Induction of simultaneous and sequential malolactic fermentation in durian wine

International Journal of Food Microbiology 230 (2016) 1–9

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Induction of simultaneous and sequential malolactic fermentation in durian wine Fransisca Taniasuri a, Pin-Rou Lee a, Shao-Quan Liu a,b,⁎ a b

Food Science and Technology Programme, Department of Chemistry, 3 Science Drive 3, National University of Singapore, 117543, Singapore National University of Singapore (Suzhou) Research Institute, No. 377 Linquan Street, Suzhou Industrial Park, Suzhou, Jiangsu 215123, China

a r t i c l e

i n f o

Article history: Received 19 November 2015 Received in revised form 29 March 2016 Accepted 3 April 2016 Available online 13 April 2016 Keywords: Malolactic fermentation Durian wine Oenococcus oeni Saccharomyces cerevisiae

a b s t r a c t This study represented for the first time the impact of malolactic fermentation (MLF) induced by Oenococcus oeni and its inoculation strategies (simultaneous vs. sequential) on the fermentation performance as well as aroma compound profile of durian wine. There was no negative impact of simultaneous inoculation of O. oeni and Saccharomyces cerevisiae on the growth and fermentation kinetics of S. cerevisiae as compared to sequential fermentation. Simultaneous MLF did not lead to an excessive increase in volatile acidity as compared to sequential MLF. The kinetic changes of organic acids (i.e. malic, lactic, succinic, acetic and α-ketoglutaric acids) varied with simultaneous and sequential MLF relative to yeast alone. MLF, regardless of inoculation mode, resulted in higher production of fermentation-derived volatiles as compared to control (alcoholic fermentation only), including esters, volatile fatty acids, and terpenes, except for higher alcohols. Most indigenous volatile sulphur compounds in durian were decreased to trace levels with little differences among the control, simultaneous and sequential MLF. Among the different wines, the wine with simultaneous MLF had higher concentrations of terpenes and acetate esters while sequential MLF had increased concentrations of medium- and long-chain ethyl esters. Relative to alcoholic fermentation only, both simultaneous and sequential MLF reduced acetaldehyde substantially with sequential MLF being more effective. These findings illustrate that MLF is an effective and novel way of modulating the volatile and aroma compound profile of durian wine. © 2016 Elsevier B.V. All rights reserved.

1. Introduction Durian (Durio zibethinus Murray) is a tropical fruit widely grown in Southeast Asia. Durian pulp is nutrient rich and possesses high bioactive properties, which give rise to its increased consumption in the past few years (Haruenkit et al., 2007). Apart from its special shape and high nutritional value, durian also possesses distinctive creamy taste and pungent odour (Voon et al., 2007). Some studies have been done to identify the volatile profiles of durian that are responsible for its unique odour. Over 170 constituents have been reported in the volatile fraction of durian. Among these volatiles, sulphur containing compounds (e.g. propanethiol, diethyl disulphide) and ethyl esters (e.g. ethyl 2methylbutanoate) were the key contributors to the strong onion like note and fruity durian aroma, respectively (Weenen et al., 1996). Despite being highly favoured, the market of durian is limited to its harvesting season and short shelf life of 3–4 days at ambient temperatures (Che Man et al., 1999). Various preservation and processing methods have been developed to add value and extend shelf life of durian. Fermentation of durian into wine is a novel approach to creating a new industrial outlet for this fruit. However, limited studies have been ⁎ Corresponding author at: Food Science and Technology Programme, Department of Chemistry, 3 Science Drive 3, National University of Singapore, 117543, Singapore. E-mail address: [email protected] (S.-Q. Liu).

http://dx.doi.org/10.1016/j.ijfoodmicro.2016.04.006 0168-1605/© 2016 Elsevier B.V. All rights reserved.

conducted on alcoholic fermentation of durian. This might be attributed to the potentially unsafe combination of durian and ethanol purportedly due to the inhibition of aldehyde dehydrogenase by the hydrophobic sulphides in durian (Maninang et al., 2009). However, Lee et al. (2012) observed the decrease of indigenous sulphides during yeast alcoholic fermentation, thus mitigating the potential risk of consuming durian wine. In the fermentation of durian pulp with pure or mixed cultures of Saccharomyces cerevisiae and Williopsis saturnus, Lee et al. (2012) reported a wide range of volatile compounds (e.g. esters and higher alcohols) were generated, while most of the volatile sulphur compounds (VSCs) initially present in the durian pulp were catabolised. With supplementation of a mixture of L-leucine and L-phenylalanine as aroma precursors in durian fermentation, further reduction and lower formation of VSCs was observed and there was increased production of isoamyl alcohol and 2-phenylethyl alcohol (Lee et al., 2013). Nevertheless, despite elimination of VSCs and enhanced desirable volatiles production, there were prominent sulphury notes in the final wine (Lee et al., 2012, 2013). Thus, the present study aimed to further modulate the aroma profile of the final durian wine through malolactic fermentation (MLF). MLF is well known for improving grape wine quality through deacidification, enhancement of microbial stability and production of desirable flavour compounds (Bartowsky et al., 2002). Oenococcus oeni

