-
Food Chemistry 141 (2013) 2952–2959
Contents lists available at SciVerse ScienceDirect
Food Chemistry
journal homepage: www.elsevier .com/locate / foodchem
Formation of complex natural flavours by biotransformation of
applepomace with basidiomycetes
0308-8146/$ - see front matter � 2013 Elsevier Ltd. All rights
reserved.http://dx.doi.org/10.1016/j.foodchem.2013.05.116
⇑ Corresponding author. Tel.: +49 (0) 641 99 34 900; fax: +49
(0) 641 99 34 909.E-mail address:
[email protected] (H. Zorn).
Andrea K. Bosse, Marco A. Fraatz, Holger Zorn ⇑Justus Liebig
University Giessen, Institute of Food Chemistry and Food
Biotechnology, Heinrich-Buff-Ring 58, 35392 Giessen, Germany
a r t i c l e i n f o
Article history:Received 2 April 2013Received in revised form 23
May 2013Accepted 27 May 2013Available online 5 June 2013
Keywords:BasidiomycetesApple pomaceBiotransformationTyromyces
chioneus3-Phenylpropanal
a b s t r a c t
Altogether 30 different basidiomycetes were grown submerged in
liquid culture media using seven dif-ferent by-products of the food
industry as the only carbon source. Seven fungus/substrate
combinationsrevealed interesting flavour profiles. Culture
supernatants of Tyromyces chioneus grown on apple pomacewere
extracted, and the aroma compounds were analysed by gas
chromatography–olfactometry (GC–O).Potent odorants were identified
by aroma extract dilution analysis (AEDA), calculation of the odour
activ-ity values (OAV), and proven by confection of an aroma model.
3-Phenylpropanal, 3-phenyl-1-propanol,and benzyl alcohol were
identified as potent aroma biotransformation products. Headspace
solid-phasemicroextraction gas chromatography mass spectrometry
(HS-SPME–GC–MS) experiments showed that3-phenylpropanal,
3-phenyl-1-propanol, benzyl alcohol, methyl 3-phenylpropionate,
methyl 2-phenylac-etate, cinnamaldehyde and methyl cinnamate were
produced during the cultivation period of eight days.By means of
labelling experiments, (E)-cinnamic acid was identified as the
precursor of 3-phenylpropanaland 3-phenyl-1-propanol.
Basidiomycetes were able to biotransform food by-products to
pleasant com-plex flavour mixtures.
� 2013 Elsevier Ltd. All rights reserved.
1. Introduction
The industrial demand for natural flavours is
constantlyincreasing (Guentert, 2007). Concurrently, the volume of
availableby-products of the food industry is growing, as food
products aremore and more processed and ready-made. Many
by-products con-tain valuable components, such as lipids or amino
acids, whichmay act as biogenetic precursors of flavour compounds.
Article3.2(c) of the Regulation (EC), No 1334/2008 considers a
‘‘naturalflavouring substance’’ as ‘‘a flavouring substance
obtained byappropriate physical, enzymatic or microbiological
processes frommaterial of vegetable, animal or microbiological
origin, either inthe raw state or after processing for human
consumption by oneor more of the traditional food preparation
processes listed in An-nex II. Natural flavouring substances
correspond to the substancesthat are naturally present and have
been identified in nature’’. Fer-mentation of by-products of the
food industry with traditionalstarter cultures is not very
promising, as e.g., yeasts of the genusSaccharomyces form many, but
barely complex and intense flavourcompounds (Carrau et al.,
2008).
Basidiomycetes, which comprise almost all edible
mushrooms,possess a unique extracellular enzyme system (the
so-called secre-tome) and have already been shown to produce
bioflavours de novo
as well as by biotransformation (Bouws, Wattenberg, & Zorn,
2008;Fraatz & Zorn, 2010). De-novo-produced flavour compounds
ofbasidiomycetes are chemically identical to flavour substances
iso-lated from plants. Pleurotus sapidus for example was able to
trans-form the sesquiterpene hydrocarbon valencene into the
grapefruitflavour nootkatone (Fraatz et al., 2009).
In 2010, 69.6 million tons of apples were produced
worldwide(Food and Agriculture Organization, 2012). 25-30% Were
pro-cessed to juice, cider, and frozen or dried products. Apple
juiceconcentrate represents the major processed product, with a
totalrecovery of 70-75% in the industrial process. Therefore,
25-30% ofapple pomace remains as a side-stream (Bhushan, Kalia,
Sharma,Singh, & Ahuja, 2008). In Germany, approximately 800 kt
of ap-ples are processed to apple juice annually, and 200 kt of
applepomace accrue (Binnig, 2001). These by-products do not
onlycause disposal costs, but also are a major environmental
problem(Bhushan et al., 2008). Currently, they are used as feed (50
kt), forthe production of biogas (50 kt), and for the isolation of
pectin(100 kt) (Binnig, 2001).
