Letters in Applied Microbiology ISSN 0266-8254
UNDER THE MICROSCOPE
Bacterial spoilage of wine and approaches to minimize it
E.J. Bartowsky
The Australian Wine Research Institute, Adelaide, SA, Australia
Keywords
aroma, lactic acid bacteria, off flavour,
spoilage management, taint.
Correspondence
Eveline J. Bartowsky, The Australian Wine
Research Institute, PO Box 197, Glen
Osmond, Adelaide, SA 5064, Australia.
E-mail: [email protected]
2008 ⁄ 1406: received 14 August 2008, revised
and accepted 11 September 2008
doi:10.1111/j.1472-765X.2008.02505.x
Abstract
Bacteria are part of the natural microbial ecosystem of wine and play an
important role in winemaking by reducing wine acidity and contributing to
aroma and flavour. Conversely, they can cause numerous unwelcome wine
spoilage problems, which reduce wine quality and value. Lactic acid bacteria,
especially Oenococcus oeni, contribute positively to wine sensory characters, but
other species, such as Lactobacillus sp. and Pediococcus sp can produce undesirable volatile compounds. Consequences of bacterial wine spoilage include
mousy taint, bitterness, geranium notes, volatile acidity, oily and slimy-texture,
and overt buttery characters. Management of wine spoilage bacteria can be as
simple as manipulating wine acidity or adding sulfur dioxide. However, to control the more recalcitrant bacteria, several other technologies can be explored
including pulsed electric fields, ultrahigh pressure, ultrasound or UV irradiation, and natural products, including bacteriocins and lysozyme.
Introduction
Winemaking has a long history dating back over
7000 years. Although the concept of transforming grape
must into wine is not difficult to understand, production
of a flavoursome and stable wine that does not spoil during storage requires considerable expertise on the part of
the winemaker. Vinification practices today are not vastly
different from those of ancient Egyptians and Greeks,
however, the contemporary winemaker has much greater
control at critical stages from grape harvest to bottling
when bacteria can proliferate.
The main role of micro-organisms in winemaking is to
convert grape sugars to alcohol, reduce wine acidity and
introduce interesting and desirable aroma and flavours to
the wine. Although grape must has a relatively complete
nutrient composition, it can support only a limited number of micro-organisms, and wine, with its limited nutrients, is even less inviting. The strongest selection
pressures against yeast and bacteria in grape must are
high sugar content and low pH, whereas, in wine, it is
high ethanol, acidity, SO2 content and limited nutrients.
One of the aims of winemaking is to minimize potential
for microbial spoilage and this review focuses on bacterial
wine spoilage and explores options for curtailing the
growth of unwanted bacteria.
Wine-associated micro-organisms
Yeast and bacteria found in grape must and wine originate
from the vineyard, grapes, and winery processing equipment (Fleet 1993). This ‘natural microflora’ includes several dozen species of yeast, with Saccharomyces cerevisiae
being predominant. Lactic acid and acetic acid bacteria
(AAB) are the only families of bacteria found in grape must
and wine. These include four genera of lactic acid bacteria
(LAB), Lactobacillus, Leuconostoc, Oenococcus and Pediococcus and two genera of AAB, Acetobacter and Gluconobacter.
Bacterial wine spoilage
Many secondary metabolites produced by bacteria are
volatile and potentially affect wine sensory qualities; this
review will focus on undesirable flavour compounds.
Figure 1 summarizes the pathways for bacterial metabolism of wine spoilage compounds and Table 1 lists these
compounds, their sensory descriptors and aroma threshold concentrations.