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is the most suitable lactic acid bacterium used in MLF due to its adaptability to the harsh environmental of wine (low pH, high ethanol and SO2 concentrations) and its metabolic characteristics such as low biogenic amines production (Lonvaud-Funel, 1999). However, the aim of this research was to assess the impact of MLF on flavour compound modification in durian wine. Traditionally, MLF is conducted sequentially after alcoholic fermentation (AF), either occurring naturally or through inoculation. Sequential MLF prevents excessive lactic and acetic acid productions as a result of heterofermentative sugar metabolism by O. oeni (Massera et al., 2009). However, this strategy has its own drawbacks; in particular, after AF, growth inhibitory metabolites produced by yeast such as ethanol, SO2 and medium-chain fatty acids were already accumulated. Carreté et al. (2002) demonstrated that loss of viability of O. oeni induced by ethanol, SO2 or fatty acid was partly due to inhibition of ATPase activity of O. oeni. A simultaneous inoculation strategy enables induction of MLF due to gradual adaptation of bacteria to the harsh environment (Jussier et al., 2006) and a higher nutrient content at the beginning of fermentation (Rosi et al., 2003). Simultaneous MLF reduces fermentation time. However, co-inoculation of yeast and bacteria may lead to excessive volatile acidity and/or stuck AF due to strong bacterial growth that may inhibit yeast growth and metabolic activity (Nehme et al., 2008). This research aimed to explore MLF in durian wine and to study the effects of simultaneous vs. sequential MLF on the fermentation performance of O. oeni and yeast, especially the impact of MLF on durian wine volatile profiles. 2. Materials and methods 2.1. Reagents and standards Bacteriological peptone, yeast extract, malt extract, potato dextrose agar (PDA), de Man, Rogosa, and Sharpe (MRS) agar and MRS broth were purchased from Oxoid (Hampshire, England). Food-grade sucrose and DL-malic acid were purchased from SIS (Singapore) and Suntop Enterprise Pte Ltd (Singapore) respectively. Natamax®, containing 50% natamycin, was obtained from Danisco Singapore Pte Ltd (Singapore). Reference compounds for analysis of sugars and organic acids were obtained from commercial sources: fructose (≥ 99%), glucose (≥ 99.5%), sucrose (≥ 99.5%), citric acid (≥ 99.5%), tartaric acid (≥ 99.5%), α-ketoglutaric acid (≥ 99.0%), DL-malic acid (≥ 99%), pyruvic acid (≥ 97%), lactic acid (≥ 98%) [Sigma-Aldrich Fine Chemicals, Oakville, Ontario, Canada], oxalic acid (≥ 99.5%) [Goodrich Chemical Enterprise, Singapore], and succinic acid (≥ 99%) [Fluka, Vienna, Austria]; and acetic acid (neat) [Firmenich Asia Pte Ltd, Singapore]. All standard reference compounds for quantification of volatiles were obtained from Firmenich Asia Pte Ltd (Singapore), except for isobutyl octanoate (N99%) and isoamyl octanoate (N 98%) which were obtained from Tokyo Chemical Industry Co. Ltd (Tokyo, Japan) and Sigma-Aldrich Fine Chemicals (St. Louis, MO, USA), respectively. A C5–C40 n-alkane hydrocarbon standard mixture, used for the determination of linear retention indices, was obtained from Fluka (Buchs, Switzerland). 2.2. Durian pulp preparation Durian arils of the D666 cultivar (Malaysia) were bought from a local fruit supplier and the pulp was separated from the seed. The durian puree was then obtained by blending 30% (w/w) of durian pulp with deionised water for 1 min using a blender (MX – J210GN, Panasonic, Osaka, Japan). The puree was adjusted to a final °Brix reading of 18% with food-grade sucrose and stored at −20 °C until use. Prior to inoculation, the puree was thawed, adjusted to pH of 3.5 (initial pH 6.0) with 1 M food-grade DL-malic acid, followed by heat treatment in a water bath (Julabo, Seelbach, Germany) at 60 °C for 20 min. The effectiveness of heat treatment was checked with streak plating on PDA agar.

2.3. Microorganisms and starter culture preparation S. cerevisiae var. bayanus EC-1118 and O. oeni Viniflora® CH35 were obtained from Lallemand Inc. (Brooklyn Park, Australia) and Chr. Hansen (Hørsholm, Denmark), respectively. The active-dried yeast was cultured for 48 h at 25 °C in a sterile broth containing 20 g/L glucose, 2.5 g/L yeast extract, 2.5 g/L bacteriological peptone and 2.5 g/L malt extract, pH 5.0 and stored at −80 °C in 15% glycerol until use (Lee et al., 2012). Before inoculation, the yeast culture was propagated in pasteurised durian puree for 72 h at 25 °C to reach a cell population of ~108 CFU/ml. The freeze-dried bacterial strain was cultured for 5 days at 30 °C in modified MRS broth (pH 5.0), which was supplemented with 20% (v/v) apple juice (Marigold, Malaysia Dairy Industries Pte Ltd; pH 5.5) to obtain a pure culture. The pure culture was further propagated in the modified MRS broth at 30 °C for 5 days to obtain the preculture with a cell population of ~108 CFU/mL for inoculation. 2.4. Fermentation conditions Laboratory-scale fermentations were conducted in duplicate under static conditions at 25 °C in sterilised 1-L blue-capped bottles (fitted with cotton wool and wrapped with aluminum foil). Each bottle contained 500 mL of pasteurised durian puree. Three different fermentation treatments were carried out, namely control (yeast only), simultaneous MLF (SIM, co-inoculation of yeast–bacteria) and sequential MLF (SEQ, inoculation of bacteria after AF). For the control and SEQ treatment, the durian purees were inoculated with ~ 106 CFU/mL of the pre-culture S. cerevisiae, whereas the SIM treatment was co-inoculated with S. cerevisiae and O. oeni pre-cultures at ~106 CFU/mL each at day 0. For the SEQ treatment, an O. oeni pre-culture was inoculated at ~106 CFU/mL after 5 days of yeast fermentation to prevent potential inhibition of O. oeni. Samples were taken at days 0, 2, 5, 9, 16, 21 and 28 for the determination of viable cell counts, pH, total soluble solid (oBrix), organic acids, sugars and volatile compounds. All samples were stored at −20 °C until analysis. 2.5. Enumeration of yeast and bacteria cells Growth of yeast and bacteria was monitored by spread plating. Samples were serially diluted with 0.1% (w/v) peptone water. S. cerevisiae was then enumerated by plating 0.1 mL of adequately diluted samples on PDA agar and incubated at 25 °C for 48 h, while O. oeni was enumerated on modified MRS agar and incubated at 30 °C for 5–7 days. PDA agar plates were prepared by following manufacturer's instructions. The modified MRS agar plates were prepared by dissolving 49.6 g of MRS agar powder and 0.1 g of Natamax® (50 ppm natamycin) to 800 mL of deionised water, autoclaved at 121 °C for 15 min, followed by adding 200 mL of apple juice before dispensing. 2.6. Analytical determinations of total soluble solids, pH, sugars and organic acids Total soluble solids (°Brix) and pH were measured using a refractometer (ATAGO, Tokyo, Japan) and pH meter (Metrohm, Zofingen, Switzerland), respectively. Samples for sugars and organic acids analysis were prepared by centrifugation (Sigma 3-18K, Goettingen, Germany) at 8422 g, 4 °C for 15 min twice and filtered through an 0.2-μm Minisart RC 15 syringe filter (Sartorius, Goettingen, Germany). Analysis was performed using an ultra fast liquid chromatography (UFLC, Shimadzu, Kyoto, Japan) coupled with LC-10AT System Controller, SIL-10AD VP auto injector and LC solution software version 1.25. Sugars were determined using evaporative light scattering detector (ELSD) (gain: 5; 40 °C; 350 kPa) with a Zorbax carbohydrate column (150 × 4.6 mm, 5-μm, Agilent, Santa Clara, CA, USA) and acetonitrilewater (80:20 v/v) with an isocratic flow rate of 1.4 mL/min as mobile phase (Lee et al., 2012). Organic acids were analysed using SPD-M20A

