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Food Control 22 (2011) 647e656

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Food Control
journal homepage: www.elsevier.com/locate/foodcont

Review

Importance of acetic acid bacteria in food industry


Ilkin Yucel Sengun a, *, Seniz Karabiyikli b,1
a b

Ege University, Engineering Faculty, Food Engineering Department, 35100 Bornova, Izmir, Turkey Gaziosmanpasa University, Faculty of Engineering and Natural Science, Department of Food Engineering, 60250 Tokat, Turkey

a r t i c l e i n f o
Article history: Received 27 May 2010 Received in revised form 27 October 2010 Accepted 6 November 2010 Keywords: Acetic acid bacteria Isolation Identication Vinegar Wine

a b s t r a c t
Acetic acid bacteria (AAB) comprise a group of gram-negative or gram-variable, ellipsoidal to rod-shaped cells that have an obligate aerobic metabolism with oxygen as the terminal electron acceptor. In the rst classication of AAB, two main genera were determined as Acetobacter and Gluconobacter, but nowadays twelve genera are recognized and accommodated to the family Acetobacteraceae, the Alphaproteobacteria: Acetobacter, Gluconobacter, Acidomonas, Gluconacetobacter, Asaia, Kozakia, Swaminathania, Saccharibacter, Neoasaia, Granulibacter, Tanticharoenia and Ameyamaea. Isolation, purication, identication and preservation of AAB are very difcult. Phenotypic methods based on physiological abilitiesies have been used for identication of AAB by using various media. These phenotypic properties have now been complemented or replaced by molecular techniques, which are DNA and RNA based techniques. AAB are widespread in nature on various plants (fruits, cereals, herbs, etc.). They are important microorganisms in food industry because of their ability to oxidize many types of sugars and alcohols to organic acids as end products during fermentation process. The best known industrial application of AAB is vinegar production. This group of bacteria is also used in cellulose and sorbose production. On the other hand, the oxidizing ability of AAB could have spoilage effect in some products such as in wine. The aim of the present review is to introduce the importance of AAB in food industry by showing their current taxonomy, enumeration, isolation and identication methods, isolation sources and benecial effects in food production systems. 2010 Elsevier Ltd. All rights reserved.

1. Introduction Acetic acid bacteria (AAB) are gram-negative or gram-variable, aerobic, non-spore forming, ellipsoidal to rod-shaped cells that can occur single, in pairs or chains. Their sizes vary between 0.4e1 mm wide and 0.8e4.5 mm long. They are catalase positive and oxidase negative. The optimum pH for the growth of AAB is 5e6.5 while they can grow at lower pH values between 3 and 4 (Holt, Krieg, Sneath, Staley, & Williams, 1994). AAB are heterogeneous assemble, comprising both peritrichously and polarly agellated organisms (Gonzales, 2005). In the early years, AAB were classied into two main genera: Acetobacter and Gluconobacter, but nowadays twelve genera are recognized and accommodated to the family Acetobacteraceae, the Alphaproteobacteria: Acetobacter, Gluconobacter, Acidomonas, Gluconacetobacter, Asaia, Kozakia, Swaminathania, Saccharibacter, Neoasaia, Granulibacter, Tanticharoenia and Ameyamaea. Occurrence of
* Corresponding author. Tel.: 90 232 3113028; fax: 90 232 3427592. E-mail addresses: ilkinyucel@yahoo.com, ilkin.sengun@ege.edu.tr (I.Y. Sengun), senizkarabiyikli@hotmail.com, seniz.karabiyikli@gop.edu.tr (S. Karabiyikli). 1 Tel.: 90 3562521616/3285. 0956-7135/$ e see front matter 2010 Elsevier Ltd. All rights reserved. doi:10.1016/j.foodcont.2010.11.008