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Journal compilation ª 2008 The Society for Applied Microbiology, Letters in Applied Microbiology 48 (2009) 149–156
149
Bacterial spoilage of wine
E.J. Bartowsky
Mousy off-flavour
ACPY ACTPY
Mannitol taint
mannitol
acrolein
ACTPY
ACPY
Bitterness
mannitol
Ornithine
acetaldehyde
acrolein
glucose or
fructose
3-hydroxy propionaldehyde
ethyl acetate
Solvent
character
Ethanol
UDP-glucose
glucan
G-1-P
G-6-P
Fructose
acetic acid
Glucose
ethyl acetate
Glycerol
acetic acid
Ethanol
acetaldehyde
Cell-wall &
glucan
synthesis
Lysine
Acetyl-CoA
phenols
pyruvate
2,3 butandione
Citric acid
Sorbic acid
Tartaric acid
acetoin
Malic acid
2,3 butandione
(diacetyl)
acetaldehyde
2,3-butanediol
Vinegar
acetic acid
aroma
acetic acid
sorbyl alcohol
oxalacetic acid
3,5-hexadien-2-ol
ethanol
2-ethoxyhexa-3,5-dienne
Geranium note
malic acid
oxalacetic acid
pyruvic acid
Buttery character
lactic acid
pyruvic acid
CO2
fumaric acid
acetic acid
lactic acid
acetic acid
succinic acid
lactic acid
acetic acid
Malic acid metabolism
via malate dehydrogenase
2-ethoxyhexa-3,5-dienne
succinic acid
acetic acid
lactic acid
Tartaric acid metabolism
Acetobacter
Lactobacillus
Oenococcus
Pediococcus
Figure 1 Summary of bacterial pathways leading to spoilage aroma and flavour compounds of wine. Pathways are complied from several
sources (Sponholz 1993; Costello and Henschke 2002; Wisselink et al. 2002; Swiegers et al. 2005; Walling et al. 2005a; Bartowsky and Pretorius
2008).
Growth of Lactobacillus, Pediococcus and even some
Oenococcus species in wine, usually following malolactic
fermentation, gives rise to numerous spoilage scenarios,
as they can form undesirable aroma and flavour compounds. All AAB species are considered spoilage bacteria.
Fortunately, the occurrences of most spoilage scenarios
are uncommon and can be avoided with correct hygiene
management during the vinification and maturation
process.
Desirability of a compound in wine is dependent on
concentration and wine style (Francis and Newton 2005).
For example, the buttery or butterscotch aromas of the
carbonyl compound, diacetyl (2,3-butanedione) which is
an intermediate metabolite of citric acid metabolism in
LAB (Ramos et al. 1995), can add pleasant aromas and
complexity to wine at concentrations below 4 mg l)1.
However, above this, diacetyl in wine may become objectionable with overt buttery notes (Martineau et al. 1995).
A variety of factors, including that the winemaker can
150
control, particularly during malolactic fermentation, affect
the concentration of diacetyl. The bacterial strain used,
oxygen exposure, fermentation temperature and duration
of malolactic fermentation impact on diacetyl production
(Bartowsky and Henschke 2004b).
Acetic acid, acetaldehyde and ethyl acetate are the main
spoilage compounds produced by wine-associated AAB
species. Acetic acid and acetaldehyde are formed from the
oxidative metabolism of ethanol (Adachi et al. 1978). In
addition, AAB can form the ethyl ester of acetic acid,
ethyl acetate, which has a pungent, solvent-like aroma,
reminiscent of nail lacquer remover (Francis and Newton
2005). Wine is at high risk of spoilage by AAB during
prolonged barrel maturation if wine is not topped up and
monitored regularly, but poor management during bottling and storage of red wine can give rise to spoilage
because of the proliferation of Acetobacter pasteurianus
(Bartowsky and Henschke 2004a, 2008). Small increases in
acetic acid can be observed during alcoholic fermentation
ª 2008 The Author
Journal compilation ª 2008 The Society for Applied Microbiology, Letters in Applied Microbiology 48 (2009) 149–156
E.J. Bartowsky
Bacterial spoilage of wine
Table 1 Wine spoilage compounds as a result of bacterial metabolism during winemaking