Apple pomace has also been suggested for the extraction of
die-tary fibres, proteins, natural antioxidants, biopolymers and
pig-ments (Bhushan et al., 2008). Furthermore, it may be
employedfor the production of enzymes, organic acids, ethanol,
single cellproteins (Bhushan et al., 2008), edible mushrooms, feeds
(Vendrus-colo, Albuquerque, Streit, Esposito, & Ninow, 2008),
and aromacompounds (Bramorski, Soccol, Christen, & Revah,
1998).
http://crossmark.dyndns.org/dialog/?doi=10.1016/j.foodchem.2013.05.116&domain=pdfhttp://dx.doi.org/10.1016/j.foodchem.2013.05.116mailto:[email protected]://dx.doi.org/10.1016/j.foodchem.2013.05.116http://www.sciencedirect.com/science/journal/03088146http://www.elsevier.com/locate/foodchem
-
A.K. Bosse et al. / Food Chemistry 141 (2013) 2952–2959 2953
In the present study, the ability of basidiomycetes to
transformby-products of the food industry to complex flavour
mixtures wasinvestigated. The well-known concept of fermentative
flavour pro-duction by traditional food biotechnology was
translated to thecultivation of the biochemically complex
basidiomycetes. Cultureswere extracted by liquid/liquid extraction
as well as by headspacesolid-phase microextraction coupled to gas
chromatography massspectrometry (HS-SPME–GC/MS). The flavour
profiles of theliquid/liquid extracts were investigated by aroma
extract dilutionanalysis (AEDA), and the odour activity values
(OAVs) werecalculated.
2. Materials and methods
2.1. Microorganisms
The fungi were obtained from the German Collection
ofMicroorganisms and Cell Cultures (DSMZ, Brunswick, Germany)and
the Centraalbureau voor Schimmelcultures (CBS, Utrecht,
TheNetherlands).
2.2. Substrates
The by-products apple pomace, broken waffle, broken cake, co-coa
shells, cocoa powder, coffee grounds, and wine pomace
(Gewü-rztraminer) were received from different industrial partners
andwere used as substrates for submerged cultivation.
2.3. Chemicals
Solvents were purchased from Fisher Scientific (Schwerte,
Ger-many) and Carl Roth (Karlsruhe, Germany). All solvents were
dis-tilled before use. High-purity water was prepared with
alaboratory water system (Sartorius, Goettingen, Germany).
Sodiumchloride and benzyl alcohol were obtained from
AppliChem(Darmstadt, Germany). 3-Phenylpropanol,
3-phenylpropanal,BME Vitamins 100� solution, benzaldehyde,
(E)-D7-cinnamic acid,a-farnesene and (E)-D7-cinnamic acid were
purchased from Sig-ma–Aldrich (Taufkirchen, Germany),
1H-pyrrole-2-carboxalde-hyde and (E)-cinnamic acid from Acros
Organics (Geel, Belgium),and acetic acid, sodium sulfate and thymol
from Carl Roth. Allchemicals were of analytical grade.
2.4. Submerged cultures
Apple pomace, broken waffle, broken cake, cocoa shells,
cocoapowder, coffee ground and wine pomace (Gewürztraminer)
wereused as substrates for the submerged cultures and were stored
at�20 �C prior to usage. Cocoa powder, cocoa shells and wine
pom-ace were used untreated. Apple pomace, broken waffle,
brokencake and coffee ground were freeze dried (�25 �C, 0.63 mbar,4
days, moisture content
-
Fig. 1. Flow chart of the screening of fungi and by-products for
flavour production.
2954 A.K. Bosse et al. / Food Chemistry 141 (2013) 2952–2959
OAV: Odor activity valuesc: concentration of the odorant [lg
L�1]a:odour threshold in water [lg L�1]
2.9. Aroma model of the flavour extracts
As a matrix for the recombination experiments
pentane/diethylether (1/1.12 v/v) was selected. The recombinate was
composedaccording to the determined concentrations of the odorants
benz-aldehyde, 3-phenylpropanal, 3-phenylpropanol, and benzyl
alco-hol. One millilitre of the aroma model was transferred
intoamber glass vials with a screw-cap, containing a piece of
scentlessfilter paper. This model was compared to the flavour
extracts ob-tained by the biotransformation of apple pomace by T.
chioneusand evaluated by 5 skilled persons. The intensity was
determinedas described in Section 2.5.
2.10. Determination of odour threshold values
Odour threshold values were determined in water.
3-Phenyl-propanal and 3-phenylpropanol were dissolved in ethanol
andthen diluted with water. The water/ethanol mixture was testedfor
lack of odour. The samples were analysed in order of
increasingconcentrations in 1:1 dilution steps, and the odour
threshold of thetest groups was calculated from the quadratic mean
of the individ-ual odour thresholds according to § 64 (Amtliche
Methoden 1999,2007) LFGB methods volume I (L) L 00.09–7 and L
00.09–9.
2.11. Capillary gas chromatography–mass spectrometry (GC/MS)
2.11.1. GC–MS after liquid/liquid extractionHigh resolution
GC–MS was conducted on an Agilent 7890A gas
chromatograph equipped with an Agilent 5975C MSD
triple-axisdetector. Agilent Technologies J&W Scientific
HP-Innowax(0.25 lm film thickness, 30 m � 0.25 mm i.d.) and Agilent
Technol-ogies DB-5MS columns (30 m � 0.25 mm i.d., 0.25 lm film
thick-ness), and a split/splitless injector (250 �C, split 1:10)
were used.The following temperature programs were employed: 40
�C
(3 min), 5 �C min�1 to 240 �C (12 min) (polar column), and 40
�C(3 min), 5 �C min�1 to 240 �C (12 min), 20 �C min�1 to 300 �C(7
min) (non-polar column).