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photodiode array detector (λ = 210 nm) with a Supelcogel C-160 H column (300 × 7.8 mm, Sigma-Aldrich, Barcelona, Spain) and 0.1% (v/v) sulphuric acid as mobile phase at flow rate of 0.4 mL/min in isocratic mode at 40 °C (Lee et al., 2012, 2013). Identification and quantification were carried out by comparing the retention times and standard curves (R2 N 0.99) with that of known pure compounds. Each sample was analysed in duplicate. 2.7. Qualitative and quantitative analyses of volatiles using HS-SPME–GC– MS/FID Volatile compounds were extracted using headspace (HS) solidphase microextraction (SPME) and analysed by gas chromatography (GC)–mass spectrometry (MS) and flame ionisation detector (FID) as described in Lee et al. (2012). Prior to analysis, the sample was adjusted to pH of 2.5 with 1 M HCl and 5 mL was transferred to a 20-mL headspace vial capped with a PTFE septum. The volatiles were extracted with a carboxen/polydimethylsiloxane fibre (85 μm, Supelco, Sigma Aldrich, Barcelona, Spain) at 60 °C for 50 min under 250 rpm agitation using a SPME autosampler (CTC, Combi Pal, Switzerland) and thermally desorbed at 250 °C for 3 min into the injection port of an Agilent 7890 A gas chromatograph coupled to an Agilent 5975C triple-axis MS and FID (Santa Clara, CA, USA). Separation was carried out on a 60 m × 0.25 mm i.d. capillary column (Agilent DB-FFAP, Santa Clara, CA, USA) coated with 0.25-μm polyethylene glycol film modified with nitroterephthalic acid. The GC temperature was raised from 50 °C held for 5 min to 230 °C at 5 °C/min and held for 30 min at 230 °C. Helium was used as carrier gas with a constant flow rate of 1.2 mL/min. The FID temperature was set at 250 °C and the MS was operated in electron impact mode at 70 eV. Identification of volatiles was carried out by matching the mass spectra with those in Wiley 275 and NIST 8.0 libraries and confirmed with the linear retention index (LRI) values. The LRI values were determined by running a C5–C40 n-alkane hydrocarbon standard mixture under similar conditions and calculated using following equation, t−t n LRI ¼ 100 x ðt nþ1 −t n þ nÞ. Quantification of selected volatile compounds was determined based on the procedures of Lee et al. (2010) using external standard solutions in 10% (v/v) diluted durian puree. Calibration curves were obtained from a series of reference standards solutions of known concentrations with R2 N 0.98. Concentrations of volatile compounds were then determined by using the linear regression equations of the corresponding standards. Odour activity values (OAV) of the quantified volatiles were calculated by dividing the concentration by their odour threshold values obtained from the literature. Each sample was analysed in duplicate. 2.8. Statistical analysis A one-way analysis of variance (ANOVA) and Duncan's test (SPSS Corporation, Chicago, IL, USA, version 17.0) were applied to the experimental data with differences considered significant if the p is below 0.05. Principal component analysis (PCA) was carried out on selected volatile compounds using MATLAB R2008a (Mathworks, USA) to discriminate the volatiles among the different treatments. 3. Results and discussions 3.1. Evolution of cell biomass, °Brix and pH The evolution of S. cerevisiae and O. oeni, and changes in °Brix and pH are shown in Figs. 1 and 2 respectively. S. cerevisiae multiplied rapidly and reached its maximum population at about 5.0 × 108 CFU/mL at day 2 in all treatments. The cell counts of S. cerevisiae in the control and SIM maintained at ~ 106 CFU/mL until the end (Fig. 1A,B), while S. cerevisiae in SEQ decreased rapidly upon the inoculation of O. oeni at

Fig. 1. Evolution of S. cerevisiae and O. oeni in durian wine fermentation: control (A), simultaneous MLF (B) and sequential MLF (C). S. cerevisiae in control (□); S. cerevisiae in simultaneous MLF (◊); O. oeni in simultaneous MLF (♦); S. cerevisiae in sequential MLF (Δ); O. oeni in sequential MLF (▲). Sequential MLF: inoculation of O. oeni at day 5 of fermentation with S. cerevisiae. Arrow indicates bacterial inoculation in sequential fermentation.

day 5 (Fig. 1C). The cell counts of O. oeni increased gradually to ~ 108 CFU/mL upon inoculation at day 0 and day 5 in SIM and SEQ respectively and then remained stationary (Fig. 1B,C). At the end (day 28), bacterial viabilities in SIM were similar to those in SEQ wines. Co-inoculation of yeast and bacteria was often criticised due to the possible interference of bacteria in the course of AF carried out by yeast (Alexandre et al., 2004). The result in our study showed that yeast growth was largely unaffected by the presence of bacteria. Rapid proliferation of S. cerevisiae co-inoculated with bacteria indicated the absence of inhibitory effects on S. cerevisiae by O. oeni (Fig. 1B). All the treatments had similar trends in the total soluble solid changes (Fig. 2A). °Brix values rapidly decreased from 18 to 9 and remained constant from day 2 onwards. Rapid sugar utilisation directly correlated with the growth kinetics of S. cerevisiae which reached the maximum viable cell count at day 2 (Fig. 1). This finding corresponded to other observations that showed no interference with growth and fermentative activity of S. cerevisiae by O. oeni during co-fermentation in grape must (Jussier et al., 2006; Rosi et al., 2003), although there are studies that showed otherwise. Thus, this compatibility would depend on the yeast–bacterial strain combination and the role that each plays as well as fermentation conditions. Relative to yeast fermentation only, accelerated reductions of yeast populations were observed when rapid bacterial growth occurred (duration of 2–9 days for SIM and 5–16 days for SEQ) (Fig. 1B,C). King and

