other microorganisms do not live alone. Rather, they form complex, multispecies networks, alliances, and symbioses. In seeking the chemical basis by which microbes
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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 and in terrestrial habitats; they are
carriers of various aerial signals (Effmert et al., 2012 and Morath et al., 2012).
3.6.1. Enhancement of plant growth:
Fungal VOCs affect plants in many ways. Different volatile species like alcohols, pyrones,
phenols, sesquiterpenes, ketones, and aldehyde emitted by fungi are able to actively modify
plant performance. Many of them are classified as being growth manipulating since they affect
growth and architecture. Others improve plant resistance by activation of plant defense
signaling pathways (Fig. 7) (Wener et al., 2016).
Volatile mixtures emitted from the biocontrol fungus Trichoderma viride 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).
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. Other
fungal endophytes make volatiles that defend against pathogens of their host plants (Strobel et
al., 2011 and Macías-Rubalcava et al., 2010).
Fig. (7): Enhancement of plant growth by fungal VOCs.
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3.6.2. Interaction of fungi with 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 as
shown in fig. 8 (Wheatley, 2002 and 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 ‘‘mycofumigation’’ (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. The VOCs of Oxyporus
latemarginatus, an endophyte isolated from red peppers, also had a negative effect on the
mycelial growth of several plant pathogens (Atmosukarto et al., 2005 and 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 ‘‘mushroom alcohol’’, acts as a selfinhibitor of spore germination in Penicillium paneum (Chitarra et al., 2004 and 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, 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).
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Fig. (8): Fungal VOCs affecting phytopathogenic fungi, bacteria, and soil fauna.
3.6.3. 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 ‘‘semiochemicals’’ or ‘‘infochemicals’’
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. 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. It also serves as an attractant for midges. 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. In another interesting example, fungal volatiles
produced on pine weevil frass protect weevil eggs and affect the pine weevil host-odor search
(George et al., 2013 and Azeem et al, 2015).
3.6.4. Tools used for FVOCs interaction studies:
Simple techniques have been used for the microorganism interaction studies. Among
those, Fernando et al. (2005) used compartmented Petri dishes. Strobel et al. (2001) used a 9
cm Petri dish with cultural medium. One test microorganism is placed on one side, a central
strip of medium is removed and the other tested microorganism is placed on opposite side of
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the dish. Bruce et al. (2003) cultured each microorganism in separate Petri dishes. To set up the
assay, the Petri dish lids were removed, cultured microorganism dishes were inverted over each
other, being the lid one of them, sealed and incubated (Fig. 9).
Fig. (9): Different methods for studying FVOCs interactions with other organisms in vitro.
3.7. Detection indoor and outdoor air quality by microbial VOCs:
Bioaerosols or the biological particles of aerosols are predominantly formed by microbial,
plant and animal origin (Gomez-Domenech et al., 2010). Bioaerosols are ubiquitous in the
environment and due to their small particle size (<2.5 mm) are easily dispersed in the air. Given
the potential high concentration of bioaerosols from urban, agricultural and industrial emissions
(such as composting and other biowaste processing facilities), its impact on local air quality is
of a growing public health concern (Pankhurst et al., 2012). It is well known that the presence
of pathogenic microorganisms in air (bioaerosols) can induce respiratory diseases and
infections including asthma (Connor et al., 2015).
The recent advances in analytical techniques open a new door for the chemical
characterisation of bioaerosol. Specifically, chemical analysis of microbial volatile organic
compounds (MVOCs) can be a reliable and rapid assessment of the nature of ambient
bioaerosols as microbial communities express different MVOCs profiles depending in which
environment they are (Lemfack et al., 2014 and Konouma et al., 2015). Further to this, it has
been shown that species-specific volatiles may serve as marker compounds for the selective
detection of pathogenic microbial species in indoor and outdoor environments. MVOCs are
secondary metabolites produced by fermentation and are volatile due to their physicochemical
properties (low molecular weight, low boiling point and high vapour pressure). Characterizing
and quantifying MVOCs can also be used as a proxy approach to estimate microbial
concentration (Fig. 10) (Schenkel et al., 2015).