Helium was used as carrier gas (1.2 mL min�1, constant flow).The
ion source was set to 230 �C, the interface to 250 �C, and
thequadrupole to 150 �C. The electron impact energy was 70 eV.
Sys-tem software, data management, and analysis were controlled
byChemStation (E.02.00.493).
Compounds were identified by comparison of their mass spec-tra
with those of authentic standards and to the database NIST2008 MS
LIB. The concentrations were estimated by the internalstandard
method, using thymol as internal standard. The responsefactor (Rf)
was calculated for each analyte according to the follow-ing
equation:
Rf ¼ AIS �mamIS � Aa
ð2Þ
where A = peak area, m = mass (lg), IS = internal standard,a =
analyte.
2.11.2. HS-SPME–GC–MSHS-SPME analyses were performed with a
split/splitless injector
(250 �C, splitless time: 5 min) using an Agilent Technologies
J&WScientific HP-Innowax column (30 m � 0.25 mm i.d., 0.25 lm
filmthickness) under the conditions described above. Compounds
wereidentified by comparison of their mass spectra with those of
thedatabase NIST 2008 MS LIB and were confirmed by calculation
oftheir respective Kováts indices.
3. Results and discussion
3.1. Screening
In a broad screening, 30 different basidiomycetes were grownon
seven different by-products of the food industry (Fig. 1).
Alto-gether, seven fungus/substrate combinations imparted
interestingflavour impressions (Fig. 1). Due to the intense and
unique flavour,
-
Fig. 2. (I) GC/FID/O chromatogram of the biotransformation of
apple pomace by T. chioneus (day 4) with FID (black) and ODP signal
(red); ⁄internal standard and (II) potentodorants (flavor dilution
chromatogram) formed during the biotransformation. (For
interpretation of the references to colour in this figure legend,
the reader is referred to theweb version of this article.)
A.K. Bosse et al. / Food Chemistry 141 (2013) 2952–2959 2955
the cultures of T. chioneus grown on freeze-dried apple pomace
assubstrate were chosen for further analysis.
After four days, these cultures emitted an odour reminiscent
ofstewed fruit, sweetish and plum purée. The olfactory
impressionsof the corresponding blanks of T. chioneus and of
lyophilised applepomace differed significantly from those of the
biotransformations.The blank cultures of T. chioneus smelled
sweetish and musty,while the substrate blanks smelled like apples
and freshly-squeezed apple pomace.
3.2. Flavour analysis
Fourteen flavour compounds were detected by means of GC–Oin the
liquid/liquid extracts in two independent runs (Fig. 2).
Sevencompounds were identified by comparison of Kováts indices
andmass spectra with those in the database (NIST 2008 MS LIB)
and
confirmed by authentic standards on a polar and a non-polar
GCcolumn. FD-factors were determined by AEDA (Fig. 2; Table
1).3-Phenylpropanal (FD-factor 128; OAV 94) was identified as
themost potent odorant (Table 2). The odour of 3-phenylpropanalhas
been described as ‘‘green and flowery’’ (Ranson & Belitz,1992).
Apart from 3-phenyl-1-propanol (FD-factor 8, OAV 30),benzyl alcohol
(FD-factor 32, OAV 17) contributed significantly tothe overall
flavour of the cultures. Benzyl alcohol exhibits a floweryand
fruity flavour (Fang & Qian, 2005). The influence of acetic
acidwith an OAV smaller than one was negligible.
3-Phenylpropanal,benzyl alcohol, and 3-phenyl-1-propanol were
formed bybiotransformation and shaped the sweetish,
plum-purée-likeflavour. While 3-phenyl-1-propanol and benzyl
alcohol are wellknown basidiomycetes biotransformation products,
3-phenylprop-anal has not been reported as a flavour compound
formed bybasidiomycetes yet. The basidiomycete Bjerkandera
adusta
-
Table 1Volatile flavour compounds of the biotransformation of
apple pomace by T. chioneus with FD-factors and Kováts indices (KI)
in increasing elution order on an HP-Innowax column.
No. Compounda Odor descriptionb KI GC-OHP-Innowax
KI GC-MSHP-Innowax
KI GC–MS DB5-MS
FD-factor
1 n.i. Sweetish fruity 912 22 Acetic acid Vinegar 1447 1465
-
Fig. 3. (A) Formation of phenylpropanoic and benzoic volatile
compounds in the biotransformation of apple pomace by T. chioneus
during the cultivation period of 8 days. (B)Formation of minor
compounds.
A.K. Bosse et al. / Food Chemistry 141 (2013) 2952–2959 2957
Furthermore, methyl 3-phenylpropionate, methyl
2-phenylacetate,cinnamaldehyde, and methyl cinnamate were detected.
Methyl 3-phenylpropionate was found in cooked pine mushrooms
andmethyl 2-phenylacetate in the hydrodistillates of the
basidiomy-cete Gloeophyllum odoratum (Cho, Choi, & Kim, 2006;
Rösecke &König, 2000). Cinnamaldehyde contributed to the
pungent andspicy flavour of the medicinal mushroom Hericium
erinaceus (pompom mushroom) (Abraham & Berger, 1994). In the
culture brothsof Lenzites frabea, Poria subvermispora,
Hirschioporus pergamenus,Poria subacida, and Vararia effuscata, up
to 250 lg L-1 methyl cinna-mate were found, depending on the media
composition (Gallois,Gross, Langlois, Spinnler, & Brunerie,
1990).