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biomass (Narendranath et al., 2001). However, the death of S. cerevisiae could not be fully explained by acetic acid alone since further reduction in yeast counts was not observed in SIM (Fig. 2B). It was possible that during co-inoculation, S. cerevisiae became progressively adaptive to the presence of O. oeni and stresses, thus improving their survival and performance (Zapparoli et al., 2009). The pH of wines gradually increased (Fig. 2B), from 3.62 to 3.73 in the control, to 3.84 in SIM and to 3.90 in SEQ, being in line with typical pH increases of 0.1 to 0.3 units after MLF. Higher increases of pH in SIM and SEQ as compared to AF concurred with the catabolism of L-malic acid.

3.2. Sugar utilisation and organic acid transformation

Fig. 2. Changes in °Brix (A) and pH (B) in durian wine fermentation: control (■); simultaneous MLF (♦); sequential MLF (▲). Sequential MLF: inoculation of O. oeni at day 5 of fermentation with S. cerevisiae.

Beelman (1986) demonstrated that bacteria accelerated yeast death without any effect on AF, which was possibly due to the production of inhibitory bacterial metabolites in addition to depletion of certain nutrients or survival factors required by the yeast. Acetic acid is a wellknown inhibitory substance towards S. cerevisiae (Narendranath et al., 2001) and indeed, its significant increase was observed in both SIM and SEQ (Table 1). Cell death was possibly induced by acetic acid due to the passive diffusion of its undissociated form across cell membrane, followed by deprotonation that caused intracellular acidification. Subsequently, ATP was channeled for pH homeostasis, resulting in the reduction of cell

Oenological parameters of the durian wines before and after fermentation are shown in Table 1. Sucrose, fructose and glucose were the sugars detected and were completely catabolised, except for glucose with residual trace amounts (Table 1). All sugars were rapidly utilised by day 2 of fermentation and the trends of sugar utilisation in both SIM and SEQ were similar to those of the control (data not shown), mirroring that of oBrix reduction (Fig. 2A). No significant difference in the ethanol content was found between samples with or without MLF (Table 1). Organic acid transformation is shown in Fig. 3. Most of the fermentation characteristics of SIM were similar to that of SEQ, hence the timing of bacterial inoculation did not appear to affect the final organic acid concentration (Table 1). DL-Malic acid was used to adjust the pH of durian pulp in this study. It must be noted that only L-malic acid was degradable by O. oeni. MLF progressed in line with L-malic and citric acids degradation. The rate of MLF in wine was directly linked to the bacterial cell density, with malolactic activity at its highest during the early stages of growth (Krieger et al., 1992). Indeed, L-malic acid degradation corresponded with growth of O. oeni which occurred mainly from day 2 to 5 in SIM and day 5 to 9 in SEQ (Figs. 1, 3). The degradation of L-malic acid correlated with the production of lactic acid in SIM and SEQ (Fig. 3). The conversion of L-malic acid to L-lactic acid could have a significant impact on taste of wine, giving more palatable wine as a result of reduced acidity (Ugliano and Moio, 2005). The decrease in malic acid concentration was also observed in the control wine. Although certain strains S. cerevisiae were shown to metabolise 3–45% (w/v) of L-malic acid in grape juice (Rankine, 1966), Redzepovic et al. (2003) demonstrated that S. cerevisiae EC-1118 lacks malic enzyme and thus does not readily

Table 1 Oenological parameters of final durian wine (day 28). Day 0 pH Total soluble solids (°Brix) Ethanol (% v/v) Sugar (g/100 mL) Fructose Glucose Sucrose Organic acid (g/100 mL) Acetic acid α-Ketoglutaric acid Citric acid Lactic acid Malic acid Oxalic acid Pyruvic acid Succinic acid Tartaric acid a,b,c,d

Control (No MLF)

Simultaneous MLF

Sequential MLF

3.624 ± 0.003a 18.68 ± 0.06a 0.262 ± 0.032a

3.734 ± 0.012b 9.14 ± 0.05b 5.983 ± 0.334b

3.837 ± 0.004c 9.12 ± 0.13b 5.789 ± 0.346b

3.904 ± 0.008d 9.12 ± 0.000b 6.148 ± 0.225b

0.638 ± 0.012a 0.576 ± 0.014a 10.621 ± 0.119a

0.000 ± 0.000b 0.046 ± 0.002b 0.000 ± 0.000b

0.000 ± 0.000 b 0.074 ± 0.005c 0.000 ± 0.000 b

0.000 ± 0.000b 0.070 ± 0.000d 0.000 ± 0.000b

0.000 ± 0.000a 0.000 ± 0.000a 0.000 ± 0.000a 0.027 ± 0.001a 0.882 ± 0.006a 0.000 ± 0.000a 0.044 ± 0.002a 0.074 ± 0.002a 0.090 ± 0.002a

0.100 ± 0.012b 0.014 ± 0.001b 0.013 ± 0.000b 0.218 ± 0.116b 0.441 ± 0.147b 0.017 ± 0.001b 0.024 ± 0.003b 0.347 ± 0.062b 0.023 ± 0.005b

0.173 ± 0.002c 0.009 ± 0.000c 0.000 ± 0.000a 0.368 ± 0.005c 0.310 ± 0.013c 0.018 ± 0.000b 0.020 ± 0.000c 0.153 ± 0.005c 0.016 ± 0.000c

0.167 ± 0.006c 0.009 ± 0.000c 0.000 ± 0.000a 0.446 ± 0.004c 0.308 ± 0.003c 0.018 ± 0.000b 0.019 ± 0.000c 0.162 ± 0.003c 0.016 ± 0.000c

Statistical analysis at 95% confidence level with same letters indicating no significant difference.