Sensory
descriptor
Compound
Acetaldehyde
Aroma
threshold
)1
Bacteria (genus)
100 mg l
OH
Bruised apple,
sherry-like,
nutty
Vinegar, sour,
pungent
0Æ2 g l)1
H
Acetobacter,
Gluconobacter,
LAB*
7Æ5 mg l)1
O
Nail polish
remover
Acetobacter,
Gluconobacter,
LAB
Buttery, nutty,
caramel
0Æ1–2 mg l)1
Oenococcus,
Lactobacillus
Crushed
geranium
leaves
0Æ1 lg l)1
Lactobacillus,
Pediococcus
Caged mouse
4–5 lg l)1
Lactobacillus,
Oenococcus
Caged mouse
2–18 lg l)1
Lactobacillus,
Oenococcus
Caged mouse
7Æ8 lg l)1
Lactobacillus,
Oenococcus
O
O
Acetic acid
O
Ethyl acetate
Acetobacter,
Gluconobacter
O
2,3-Butandione (diacetyl)
O
2-Ethoxy-3,5-hexadiene
O
O
2-Acetyl-tetrahydropyridine
(ACTPY)
N
2-Ethyltetrahydropyridine
(ETPY)
N
O
2-Acetyl-1-pyrroline
(ACPY)
N
O
Acrolein
Bitterness
Lactobacillus,
Pediococcus
Ropy, viscous,
oily, slimy,
thick texture
Pediococcus
Viscous, sweet,
irritating finish
Oenococcus
H
b-D-Glucan
(exopolysaccharide)
OH
Mannitol
OH
OH
HO
OH OH
*LAB, lactic acid bacteria; includes species from Lactobacillus, Oenococcus and Pediococcus.
ª 2008 The Author
Journal compilation ª 2008 The Society for Applied Microbiology, Letters in Applied Microbiology 48 (2009) 149–156
151
Bacterial spoilage of wine
E.J. Bartowsky
because of yeast metabolism, or after the completion of
malolactic fermentation, usually from citric acid metabolism by LAB (Ramos and Santos 1996).
Mousy wines result from the metabolism of ornithine
and lysine, leading to the formation of extremely potent
and unpleasant nitrogen-heterocylic compounds [2-acetyltetrahydropyridine (ACTPY), 2-acetyl-1-pyrroline (ACPY)
and 2-ethyltetrahydropyridine (ETPY)] (Costello et al.
2001; Costello and Henschke 2002). These compounds
are perceived on the back palate as a persistent aftertaste
reminiscent of caged mice (Tucknott 1977) because of
interactions with the mouth environment; an increase in
pH renders the compounds volatile. Production of the
nitrogen-heterocylic compounds appears to be limited to
the heterofermentative LAB (O. oeni and some species of
Lactobacillus) (Costello et al. 2001; Costello and Henschke
2002). Wine associated Dekkera and Brettanomyces yeast
have also been shown to produce these compounds
(Grbin and Henschke 2000), however, they do not appear
to be the major source of this problem.
Sorbic acid (2,4-hexadienoic acid) can be used as a
chemical preservative in sweetened wines at bottling to
prevent yeast fermentation after packaging. However, several LAB species, including O. oeni strains, are able to
metabolize sorbic acid resulting in the formation of 2-ethoxyhexa-3,5-diene, which has an odour reminiscent of
crushed geranium leaves (Pelargonium spp.) (Riesen
1992). Thus, care is needed when bottling wine preserved
with sorbic acid to ensure that the bacterial population
has been eliminated.
Metabolism of several sugars and polyols by bacteria
can result in wine spoilage. Bitterness in wine can develop
from metabolism of glycerol, mainly by Lactobacillus sp.
The bitter taste is thought to result from the reaction of
red wine phenolics with acrolein (Fig. 1) (Sponholz
1993). This type of wine spoilage is often referred to as
‘amertume’ (bitter in French).
Fructose metabolism by heterofermentative LAB
including O. oeni can result in the formation of mannitol,
a six-carbon sugar alcohol (Wisselink et al. 2002). Mannitol tainted wine is complex as it is usually also accompanied by high acetic acid, d-lactic acid, n-propanol and
2-butanol (Sponholz 1993). Such spoiled wine can also be
perceived as having a slimy texture with a vinegar-estery
aroma and slightly sweet taste. The switch to mannitol
formation via heterolactic and mannitol fermentation
occurs at the metabolic level, is growth rate related and
maintenance of the redox balance (Richter et al. 2003).