3.4. Cinnamic acid as a precursor of 3-phenylpropanal
and3-phenylpropanol
To identify the precursor and to elucidate the biogenetic
path-way of 3-phenylpropanal and 3-phenyl-1-propanol,
(E)-cinnamicacid and (E)-D7-cinnamic acid (1 mM) were added to the
culturemedia of T. chioneus. The culture supernatants were
extracted bymeans of liquid/liquid extraction and analysed by
GC–MS. Themass spectra were compared to the mass spectra of
authenticstandards.
The addition of (E)-cinnamic acid led to a ten times
increasedformation of 3-phenylpropanal and 3-phenyl-1-propanol
(Fig. 4).Additionally, 2-phenyl-1-ethanol, maltol and
cinnamaldehydewere detected in these cultures. In oven-dried apple
pomace,�180 mg kg�1 cinnamic acid was detected (Bai, Yue, Yuan,
&Zhang, 2010). This represents a sufficient amount to explain
theformation of the C6–C3 biotransformation products. To
elucidatethe potential role of L-phenylalanine as an additional
precursor of3-phenylpropanal and 3-phenyl-1-propanol, 10 mM of
l-phenylal-
anine were added to the culture media of T. chioneus. In
contrast tothe addition of (E)-cinnamic acid, no enhanced formation
of 3-phe-nylpropanal and 3-phenyl-1-propanol was observed in the
corre-sponding cultures.
The mass spectrum of 3-phenylpropanal after supplementationwith
(E)-D7-cinnamic acid showed an intensive molecular ions(M+�) at m/z
140 and 141 compared to the non-labelled referencecompound with an
M+� at m/z 134 (Fig. 4). The ratio of analyte Ato the labelled
analyte Ad6+d7 was 40/757, which represented a pro-portion of
labelled 3-phenylpropanal of 95%. This confirmed thereduction of
cinnamic acid to 3-phenylpropanal. The massspectrum of
3-phenyl-1-propanol after supplementation with(E)-D7-cinnamic acid
revealed an intense M+� at m/z 142 and 143.compared to the
non-labelled molecule with an M+� at m/z 136.The ratio of A to
Ad6+d7 was 5/294, which indicated 98% labelled3-phenyl-1-propanol.
Likewise, 3-phenyl-1-propanol was thebiotransformation product of
cinnamic acid.
The carboxyl group of (E)-cinnamic acid was reduced to
cinna-maldehyde. The Ca–Cb double bound was hydrogenated, and
thealdehyde was subsequently reduced to the corresponding
alcohol.All of the metabolites of the postulated pathway were
detected inthe cultures supplemented with (E)-cinnamic acid. A
similar bio-synthetic pathway from cinnamic acid via cinnamaldehyde
andcinnamic alcohol to 3-phenyl-1-propanol was presumed in thewhite
rot mushroom Schizophyllum commune (Nimura et al.,2010).
This reaction pathway is commonly catalysed by two classes
ofenzymes: aldehyde oxidoreductases and alcohol dehydrogenases(Van
den Ban et al., 1999). The reduction of aromatic acids andthe
release of aldehydes by the breakdown of lignin has alreadybeen
reported (Hage, Schoemaker, & Field, 1999). Numerous whiterot
mushrooms are able to reduce aryl acids to the corresponding
-
Fig. 4. (I) Concentrations of the biotransformation products of
apple pomace by T.chioneus supplemented with (E)-cinnamic acid
compared to the cultures withoutaddition of cinnamic acid, and (II)
mass spectrum of 3-phenylpropanal aftersupplementation of
(E)-D7-cinnamic acid (1 mM) as a precursor to the
biotransfor-mation of apple pomace by T. chioneus (B) in comparison
to the mass spectrum ofthe non-labelled standard 3-phenylpropanal
(A).
2958 A.K. Bosse et al. / Food Chemistry 141 (2013) 2952–2959
aldehydes and alcohols. The reduction of the aldehyde to the
alco-hol is catalysed by the NADPH-dependent enzyme aryl
alcoholdehydrogenase. The aryl alcohols serve as substrates for the
extra-cellular enzyme aryl alcohol oxidase (AAO), which produces
theH2O2 required for peroxidase activity (Hage et al., 1999).
Oxidative enzymes of white rot mushrooms have been
studiedintensely. On the other hand, only little is known about
reductiveenzymes. Up to now, a number of quinone reductases
wereidentified, like 1,4-benzoquinone reductase, which reduces
qui-nones to hydroquinones by a ping-pong steady state (Brock &
Gold,1996). A xylose reductase was identified in the fungus
Cryptococcusflavus, which can reduce d-xylose NADPH dependent to
xylitol(Mayr, Petschacher, & Nidetzky, 2003). A
membrane-associatedactivity of an aromatic nitroreductase was found
in extracts ofPhanerochaete chrysosporium. The extracts reduced the
nitrogroups of 1,3-dinitrobenzene, 2,4-dinitrotoluene,
2,4,6-trinitrotolu-ene, 1-chloro-2,4-dinitrobenzene, and
2,4-dichloro-1-nitrobenzene(Rieble, Joshi, & Gold, 1994).