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Fig. 3. Changes in organic acids during fermentation of durian wine: control (■); simultaneous MLF (♦); sequential MLF (▲).

degrade L-malic acid. Hence, the reduction of total malic acid in the control wine might be partially due to its passive diffusion into the cell of S. cerevisiae, especially D-malic acid (Coloretti et al., 2002). Citric acid is the intermediate product of tri-carboxylic acid (TCA) cycle; its increase at day 2 could be linked to the aerobic respiration of sugar by yeast where oxygen was still available at the early stage of fermentation (Fig. 1). Citric acid was completely utilised by O. oeni independent of the timing of inoculation (Fig. 3). O. oeni is known to metabolise citric acid together with the residual glucose present after AF and this citrate-glucose co-metabolism could be important to O. oeni due to increased ATP synthesis arising from both substratelevel phosphorylation and chemiosmotic mechanism (Ramos and Santos, 1996). However, the level of citric acid in durian was too low to be significant. Bacterial citric acid consumption is directly involved in the production of acetic acid, lactic acid, diacetyl via the citric acid pathway (Bartowsky and Henschke, 2004). An increase in acetic acid was observed during MLF, as shown in SIM and SEQ (Fig. 3). O. oeni could generate acetic acid either through heterofermentative sugar metabolism or from citric acid metabolism (Bartowsky and Henschke, 2004). The decrease in citric acid in SIM and SEQ corresponded with the increase of acetic acid (Fig. 3). Coinoculation of malolactic bacteria with yeast is often associated with excessive increases of acetic acid due to the availability of sugars (Massera et al., 2009). In this study, although the acetic acid concentration in SIM was higher than that in SEQ, it was not statistically significant (Table 1). Other studies also demonstrated no significant negative impact of co-inoculation of S. cerevisiae and O. oeni on acetic acid production (Jussier et al., 2006; Rosi et al., 2003). Acetic acid is of particular importance in wine as it may serve as the precursor of fruity acetate esters via acetyl-CoA (Swiegers et al., 2005). Correspondingly, SIM and SEQ with elevated amounts of acetic acid had higher concentrations of ethyl and isoamyl acetate as compared to AF only (Table 2).

Succinic and α-ketoglutaric acids were produced by yeast but catabolised by O. oeni (Fig. 3). S. cerevisiae strains are known to be strong succinic acid producers and tend to accumulate succinic acid (Heerde and Radler, 1978), thus explaining the marked increases of succinic acid (Fig. 3). Succinic acid could also be produced by O. oeni from αketoglutarate. Being different from other lactic acid bacteria that reduce α-ketoglutarate to 2-hydroxyglutarate or convert α-ketoglutarate into glutamate via transamination, O. oeni strains metabolise αketoglutarate to produce 4-hydroxybutyrate and succinic acid (Zhang and Ganzle, 2010). However, a decrease in succinic acid concentration was observed in the wines subjected to MLF (Fig. 3) and this acid could be transformed into fumaric acid, then to malic acid via the oxidative branch of the TCA cycle but further study is required. Nevertheless, the utilisation of succinic acid by O. oeni in SIM and SEQ could be linked to the production of its corresponding esters, diethyl and diisobutyl succinates (Table S1). Succinic acid has an unusual bitter-salty taste (Coulter et al., 2004), thus its reduction may be beneficial. The decrease in tartaric acid is shown in Fig. 3 was likely due to precipitation as potassium hydrogen tartrate, as this acid is generally not degraded by yeast and O. oeni. As illustrated in Fig. 3, the kinetics of pyruvic acid changes were similar among AF, SIM and SEQ, although a lower amount of pyruvic acid was detected at day 2 in SIM, suggesting its utilisation by O. oeni. A small amount of oxalic acid increased consistently in AF, SIM and SEQ with no discernible difference among them (Fig. 3). Neither S. cerevisiae nor O. oeni is known to produce oxalic acid. Oxalic acid could be the product of oxaloacetic acid degradation chemically or biologically or released from durian pulp, which requires further research. 3.3. Impact of malolactic fermentation on the volatile profile of durian wine Various volatiles, comprising alcohols, esters, acids, carbonyl compounds, VSCs and terpenes, were identified and quantified using HS-

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Table 2 Concentrations of major volatiles (mg/L) in final durian wine (day 28). Compound quantified

Hexanoic acid Octanoic acid Decanoic acid 1-Propanol Isobutyl alcohol Active amyl alcohol Isoamyl alcohol 2-Phenylethyl alcohol Benzaldehyde Ethyl 2-methylbutanoate Ethyl hexanoate Ethyl octanoate Ethyl nonanoate Ethyl decanoate Ethyl dodecanoate Ethyl tetradecanoate Ethyl hexadecanoate Isobutyl octanoate Isoamyl octanoate Ethyl acetate Isoamyl acetate Diethyl disulphide 1-Propanethiol

Day 0

Control

Simultaneous MLF

Sequential MLF

Concentration (mg/L)

OAVe

Concentration (mg/L)

OAVe

Concentration (mg/L)

OAVe

Concentration (mg/L)

OAVe

0.21 ± 0.01a 0.22 ± 0.01a 0.48 ± 0.00a 0.32 ± 0.05a 0.00 ± 0.00a 0.00 ± 0.00a 0.96 ± 0.14a 0.59 ± 0.05a 0.008 ± 0.00a 0.20 ± 0.02a 0.006 ± 0.00a 0.01 ± 0.00a 0.00 ± 0.00a 0.03 ± 0.00a 0.00 ± 0.00a 0.00 ± 0.00a 0.00 ± 0.00a 0.00 ± 0.00a 0.00 ± 0.00a 0.22 ± 0.03a 0.04 ± 0.01a 2.44 ± 0.25a 0.41 ± 0.05a

0.03 0.03 0.08 0.00 0.00 0.00 0.03 0.06 0.00 11.11 0.12 0.50 0.00 0.15 0.00 0.00 0.00 0.00 0.00 0.03 1.20 566.98 544.00