A wine with a viscous and thick texture is referred to
as ‘ropy’; this is because of the presence of excess exopolysaccharides such as b-d-glucan. In this context, the
production of exopolysaccharides is almost exclusively
because of Pediococcus growth in wine, which is prompted
152
by high pH. The production of b-d-glucan and its polymerization are well characterized (Walling et al. 2005a)
and shown to be as a result of the presence of a plasmid
carrying the dps (glucosyltransferase) gene (Walling et al.
2005b). Recently, some O. oeni strains have been isolated
carrying the dps gene (Walling et al. 2005b).
Removal or inhibition of unsolicited wine bacteria
How best to avoid wine spoilage is not always clear-cut.
Even appropriate hygiene practices and the chemically
harsh nature of wine cannot be relied on as a deterrent to
unwanted bacteria and winemaking regulations may further limit the options for intervention available to the
winemaker. As an initial barrier, the high ethanol concentrations (up to 16% v ⁄ v), high wine acidity (pH as low as
2Æ9) can inhibit development of bacterial populations,
however, in wines with lower ethanol concentrations and
low acidity (above pH 3Æ7), it can be challenging to arrest
bacterial growth. Storage of wine at temperatures below
15C might assist with minimizing the ability of bacteria
to proliferate in wine, but will also delay wine maturation. Unlike the treatment of wort in beer brewing, grape
must is not pasteurized prior to yeast inoculation. Heating wine prior to bottling has been explored, including
flash pasteurization, however, concerns on the impact of
this on wine sensory characteristics have meant that this
technology is not widely used (Ribéreau-Gayon et al.
2006).
Treatment of wine with chemical inhibitors or natural
products
Traditionally, sulfur dioxide has been used to control
unwanted micro-organisms during winemaking, where it
is usually added to bins of machine-harvested grapes and
after malolactic fermentation. Sulfur dioxide acts as both
an antimicrobial agent and an antioxidant in wine
(Romano and Suzzi 1993). However, several bacterial species are resistant to high concentrations of sulfur dioxide.
Physical removal of micro-organisms through filtration of
juice or wine can also be used. However, filtration typically is mainly conducted prior to bottling and hence is
not used to remove micro-organisms during winemaking.
An overall trend to reduce the use of sulfur dioxide,
mainly for public health concerns, and a move in recent
years to reduce the use of filtration, as some winemakers
feel that filtration might impact unfavourably on wine flavour, has seen the search for alternative methodologies
including chemical inhibitors and physical means to curb
bacterial wine spoilage.
There are several chemical inhibitors and natural products that can be used for the control of bacteria in wine
ª 2008 The Author
Journal compilation ª 2008 The Society for Applied Microbiology, Letters in Applied Microbiology 48 (2009) 149–156
E.J. Bartowsky
Bacterial spoilage of wine
Table 2 Approaches to limit or halt bacterial growth in wine
Controlling agent
Mechanism of action
Traditional
Sulfur dioxide
Inhibits the development of bacteria
Filtration
Physical removal of bacteria from wine
Chemical
Dimethyl dicarbonate Reacts irreversibly with the amino groups
(DMDC)
on active sites of enzymes
Natural products
Lysozyme
Disrupts cell wall synthesis causing cell lysis
Bacteriocins
Alters cell wall components causing cell lysis
Up and coming physical technologies
Ultrahigh pressure
Causes damage to cytoplasmic membrane
and inactivates enzymes
High power
Sound waves cause thinning of cell
ultrasound
membranes, localized heating and
production of free radicals
UV irradiation
Damages DNA
Pulsed electric fields
Dielectrical breakdown of cell membranes
(Table 2). Although these options have great potential to
reduce or eliminate bacterial populations, they are additives, and as such, legislative approval is required for their
use in winemaking.