An aldehyde oxidoreductase has not been isolated from
basidi-omycetes yet. Li and Rosazza (1997) purified and
characterized a163 ± 3.8 kDa aldehyde oxidoreductase from the
gram-negativebacterium Nocardia sp. NRRL 5646, which was able to
reduce arylcarboxylic acids, including substituted benzoic acids,
phenyl-substituted aliphatic acids, heterocyclic carboxylic acids,
and poly-aromatic ring carboxylic acids to the corresponding
aldehydes.
4. Conclusions
A pleasant flavour mixture reminiscent of stewed fruit andplum
purée was generated by the biotransformation of apple pom-ace using
submerged cultures of the basidiomycete T. chioneus
after four days. Fourteen flavour compounds were detected byGC–O
in the liquid/liquid extracts of the culture media. Seven
com-pounds were identified (acetic acid, benzaldehyde, a-farnesene,
3-phenylpropanal, benzyl alcohol, 1H-pyrrole-2-carboxaldehyde
and3-phenyl-1-propanol). The biotransformation products
3-phenyl-propanal, 3-phenyl-1-propanol, and benzyl alcohol were
identifiedas the most potent biotransformation products.
HS-SPME–GC–MSanalyses of the culture broths over the cultivation
period of eightdays revealed that a-farnesene, benzaldehyde and
linalool werepartially degraded, while 3-phenylpropanal,
3-phenyl-1-propanol,benzyl alcohol, methyl 3-phenylpropionate,
methyl 2-phenylace-tate, cinnamaldehyde, and methyl cinnamate were
formed. (E)-Cinnamic acid was identified as the precursor of
3-phenylpropanaland 3-phenyl-1-propanol. Basidiomycetes
successfully trans-formed by-products of the food industry to
complex and highlyinteresting natural flavour mixtures.
Acknowledgements
The authors thank the FEI (Forschungskreis der
Ernährungsin-dustrie e.V.) and AiF (Arbeitsgemeinschaft
industrieller Fors-chungsvereinigungen ‘‘Otto von Guericke’’) for
funding theresearch project AiF 299 ZN and Katja Fast for her
support in theolfactometric evaluation. Part of the work was
supported by theexcellence initiative of the Hessian Ministry of
Science and Artwhich encompasses a generous grant for the LOEWE
research focus‘integrative fungal research’’.
References
Abraham, B. G., & Berger, R. G. (1994). Higher fungi for
generating aromacomponents through novel biotechnologies. Journal
of Agricultural and FoodChemistry, 42(10), 2344–2348.
Amtliche Methoden für die Untersuchung von LebensmittelnAmtliche
Sammlungvon Untersuchungsverfahren nach § 64 LFGB (vormals § 35
LMBG), Band I (L), L00.90-9: Sensorische Prüfverfahren - Bestimmung
derGeschmacksempfindlichkeit (Übernahme der gleichnamigen Deutschen
NormDIN 10959, Ausgabe Juli 1998). Ausgabedatum: 1999–11.
Amtliche Methoden für die Untersuchung von LebensmittelnAmtliche
Sammlungvon Untersuchungsverfahren nach § 64 LFGB (vormals § 35
LMBG), Band I (L), L00.90-7: Untersuchung von Lebensmitteln -
Sensorische Prüfverfahren –Dreiecksprüfung (Übernahme der
gleichnamigen Deutschen Norm DIN EN ISO4120, Ausgabe Oktober 2007).
Ausgabedatum: 2007–12.
Bai, X.-L., Yue, T.-L., Yuan, Y.-H., & Zhang, H.-W. (2010).
Optimization of microwave-assisted extraction of polyphenols from
apple pomace using response surfacemethodology and HPLC analysis.
Journal of Separation Science, 33(23–24),3751–3758.
Bhushan, S., Kalia, K., Sharma, M., Singh, B., & Ahuja, P.
S. (2008). Processing of applepomace for bioactive molecules.
Critical Reviews in Biotechnology, 28(4),285–296.
Binnig, R. (2001). Die Möglichkeiten der Verwertung von Trestern
aus der Fruchtsaft-Herstellung (insbesondere am Beispiel Apfel): 2.
Überarbeitete und (erweiterteAuflage). Trier / Bonn: Verband der
deutschen Fruchtsaft-Industrie e. V.
Bouws, H., Wattenberg, A., & Zorn, H. (2008). Fungal
secretomes—Nature’s toolboxfor white biotechnology. Applied
Microbiology and Biotechnology, 80(3),381–388.
Bramorski, A., Soccol, C. R., Christen, P., & Revah, S.
(1998). Fruity aroma productionby Ceratocystis fimbriata in solid
cultures from agro-industrial wastes. Revista deMicrobiologia,
29(3), 208–212.
Brock, B. J., & Gold, M. H. (1996). 1,4-Benzoquinone
reductase from basidiomycetePhanerochaete chrysosporium: Spectral
and kinetic analysis. Archives ofBiochemistry and Biophysics,
331(1), 31–40.
Carrau, F. M., Medina, K., Farina, L., Boido, E., Henschke, P.