0.18 ± 0.03a 0.33 ± 0.02b 0.56 ± 0.01b 11.94 ± 0.59b 33.24 ± 3.63b 3.09 ± 0.24b 33.87 ± 1.57b 150.19 ± 4.75b 0.02 ± 0.00b 0.04 ± 0.01b 0.03 ± 0.00b 0.21 ± 0.02b 0.005 ± 0.00b 0.88 ± 0.10b 6.02 ± 0.61b 0.39 ± 0.03b 2.69 ± 0.31b 0.03 ± 0.00b 0.06 ± 0.00b 2.42 ± 0.10b 0.001 ± 0.00b 0.003 ± 0.00b 0.00 ± 0.00b

0.02 0.04 0.09 0.02 0.83 0.05 1.13 15.01 0.01 2.44 0.52 10.50 0.00 4.38 1.02 0.19 1.35 0.04 0.50 0.32 0.03 0.70 0.00

0.19 ± 0.02a 0.36 ± 0.00c 0.58 ± 0.01c 10.64 ± 2.06bc 34.19 ± 3.02b 3.08 ± 0.39b 28.72 ± 1.95c 170.94 ± 2.02b 0.02 ± 0.00bc 0.05 ± 0.00b 0.03 ± 0.00b 0.24 ± 0.02bc 0.006 ± 0.00c 0.93 ± 0.08b 6.36 ± 0.55c 0.46 ± 0.04c 4.67 ± 0.46c 0.03 ± 0.00c 0.06 ± 0.00b 4.09 ± 0.44c 0.017 ± 0.00c 0.004 ± 0.00b 0.00 ± 0.00b

0.02 0.04 0.10 0.02 0.85 0.05 0.96 17.09 0.01 2.89 0.56 11.85 0.00 4.67 1.08 0.23 2.33 0.04 0.49 0.55 0.57 0.93 0.00

0.18 ± 0.03a 0.38 ± 0.00c 0.61 ± 0.02d 9.84 ± 0.41c 32.23 ± 3.58b 3.11 ± 0.64b 29.95 ± 2.41c 129.70 ± 11.99d 0.02 ± 0.00c 0.07 ± 0.01b 0.03 ± 0.00b 0.26 ± 0.02c 0.006 ± 0.00c 1.05 ± 0.06c 6.92 ± 0.53d 0.49 ± 0.01c 5.36 ± 0.17d 0.03 ± 0.00bc 0.07 ± 0.00c 3.99 ± 0.59c 0.011 ± 0.00d 0.004 ± 0.00b 0.00 ± 0.00b

0.02 0.04 0.10 0.02 0.81 0.05 1.00 12.97 0.00 3.72 0.54 12.80 0.00 5.26 1.17 0.25 2.68 0.04 0.54 0.53 0.37 0.93 0.00

Odour thresholdf (mg/L)

8 8.8 6 500 40 65 30 10 3.5g 0.018h 0.05 0.02 1.3i 0.2 5.9j 2k 2i 0.8h 0.125l 7.5 0.03 0.0043 0.00075

a,b,c,d e f g h i j k l

Statistical analysis at 95% confidence level with same letters indicating no significant difference. From Bartowsky et al. (2008). OAV: Odour activity values calculated by dividing concentration by the odour threshold value of the compound. From Buttery et al. (1990). From Ferreira et al. (2000). From Li (2006). The matrix was a 12% ethanol/water mixture containing 5 g/L tartaric acid at pH 3.2. From Pino and Queris (2011). From Tao and Zhang (2010). From Li et al. (2008).

SPME-GC–MS/FID (Table S1). Higher alcohols and esters were the main volatiles of durian wine. Carbonyl compounds, VSCs and terpenes were also present and contributed to the complex aroma profile. Table S1 lists the volatile compounds identified in the initial durian and wines after the different treatments. The concentration of selected volatiles compounds and their odour activity is listed in Table 2. Alterations of volatiles associated with MLF could arise from a shift in the production by yeast due to the presence of bacteria and additional contribution by bacteria (Rossouw et al., 2012). Alcohols were the major volatiles produced during fermentation, contributing to over 90% peak area of total volatiles detected (Table S1). An increase in the majority of higher alcohols was observed and considered to contribute to the fruity and aroma complexity in wine. These included propanol, isobutyl alcohol, active amyl alcohol, isoamyl alcohol, and 2-phenylethyl alcohol (Table S1). Generally, no significant difference in the levels of higher alcohols was observed with MLF as compared to the control, except for isoamyl alcohol which was found to be lower in the wines subjected to MLF (Table 2), being largely consistent with findings of Herjavec et al. (2001). Nonetheless, Jeromel et al. (2008) observed increases in isobutyl alcohol and 2-phenylethanol after MLF, while de Revel et al. (1999) found an increase in isoamyl alcohol after MLF. This discrepancy could stem from different O. oeni strains used. Besides, the lower concentration of isoamyl alcohol was accompanied by the higher concentration of its corresponding ester i.e. isoamyl acetate (Table 2). Esters initially present in durian were degraded during fermentation; these included methyl 2-methylbutanoate, ethyl 2-butenoate, ethyl 2-methylbutanoate, ethyl 2-methyl-2-butenoate and propyl 2methylbutanoate (Table S1). The majority of esters were produced by yeast during alcoholic fermentation. MLF, irrespective of the bacterial inoculation regimes, consistently caused increases in almost all esters (Table S1). The most important esters associated with and produced

during MLF are ethyl acetate, ethyl lactate and diethyl succinate (Pozo-Bayόn et al., 2005). The production of these esters was coupled to the metabolism of their acid precursors (acetic, lactic and succinic acid) during MLF by O. oeni (Fig. 3). Ethyl lactate is associated with fruitiness, milky notes and increased mouthfeel in wine while diethyl succinate contributes to fruity and floral notes (Ugliano and Moio, 2005); both MLF esters have relatively high odour detection thresholds (100 ppm each in ethanol solution). The levels of other acetate esters including isoamyl acetate and 2-phenylethyl acetate were also higher in the MLF wines (Table S1). In contrast, Jeromel et al. (2008) and Gambaro et al. (2001) reported the reduction of these esters after MLF, which could be due to the strains variations. The amounts of ethyl esters of fatty acids were also significantly higher in the wines subjected to MLF (Table S1), which concurred with the study by Ugliano and Moio (2005). Final concentrations of esters in the MLF wines were dependent on the timing of inoculation of O. oeni. SIM produced higher concentrations of acetate esters including ethyl acetate and isoamyl acetate, while SEQ caused higher increases in medium- and long-chained ethyl esters such as ethyl decanoate, ethyl dodecanoate and ethyl hexadecanoate (Table S1). Since acetate esters are more associated with fruity characters, this result corresponded to those of Bartowsky et al. (2008) and Massera et al. (2009), who reported that the wine produced with coinoculation of S. cerevisiae and O. oeni scored higher in fruity character than that with sequential inoculation. Volatile fatty acids initially present in durian (i.e. propanoic, pentanoic, heptanoic and nonanoic acids) were metabolised to trace levels, possibly to form their corresponding esters (Table S1). On the other hand, the concentrations of octanoic and decanoic acids increased during fermentation. These fatty acids could be generated through βoxidation of long-chain fatty acids liberated from triglycerides in durian pulp by yeast lipase or through successive steps of fatty acid synthesis in