Dimethyl dicarbonate is a chemical inhibitor of
micro-organisms (Daudt and Ough 1980) by inactivating
cellular enzymes. It hydrolyses to methanol and carbon
dioxide, natural constituents of grape juice and wine that
do not affect wine flavour or colour. Although dimethyl
dicarbonate is approved for use in most winemaking
countries, the effectiveness of dimethyl dicarbonate varies
between species and strain. Studies in grape must demonstrated that bacteria were more resistant than yeast to
dimethyl dicarbonate (500–1000, 150–400 mg l)1, respectively) (Delfini et al. 2002). More recent studies in red
wine suggest that the permitted rate of dimethyl dicarbonate addition (200 mg l)1) does not effectively inhibit
LAB or AAB (Costa et al. 2008) implying that dimethyl
dicarbonate might not be a good preservative against
undesired bacterial contamination of wine. Other disadvantages of the use of dimethyl dicarbonate in wine are
its low solubility in water, and, potential toxicity after
ingestion or inhalation during treatment of wine.
‘Natural products’ such as lysozyme and bacteriocins to
inhibit bacterial growth have been successfully utilized in
various pharmaceutical and food industries for almost
50 years, and lysozyme has recently been approved for
use in winemaking (maximum addition rate: 500 mg l)1).
Lysozyme, a small single peptide with muramidase activity, is ineffective against eukaryotic cells; that is it cannot
be used to control spoilage yeast, such as Dekkera ⁄ Brettanomyces (McKenzie and White 1991). Structural
differences between the cell wall of Gram-positive and
Gram-negative bacteria also limit its use for controlling
AAB species.
Lysozyme can be added at various stages throughout
grape vinification to inhibit LAB (Gerbaux et al. 1997;
Bartowsky 2003). Different LAB vary in their susceptibility to lysozyme in wine (Bartowsky 2003), however, uses
of lysozyme include the inhibition of Lactobacillus species
during alcoholic fermentation thus reducing the risk of
increased volatile acidity, delaying or blocking the onset
of malolactic fermentation, controlling LAB populations
during sluggish or stuck alcoholic fermentation, and to
inhibit the onset of malolactic fermentation postbottling
(Gerbaux et al. 1999). The aroma of wine is not affected
by the addition of lysozyme (Bartowsky et al. 2004). As
with all treatments of wine, the addition of lysozyme
must be considered carefully; it is able to bind with tannins and polyphenols in red wines and typically results in
a slight decrease in wine colour or might result in the formation of a wine haze (Gerbaux et al. 2000; Bartowsky
2003; Bartowsky et al. 2004).
Bacteriocins, such as nisin, pediocin and plantaricin,
produced by some LAB, are small polypeptides that are
inhibitory to other bacterial species. These polypeptides
act on the cell wall of bacteria to induce cell lysis (Bruno
et al. 1992). Species of Lactobacillus and Pediococcus are
more resistant to nisin than O. oeni strains (Mendes Faia
and Radler 1990), and pediocin and plantarincin have
been shown to successfully kill O. oeni cells (Nel et al.
2002). A combination of nisin and sulfur dioxide has
been proposed as a means to reduce the use of sulfur
dioxide in winemaking (Rojo-Bezares et al. 2007). More
recently, a bacteriocin-like inhibitory substance has been
shown to be affective against wine Lactobacillus species
(Yurdugül and Bozoglu 2002, 2008). Although the use of
bacteriocins to control LAB in wine has great potential,
its use has not yet been approved in winemaking.
Oenological products, such as phenolic compounds,
have been demonstrated to have antimicrobial activity
against pathogenic bacteria (Papadopoulou et al. 2005;
Vaquero et al. 2007) and several compound types (hydroxycinnamic and hydroxybenzoic acids) can hinder
wine bacterial growth (Vivas et al. 1997; Reguant et al.
2000). Limited investigations have been undertaken in
using individual phenolic compounds to control spoilage
bacteria (Garcia-Ruiz et al. 2008).