A., & Dellacassa, E. (2008).Production of fermentation aroma
compounds by Saccharomyces cerevisiae wineyeasts: effects of yeast
assimilable nitrogen on two model strains. FEMS YeastResearch,
8(7), 1196–1207.
Cho, H., Choi, H.-K., & Kim, Y.-S. (2006). Difference in the
volatile composition ofpine-mushrooms (Tricholoma matsutake Sing.)
according to their grades. Journalof Agricultural and Food
Chemistry, 54(13), 4820–4825.
Fang, Y., & Qian, M. (2005). Aroma compounds in Oregon Pinot
Noir winedetermined by aroma extract dilution analysis (AEDA).
Flavour and FragranceJournal, 20(1), 22–29.
Food and Agriculture Organization. (2012). FAOSTAT-Production
(tonnes) apples: FAOstatistical databases. Retrieved from .
Fraatz, M. A., Riemer, S. J. L., Stöber, R., Kaspera, R., Nimtz,
M., Berger, R. G.,et al. (2009). A novel oxygenase from Pleurotus
sapidus transforms
http://refhub.elsevier.com/S0308-8146(13)00722-X/h0005http://refhub.elsevier.com/S0308-8146(13)00722-X/h0005http://refhub.elsevier.com/S0308-8146(13)00722-X/h0005http://refhub.elsevier.com/S0308-8146(13)00722-X/h0010http://refhub.elsevier.com/S0308-8146(13)00722-X/h0010http://refhub.elsevier.com/S0308-8146(13)00722-X/h0010http://refhub.elsevier.com/S0308-8146(13)00722-X/h0010http://refhub.elsevier.com/S0308-8146(13)00722-X/h0015http://refhub.elsevier.com/S0308-8146(13)00722-X/h0015http://refhub.elsevier.com/S0308-8146(13)00722-X/h0015http://refhub.elsevier.com/S0308-8146(13)00722-X/h0020http://refhub.elsevier.com/S0308-8146(13)00722-X/h0020http://refhub.elsevier.com/S0308-8146(13)00722-X/h0020http://refhub.elsevier.com/S0308-8146(13)00722-X/h0025http://refhub.elsevier.com/S0308-8146(13)00722-X/h0025http://refhub.elsevier.com/S0308-8146(13)00722-X/h0025http://refhub.elsevier.com/S0308-8146(13)00722-X/h0030http://refhub.elsevier.com/S0308-8146(13)00722-X/h0030http://refhub.elsevier.com/S0308-8146(13)00722-X/h0030http://refhub.elsevier.com/S0308-8146(13)00722-X/h0035http://refhub.elsevier.com/S0308-8146(13)00722-X/h0035http://refhub.elsevier.com/S0308-8146(13)00722-X/h0035http://refhub.elsevier.com/S0308-8146(13)00722-X/h0040http://refhub.elsevier.com/S0308-8146(13)00722-X/h0040http://refhub.elsevier.com/S0308-8146(13)00722-X/h0040http://refhub.elsevier.com/S0308-8146(13)00722-X/h0040http://refhub.elsevier.com/S0308-8146(13)00722-X/h0045http://refhub.elsevier.com/S0308-8146(13)00722-X/h0045http://refhub.elsevier.com/S0308-8146(13)00722-X/h0045http://refhub.elsevier.com/S0308-8146(13)00722-X/h0050http://refhub.elsevier.com/S0308-8146(13)00722-X/h0050http://refhub.elsevier.com/S0308-8146(13)00722-X/h0050http://faostat.fao.org/site/567/DesktopDefault.aspx?PageID=567#ancorhttp://faostat.fao.org/site/567/DesktopDefault.aspx?PageID=567#ancorhttp://refhub.elsevier.com/S0308-8146(13)00722-X/h0055http://refhub.elsevier.com/S0308-8146(13)00722-X/h0055
-
A.K. Bosse et al. / Food Chemistry 141 (2013) 2952–2959 2959
valencene to nootkatone. Journal of Molecular Catalysis B:
Enzymatic, 61(3–4), 202–207.
Fraatz, M. A., & Zorn, H. (2010). Fungal flavours:
Industrial applications. In M.Hofrichter (Ed.), The mycota (pp.
249–268). Berlin, Heidelberg: Springer.
Gallois, A., Gross, B., Langlois, D., Spinnler, H.-E., &
Brunerie, P. (1990). Influence ofculture conditions on production
of flavour compounds by 29 ligninolyticbasidiomycetes. Mycological
Research, 94(4), 494–504.
Grosch, W. (1994). Determination of potent odourants in foods by
aroma extractdilution analysis (AEDA) and calculation of odour
activity values (OAVs). Flavourand Fragrance Journal, 9(4),
147–158.
Guentert, M. (2007). The flavour and fragrance industry—Past,
present, and future.In R.G. Berger (Ed.),Flavours and Fragrances
(pp. 1–14). Springer BerlinHeidelberg.
Hage, A., Schoemaker, H. E., & Field, J. A. (1999).
Reduction of aryl acids by white-rotfungi for the biocatalytic
production of aryl aldehydes and alcohols. AppliedMicrobiology and
Biotechnology, 52(6), 834–838.
Kováts, E. (1958). Gas-chromatographische charakterisierung
organischerverbindungen. Teil 1: Retentionsindices aliphatischer
halogenide, alkohole,aldehyde und ketone. Helvetica Chimica Acta,
41(7), 1915–1932.