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the presence of acetyl CoA (Hiltunen et al., 2003). The concentrations of both octanoic and decanoic acids were higher in the MLF wines (Table 2), regardless of the timing of O. oeni inoculation. These results were in agreement with Herjavec et al. (2001) and Pozo-Bayόn et al. (2005) who also reported significant increases in the levels of octanoic and decanoic acids after MLF. The concentrations of octanoic and decanoic acids were below their threshold values (Table 2), hence unlikely to affect the aroma profile of wine. The level of acetaldehyde was significantly lower in the MLF wines especially SEQ as compared to the control wine (Table S1), which agreed with other studies (Osborne et al., 2006; Pozo-Bayόn et al., 2005). O. oeni was able to metabolise both free and bound acetaldehyde to produce acetic acid and ethanol (Osborne et al., 2000). Although the chemical impact of acetaldehyde metabolism was limited since no or insignificant increases in the levels of ethanol and acetic acid was observed (Table S1), degradation of acetaldehyde may lead to reduction in herbaceous green odour, thus improving wine aroma (Osborne et al., 2000). Higher aliphatic aldehydes initially present in durian from hexanal to nonanal decreased or became not detectable after fermentation (Table S1), probably being reduced to alcohols or oxidised to acids and even transformed into esters (Sumby et al., 2010). There were productions of benzaldehyde, 2-octenal and 2-decenal (Table S1). Benzaldehyde was an intermediate product of metabolism of phenylalanine, while 2-octenal and 2-decenal were likely formed due to auto-oxidation of unsaturated fatty acids present in durian pulp (Jaswir et al., 2008). Diacetyl was initially present in durian pulp but became not detectable after fermentation in all treatments (Table S1). Diacetyl was supposed to be produced from metabolism of citric acid by O. oeni during MLF. However, diacetyl is chemically unstable and thus readily reduced to form acetoin or 2,3-butanediol during fermentation. Indeed, the level of acetoin increased with MLF and was significantly higher in SIM (Table S1). Knoll et al. (2011) found no detectable levels of diacetyl and acetoin in wines after MLF but increased levels of its reduced form, 2,3-butanediol. Reduction of diacetyl to acetoin or 2,3-butanediol depends on the redox potential of the wine as well as the activity of NADPH-dependent diacetyl reductase and acetoin reductase (Nielsen and Richelieu, 1999). An increase in γ-butyrolactone, a by-product of glutamate metabolism in O. oeni, was often observed with MLF (Maicas et al., 1999). A higher γ-butyrolactone level was also observed in SIM and SEQ (Table S1). Ugliano and Moio (2005) obtained similar findings and explained that the low levels of γ-butyrolactone detected could be due to individual O. oeni strain characteristics. The majority of VSCs initially present in the durian pulp were catabolised during fermentation (Table S1), being in agreement with the findings of Lee et al. (2012, 2013). Ethyl thioacetate, ethanethiol and propanethiol decreased to an undetectable level by end of fermentation (Table S1). Under the acidic conditions of wine, ethyl thioacetate was likely to undergo hydrolysis to the parent mercaptan (Rauhut et al., 1998). Ethanethiol and propanethiol were reactive thiols and hence easily oxidised in the presence of trace metal ions (e.g. iron, copper) or reacted with polymeric phenols to form non-volatile thiols (Nikolantonaki et al., 2010). In the presence of yeast lees, thiol consumption occurred and accounted for the formation of disulphide bridges between thiols and the cysteinyl residue of yeast cell wall mannoproteins (Nikolantonaki et al., 2010). Sulphides, 1,1bis(ethylthio)-ethane, and 3,5-dimethyl-1,2,4-trithiolane were reduced to trace levels (Table S1). Under anaerobic conditions, yeasts were able to reduce sulphides to their respective thiols (Gómez-Plaza and CanoLópez, 2011), which subsequently could be degraded via various mechanisms as mentioned above. There was no further reduction of these VSCs attributed to MLF (Table S1). Several VSCs that were absent in the durian pulp were generated during fermentation. Ethyl 3-(methylthio)-propanoate, ethyl 2(ethylthio)-propanoate, and 3-(ethylthio)-1-propanol were identified as the predominant VSCs generated and their levels were higher in