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Fig. (10): Schematic representation of different sampling techniques depending on the
downstream analysis required.
3.8. Potential biotechnological applications of fungal VOCs :
Most of the research on fungi and biofuel has focused on finding efficient enzymes for
degrading biomass into fermentable substrates. In addition, fungal VOCs may have
implications for utilization of biologically based energy sources by converting plant waste
directly into diesel (Strobel et al., 2011). VOC production by Ascocoryne sarcoides,
Ascocoryne cylichium and Ascocoryne solitaria, saprophytes isolated from deadwood,
generated VOC profiles including alkanes, alkenes, alcohols, ester, ketones, acids, benzene
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derivatives and terpenes, some of which are similar to biofuel target molecules. Further, many
of the Ascocoryne strains produced sesquiterpenes (Griffin et al., 2010), which are a potential
source of diesel or jet fuel alternatives due to their cyclic and branched nature (Rude and
Schirmer, 2009). The monoterpene 1,8-cineole, an octane derivative, also has potential use as
a fuel additive, as do the other VOCs produced by Hypoxylon sp. (Tomsheck et al., 2010). In
addition to alkanes and long-chain HCs, many fungal species produce other potential biofuel
targets, such as ethylene, ethane, propane and propylene (Ladygina et al., 2006). Some fungi
also produce terpenes and isoprenoids, another diverse family of compounds that may be used
as fuels. In summary, fungi are an excellent platform for exploiting biosynthetic routes to
hydrocarbon biofuels or biofuel precursors (Grigoriev et al., 2011).
It is likely that fungal VOCs are a chemical class with potential biotechnological
applications with greater market value beyond those in the food or agricultural industries.
Available studies have only scratched the surface. Nevertheless, road-blocks remain before
their biotechnological potential can be exploited. Fungal VOCs are produced in small
quantities, making them difficult to characterize and study. Little is known about their
biosynthesis, although genomic, transcriptomic and metabolomic studies are beginning to
correlate gene expression to volatile production. Ultimately, by using genetically modified
fungi with impaired volatile formation, the suite of volatiles that fungi produce under different
culture conditions will be determined. This is an essential step in linking genes to compounds
and to defining the biosynthetic pathways that lead to the production of important compounds.
Because fungal VOCs cannot be used directly as a fuel source, understanding these genetic
pathways is paramount. With this knowledge, the necessary genes can be overexpressed in
producing species or transferred to industrially tractable heterologous hosts for the largescale
production of compounds of human interest (Gianoulis et al., 2012).
For most of the 20th century, fungal bioprospecting has focused on the search for
traditional secondary metabolites with drug value (e.g. penicillin, lovastatin) or for enzymes
with new applications (e.g. biomass degrading enzymes from thermophiles). A concerted
search for new biotechnological products among VOCs will require a paradigm shift in the
scientific community (Morath et al., 2012).
Volatiles represent a new frontier in bioprospecting. When coupled with the power of
“omics” technologies, the study of these gas phase compounds promise the discovery of new
products for human exploitation and will generate new hypotheses in fundamental biology
(Morath et al., 2012).
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Conclusion
4. Conclusion:
In this research, 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.
Also, this research illustrates a positive side of studying VOCs where a lot of researches
showed a negative face of VOCs included a harmful toxicity effect on humans and plants,
pollution of environment and different negative effects. This research observes the positive face
includes plant growth promotion, biocontrol; also a magic face includes chemotaxonomy that
facilitates taxonomy and identification of fungi and considered an important healthy status
indicator instead of biopsy and other difficult tools for taking the specimen. Finally, FVOCs are
considered a magic, signature and fingerprinting tool used for different applications and solving
different problems.
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