Krings, U., Hinz, M., & Berger, R. G. (1996). Degradation of
[2H]phenylalanine by thebasidiomycete Ischnoderma benzoinum.
Critical Reviews in Food Science andNutrition, 51(2), 123–129.
Lapadatescu, C., Giniès, C., Le Quéré, J. L., & Bonnarme, P.
(2000). Novel scheme forbiosynthesis of aryl metabolites from
L-phenylalanine in the fungus Bjerkanderaadusta. Applied and
environmental microbiology, 66(4), 1517–1522.
Li, T., & Rosazza, J. P. (1997). Purification,
characterization, and properties of an arylaldehyde oxidoreductase
from Nocardia sp. strain NRRL 5646. Journal ofBacteriology,
179(11), 3482–3487.
Madrera, R. R., & Valles, B. S. (2011). Determination of
volatile compounds in applepomace by stir bar sorptive extraction
and gas chromatography–massspectrometry (SBSE–GC–MS). Journal of
Food Science, 76(9), C1326.
Mayr, P., Petschacher, B., & Nidetzky, B. (2003). Xylose
reductase from thebasidiomycete fungus Cryptococcus flavus:
Purification, steady-state kineticcharacterization, and detailed
analysis of the substrate binding pocket usingstructure–activity
relationships. Journal of biochemistry, 133(4), 553–562.
Nimura, Y., Tsujiyama, S.-I, & Ueno, M. (2010).
Bioconversion of cinnamic acidderivatives by Schizophyllum commune.
Journal of General and AppliedMicrobiology, 56(5), 381–387.
Regulation (EC) No 1334/2008 of the European Parliament and of
the Council of16 December 2008 on flavourings and certain food
ingredients with flavouringproperties for use in and on foods and
amending Council Regulation (EEC) No1601/91, Regulations (EC) No
2232/96 and (EC) No 110/2008 and Directive2000/13/EC (Text with EEA
relevance) Official Journal of the European Union 34,European
Parliament and Council 16.12.2008.
Rieble, S., Joshi, D. K., & Gold, M. H. (1994). Aromatic
nitroreductase from thebasidiomycete Phanerochaete chrysosporium.
Biochemical and BiophysicalResearch Communications, 205(1),
298–304.
Rösecke, J., & König, W. A. (2000). Odorous compounds from
the fungusGloeophyllum odoratum. Flavour and Fragrance Journal,
15(5), 315–319.
Rychlik, M., Schieberle, P., & Grosch, W. (1998).
Compilation of odor thresholds, odorqualities and retention indices
of key food odorants. Garching, Germany, Garching,Germany: Dt.
Forschungsanst. für Lebensmittelchemie; Inst.
fürLebensmittelchemie.
Valim, M. F., Rouseff, R. L., & Lin, J. (2003). Gas
chromatographic–olfactometriccharacterization of aroma compounds in
two types of cashew apple nectar.Journal of Agricultural and Food
Chemistry, 51(4), 1010–1015.
van den Ban, E. C. D., Willemen, H. M., Wassink, H., Laane, C.,
& Haaker, H. (1999).Bioreduction of carboxylic acids by
Pyrococcus furiosus in batch cultures. Enzymeand Microbial
Technology, 25(3–5), 251–257.
Vendruscolo, F., Albuquerque, P. M., Streit, F., Esposito, E.,
& Ninow, J. L. (2008).Apple pomace: A versatile substrate for
biotechnological applications. CriticalReviews in Biotechnology,
28(1), 1–12.
von Ranson, C., & Belitz, H.-D. (1992). Untersuchungen zur
Struktur-Aktivitätsbeziehung bei Geruchsstoffen: 3. Mitteilung:
Wahrnehmungs- underkennungsschwellenwerte sowie geruchsqualitiiten
alicyclischer undaromatischer aldehyde. Zeitschrift für
Lebensmitteluntersuchung und -ForschungA, 195(6), 523–526.
Whitaker, B. D., Solomos, T., & Harrison, D. J. (1997).
Quantification of a-farneseneand its conjugated trienol oxidation
products from apple peel by C18-HPLC withUV detection. Journal of
Agricultural and Food Chemistry, 45(3), 760–765.
Yang, C., Luo, L., Zhang, H., Yang, X., Lv, Y., & Song, H.
(2010). Common aroma-activecomponents of propolis from 23 regions
of China. Journal of the Science ofAgriculture, 90(7),
1268–1282.