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the wines subjected to MLF (Table S1). Ethyl 3-(methylthio)propanoate is considered an odour active compound, providing pleasant fruity Concord grape aroma at a low level (0.2 ppm) (Kolor, 1983). Ethyl 3-(methylthio)-propanoate was proposed to be produced via direct esterification or alcoholysis of ethanol with 3-(methylthio)propanoic acid derived by yeast from catabolism of L-methionine (Landaud et al., 2008). Both SIM and SEQ had significantly higher levels of this volatile than the control wine (Table S1). Supporting this finding, Pripis-Nicolau et al. (2004) found an elevated amount of 3(methylthio)-propanoic acid in Merlot wine after MLF. The presence of 3-(ethylthio)-1-propanol was also observed in red and white wine (Moreira et al., 2010, 2011), but its biogenesis is not clear. A wide range of terpenes was produced during fermentation (Table S1), comprised of monoterpenes and sesquiterpenes. These compounds could be released through acid hydrolysis and/or β-glucosidase activity of yeasts (Ugliano and Moio, 2006). Higher amounts of terpenes were observed in the MLF wines (Table S1), which could be due to βglucosidase activity of O. oeni. The results of this study were in agreement with D'Incecco et al. (2004) and Ugliano and Moio (2005) who also reported increased amounts of terpenes following MLF. The SIM wine had the highest amount of all terpenes except for α-humulene, while the SEQ wine only showed increases in geranial and sabinene as compared to the control wine (Table S1). Knoll et al. (2012) also reported that sequential inoculation of O. oeni resulted in a higher content of α-terpineol, while co-inoculation showed a higher content of linalool after MLF in Riesling wine. 3.4. Multivariate analysis of volatiles in durian wines Principal component analysis (PCA) was applied to acetic acid (Table 1) and quantified volatile compounds in Table 2 to illustrate the underlying trends in the data and to obtain more information on the variations in the final wines. The first two principal components (PC1 and PC2) accounted for almost 100% of the variation in the data; PC1 and PC2 displayed 66.91% and 33.08% variance, respectively (Fig. 4). The aroma compound profile of the control wine was distinguishable from SIM and SEQ wines across PC1, whereas the SIM wine could be further separated from the SEQ wine across PC2 (Fig. 4). From the bi-plot, it was clear that MLF and timing of inoculations had modulated the volatile profile of the final wines. The control wine was located on the right hand side of the bi-plot and mainly characterised by the volatiles loadings of higher alcohols (isoamyl alcohol, 1-propanol, isobutyl alcohol, 2-phenylethyl alcohol) and aldehyde (benzaldehyde). On the upper left quadrant, the SIM wine was mainly related to acetic acid and its esters (i.e. ethyl acetate and isoamyl acetate), ethyl hexanoate, ethyl nonanoate, isobutyl octanoate and diethyl disulphide. Located on the negative ends of PC1 and PC2, the SEQ wine was closely attributed to volatile fatty acids (octanoic and decanoic acids) and their respective ethyl esters, ethyl dodecanoate, ethyl tetradecanoate, ethyl 2-methyl butanoate, isoamyl octanoate, and active amyl alcohol. In terms of sensory perception, which was conducted using quantitative descriptive analysis with 30 untrained panelists, MLF wines were perceived to be less acidic, more sulphury/alliaceous and creamier. These descriptions, to a degree, agreed with analytical data. Reduction in acidity in the MLF wines aligned with degradation of malic and citric acids, whereas the increases in acetic and lactic acids did not adversely affect perception (Fig. 3). Sulphury and creamy characteristics might be related to the higher levels of certain VSCs and 3-hydroxy-2-butanone (acetoin) respectively (Table S1). Fruitiness and/or sweetness in MLF wines were not perceptibly increased despite more esters. 4. Conclusion This study showed the possibility to inoculate O. oeni at different timings without inhibiting AF or causing failure of MLF in durian wine.

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Fig. 4. Bi-plot of principal component analysis of selected volatiles of different durian wines.

Co-inoculation of S. cerevisiae and O. oeni did not negatively impact the growth and fermentation kinetics of S. cerevisiae and the final wine as compared to sequential MLF. The differences in organic acid profiles (e.g. acetic acid and lactic acid) in wine in relation to MLF indicated the different metabolic activities and could be used as a means to project the possible differences in volatiles formed (e.g. ethyl acetate and ethyl lactate). Generally, increases in esters, volatile fatty acids, volatile sulphur compounds and terpenes were observed in wine after MLF while higher alcohols were scarcely affected by MLF. Simultaneous MLF resulted in more acetate esters and terpenes, while sequential MLF produced more medium- to long-chain ethyl esters. This research demonstrated the potential of MLF to modulate durian wine flavour. Supplementary data to this article can be found online at http://dx. doi.org/10.1016/j.ijfoodmicro.2016.04.006. References Alexandre, H., Costello, P.J., Remize, F., Guzzo, J., Guilloux-Benatier, M., 2004. Saccharomyces cerevisiae–Oenococcus oeni interactions in wine: current knowledge and perspectives. Int. J. Food Microbiol. 93, 141–154. Bartowsky, E.J., Henschke, P.A., 2004. The ‘buttery’ attribute of wine — diacetyl — desirability, spoilage and beyond. Int. J. Food Microbiol. 96, 235–252. Bartowsky, E.J., Costello, P.J., Henschke, P.A., 2002. Management of malolactic fermentation — wine flavour manipulation. Aust. N. Z. Grapegrow. Winemak. 461a, 10–12. Bartowsky, E.J., Costello, P.J., McCarthy, J., 2008. MLF — adding an ‘extra dimension’ to wine flavour and quality. Aust. N. Z. Grapegrow. Winemak. 533a, 60–65. Buttery, R.G., Teranishi, R., Ling, L.C., Turnbaugh, J.G., 1990. Quantitative and sensory studies on tomato paste volatiles. J. Agric. Food Chem. 38, 336–340. Carreté, R., Teresa Vidal, M., Bordons, A., Constanti, M., 2002. Inhibitory effect of sulfur dioxide and other stress compounds in wine on the ATPase activity of Oenococcus oeni. FEMS Microbiol. Lett. 211, 155–159. Che Man, Y.B., Irwandi, J., Abdullah, W.J.W., 1999. Effect of different types of maltodextrin and drying methods on physico-chemical and sensory properties of encapsulated durian flavour. J. Sci. Food Agric. 79, 1075–1080. Coloretti, F., Zambonelli, C., Castellari, L., Tini, V., Rainieri, S., 2002. The effect of DL-malic acid on the metabolism of L-malic acid during wine alcoholic fermentation. Food Technol. Biotechnol. 40, 317–320. Coulter, A.D., Godden, P.W., Pretorius, I.S., 2004. Succinic acid — how it is formed, what is its effect on titratable acidity, and what factors influence its concentration in wine? Aust. N. Z. Wine Ind. J. 19, 21–25. D'Incecco, N., Bartowsky, E.J., Kassara, S., Lante, A., Spettoli, P., Henschke, P.A., 2004. Release of glycosidically bound flavour compounds of Chardonnay by Oenococcus oeni during malolactic fermentation. Food Microbiol. 21, 257–265. Ferreira, V., López, R., Cacho, J.F., 2000. Quantitative determination of the odorants of young red wines from different grape varieties. J. Sci. Food Agric. 80, 1659–1667.

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