Alternative technologies to eliminate bacteria from wine
There is an array of emerging technologies that have been
used successfully in several food and beverage industries
for eliminating micro-organisms (Cheftel 1995; Smelt
1998) and could be considered for removing microorganisms from wine. These include ultrahigh-pressure
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Journal compilation ª 2008 The Society for Applied Microbiology, Letters in Applied Microbiology 48 (2009) 149–156
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E.J. Bartowsky
processing, ultrasound, ultraviolet irradiation and pulsed
electric fields (Table 2).
Ultrahigh-pressure treatment was recognized as a
potential preservation technique almost a century ago
when it was demonstrated that microbial spoilage of milk
could be delayed following ultrahigh-pressure treatment
(Hite 1899). The applied pressure causes inactivation of
micro-organisms and enzymes while not affecting flavour
molecules and vitamins (Tauscher 1995). Its antimicrobial
effects are primarily as a result of cytoplasmic membrane
damage (Hoover et al. 1989). Ultrahigh-pressure technology has been successfully applied in fruit juices (Smelt
1998), desserts and rice cakes (Cheftel 1995), and has
been reviewed as an application in cheese manufacture
(Stewart et al. 2006).
High-power ultrasound uses frequencies in the range
20 to 100 kHz and has the ability to cause the formation
and collapse (cavitation) of high-energy microbubbles
and can be used in food processing to inactivate microbes
(Piyasena et al. 2003). The mechanism of microbial killing is mainly because of thinning of cell membranes,
localized heating and production of free radicals (Fellows
2000; Butz and Tauscher 2002). This technique has been
shown to inactivate numerous food-related micro-organisms and has recently been proposed as an option for
consideration in the wine industry (Jiranek et al. 2008).
Ultraviolet irradiation has been shown to significantly
reduce LAB populations (including Lactobacillus sp.) in
recirculated brines (Gailunas et al. 2008) and killing fungi
on harvested grapes (Valero et al. 2007). However, it has
not been extensively investigated for sterilizing wine. Sensory effects of UV exposure on wine will need to be
examined as beer or milk stored in clear glass bottles
exposed to light can develop ‘light struck’ off flavour
(Cardoso et al. 2006).
Pulsed electric field technology has been used in beverage industries, as a means of sterilizing the product. It
has been explored as an alternative to pasteurization in
the production of fruit drinks, which can lead to losses
in nutritional and organoleptic qualities. This technology
involves application of short pulses (1–10 ms) of highor low-intensity electric field to foods placed between
two electrodes in batch, or in continuous flow systems,
at low-processing temperatures (<50C). Pulsed electric
field has been used in combination with natural antimicrobials (bacteriocins, enzymes, lysozyme) to enhance
the micro-biocidal protection of fruit juices (Liang et al.
2006; Mosqueda-Melgar et al. 2008). Recent trials have
also shown that pulsed electric field in combination with
low concentrations of SO2 does not negatively influence
the formation of volatile compounds in grape must
(Garde-Cerdan et al. 2008). Thus, pulsed electric field
technology could be further explored as a means to
154
eliminate spoilage bacteria from wine during wine storage prior to bottling.
Conclusion and future directions
Bacterial wine spoilage continues to be of concern in
grape vinification. Consumer reactions to the use of
chemical preservatives in wine will be on-going challenges
for the winemaker. Managing wine acidity is one mechanism with which bacterial spoilage can be controlled,
however, addition of acid to grape must and wine is subject to regulations in numerous countries and may be
limited in some wine types because of impacts on wine
style. Technologies based on UV irradiation, pressure and
electric fields have been successfully employed in numerous beverage industries to sterilize products and recent
trials in grape must or wine have been encouraging.
Health concerns and changing regulatory requirements
provide further motivation for the winemaking community to seek alternative ways to limit the proliferation of
wine spoilage bacteria and these emerging technologies
might provide support in this quest.
Acknowledgements
This project was supported by Australia’s grapegrowers
and winemakers through their investment agency, the
Grape and Wine Research and Development Corporation,
with matching funds from the Australian Government.
The author is appreciative for critical comments by Drs
Paul Chambers and Paul Henschke during the preparation of the manuscript.
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