http://refhub.elsevier.com/S0308-8146(13)00722-X/h0055http://refhub.elsevier.com/S0308-8146(13)00722-X/h0055http://refhub.elsevier.com/S0308-8146(13)00722-X/h0060http://refhub.elsevier.com/S0308-8146(13)00722-X/h0060http://refhub.elsevier.com/S0308-8146(13)00722-X/h0065http://refhub.elsevier.com/S0308-8146(13)00722-X/h0065http://refhub.elsevier.com/S0308-8146(13)00722-X/h0065http://refhub.elsevier.com/S0308-8146(13)00722-X/h0070http://refhub.elsevier.com/S0308-8146(13)00722-X/h0070http://refhub.elsevier.com/S0308-8146(13)00722-X/h0070http://refhub.elsevier.com/S0308-8146(13)00722-X/h0075http://refhub.elsevier.com/S0308-8146(13)00722-X/h0075http://refhub.elsevier.com/S0308-8146(13)00722-X/h0075http://refhub.elsevier.com/S0308-8146(13)00722-X/h0080http://refhub.elsevier.com/S0308-8146(13)00722-X/h0080http://refhub.elsevier.com/S0308-8146(13)00722-X/h0080http://refhub.elsevier.com/S0308-8146(13)00722-X/h0085http://refhub.elsevier.com/S0308-8146(13)00722-X/h0085http://refhub.elsevier.com/S0308-8146(13)00722-X/h0085http://refhub.elsevier.com/S0308-8146(13)00722-X/h0085http://refhub.elsevier.com/S0308-8146(13)00722-X/h0090http://refhub.elsevier.com/S0308-8146(13)00722-X/h0090http://refhub.elsevier.com/S0308-8146(13)00722-X/h0090http://refhub.elsevier.com/S0308-8146(13)00722-X/h0090http://refhub.elsevier.com/S0308-8146(13)00722-X/h0090http://refhub.elsevier.com/S0308-8146(13)00722-X/h0095http://refhub.elsevier.com/S0308-8146(13)00722-X/h0095http://refhub.elsevier.com/S0308-8146(13)00722-X/h0095http://refhub.elsevier.com/S0308-8146(13)00722-X/h0100http://refhub.elsevier.com/S0308-8146(13)00722-X/h0100http://refhub.elsevier.com/S0308-8146(13)00722-X/h0100http://refhub.elsevier.com/S0308-8146(13)00722-X/h0105http://refhub.elsevier.com/S0308-8146(13)00722-X/h0105http://refhub.elsevier.com/S0308-8146(13)00722-X/h0105http://refhub.elsevier.com/S0308-8146(13)00722-X/h0105http://refhub.elsevier.com/S0308-8146(13)00722-X/h0110http://refhub.elsevier.com/S0308-8146(13)00722-X/h0110http://refhub.elsevier.com/S0308-8146(13)00722-X/h0110http://refhub.elsevier.com/S0308-8146(13)00722-X/h0115http://refhub.elsevier.com/S0308-8146(13)00722-X/h0115http://refhub.elsevier.com/S0308-8146(13)00722-X/h0115http://refhub.elsevier.com/S0308-8146(13)00722-X/h0120http://refhub.elsevier.com/S0308-8146(13)00722-X/h0120http://refhub.elsevier.com/S0308-8146(13)00722-X/h0125http://refhub.elsevier.com/S0308-8146(13)00722-X/h0125http://refhub.elsevier.com/S0308-8146(13)00722-X/h0125http://refhub.elsevier.com/S0308-8146(13)00722-X/h0125http://refhub.elsevier.com/S0308-8146(13)00722-X/h0130http://refhub.elsevier.com/S0308-8146(13)00722-X/h0130http://refhub.elsevier.com/S0308-8146(13)00722-X/h0130http://refhub.elsevier.com/S0308-8146(13)00722-X/h0135http://refhub.elsevier.com/S0308-8146(13)00722-X/h0135http://refhub.elsevier.com/S0308-8146(13)00722-X/h0135http://refhub.elsevier.com/S0308-8146(13)00722-X/h0140http://refhub.elsevier.com/S0308-8146(13)00722-X/h0140http://refhub.elsevier.com/S0308-8146(13)00722-X/h0140http://refhub.elsevier.com/S0308-8146(13)00722-X/h0145http://refhub.elsevier.com/S0308-8146(13)00722-X/h0145http://refhub.elsevier.com/S0308-8146(13)00722-X/h0145http://refhub.elsevier.com/S0308-8146(13)00722-X/h0145http://refhub.elsevier.com/S0308-8146(13)00722-X/h0145http://refhub.elsevier.com/S0308-8146(13)00722-X/h0150http://refhub.elsevier.com/S0308-8146(13)00722-X/h0150http://refhub.elsevier.com/S0308-8146(13)00722-X/h0150http://refhub.elsevier.com/S0308-8146(13)00722-X/h0155http://refhub.elsevier.com/S0308-8146(13)00722-X/h0155http://refhub.elsevier.com/S0308-8146(13)00722-X/h0155
Formation of complex natural flavours by biotransformation of
apple pomace with basidiomycetes1 Introduction2 Materials and
methods2.1 Microorganisms2.2 Substrates2.3 Chemicals2.4 Submerged
cultures2.5 Sensory evaluation2.6 Sample preparation2.6.1
Liquid/liquid extraction2.6.2 Headspace solid-phase microextraction
(HS-SPME)
2.7 Capillary gas chromatography–olfactometry (GC–O)2.8 Aroma
extract dilution analysis (AEDA) and odour activity values (OAV)2.9
Aroma model of the flavour extracts2.10 Determination of odour
threshold values2.11 Capillary gas chromatography–mass spectrometry
(GC/MS)2.11.1 GC–MS after liquid/liquid extraction2.11.2
HS-SPME–GC–MS
3 Results and discussion3.1 Screening3.2 Flavour analysis3.3
Kinetics of flavour formation3.4 Cinnamic acid as a precursor of
3-phenylpropanal and 3-phenylpropanol
4 ConclusionsAcknowledgementsReferences