Acidomonas, Kozakia, Swaminathania, Saccharibacter, Neoasaia, Granulibacter, Tanticharoenia and Ameyamaea strains is rather rare in common isolation sources such as vinegar, wine, fruits and owers (Yamada & Yukphan, 2008; Yukphan et al., 2009, 2008). AAB have traditionally been enumerated by quantifying viable colonies by plating in solid culture media. Not all the media support growth of AAB equally and they are selective for one strain or another (Gullo, Caggia, De Vero, & Giudici, 2006). Thus, different media were used for isolation and phenotypic methods based on physiological abilities were used for identication. On the other hand, there are some limitations for plating such as time requirement, inability to detect viable but noncultivable (VBNC) cells. To overcome these disadvantages of culturing, new techniques have been developed using molecular approaches (Gonzalez, Guillamon, Mas, & Poblet, 2006). AAB were studied genotypically by DNAerRNA hybridization, DNAeDNA hybridization and ribosomal RNA gene sequences (5S rRNA, 16S rRNA, and 23S rRNA). AAB are well known for the ability to oxidize the sugars and alcohols, resulting an accumulation of organic acids as nal products. A considerable number of AAB can oxidize alcohols into sugars; mannitol into fructose; sorbitol into sorbose or erythritol into erythrulose (Gonzales, 2005). Gluconobacter is an industrially

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important genus for the production of L-sorbose from D-sorbitol; Dgluconic acid, 5-keto- and 2-keto-D-gluconate from D-glucose; and dihydroxyacetone from glycerol (Gupta, Singh, Qazi, & Kumar, 2001). AAB are involved in some important industrial process (De Vero, 2010; Raspor & Goranovic, 2008). These bacteria can produce high concentrations of acetic acid from ethanol, which makes them important to the vinegar industry. The other known application of AAB is to produce sorbose and cellulose (Gonzales, 2005). On the other hand, AAB are sometimes involved in foods and beverages in detrimental way, such as in wine (Bartowsky & Henschke, 2008). The present review is focused on the taxonomy, isolation and identication of AAB and occurrence or usage of this group in foods and beverages. 2. Taxonomy of AAB The taxonomy of AAB has not been fully established yet and rearrangements of the group are still in progress. The reasons for this taxonomic uncertainty are both due to the limited knowledge of the AAB phylogenesis and isolation, identication and preservation difculties of these bacterial strains (De Vero & Giudici, 2008). The taxonomy of AAB initially based on morphological and physiological criteria. The rst classications were proposed by Hansen in 1894, based on the occurrence of a lm in the liquid media, and its reaction with iodine. Asai (1934e1935) formulated the proposal of classifying AAB into two genera: Acetobacter and Gluconobacter. A major change in the classication of AAB was introduced by Yamada, Hoshino, and Ishikawa (1997, 1998), in which they transferred Acetobacter species containing Q-10 (Acetobacter xylinus, Acetobacter liquefaciens, Acetobacter hansenii,
Table 1 Species of the twelve genera of acetic acid bacteria. Genus Acetobacter Species A. aceti A. cerevisiae A. cibinongensis A. estunensis A. indonesiensis A. lovaniensis A. malorum A. nitrogenigens A. oeni A. orientalis A. orleanensis A. pasteurianus A. peroxydans A. pomorum A. syzygii A. tropicalis Ac. methanolica As. bogorensis As. krungthrpensis As. lannensis As. siamensis As. spathodeae Genus Gluconacetobacter Species Ga. Ga. Ga. Ga. Ga. Ga. Ga. Ga. Ga. Ga. Ga. Ga. Ga. Ga. Ga. azotocaptans diazotrophicus entanii europaeus hansenii intermedius johannae liquefaciens nataicola oboediens rhaeticus sacchari saccharivorans swingsii xylinus

Acidomonas Asaia

Granulibacter Gluconobacter

Ameyamaea Neoasaia Kozakia

Am. chiangmaiensis N. chiangmaiensis K. baliensis

Saccharibacter Swaminathania Tanticharoenia

Gr. bethesdensis G. albidus G. cerinus G. frateurii G. japonicus G. kondonii G. oxydans G. roseus G. sphaericus G. thailandicus G. wancherniae S. oricola Sw. salitolerans T. sakaeratensis

Table is adapted from Yamada and Yukphan (2008) with combining data from Malimas et al. (2007) (for G. kondonii); Malimas et al. (2008) (As. lannensis); Malimas et al. (2008a) (for G. roseus); Malimas et al. (2008b) (for G. sphaericus); Yukphan et al. (2008) (for Tanticharoenia); Malimas et al. (2009) (for G. japonicus); Yukphan et al. (2009) (for Ameyamaea); Kommanee et al. (2010) (for As. spathodeae); Yukphan et al. (2010) (for G. wancherniae).

Acetobacter diazotrophicus and Acetobacter europaeus) to the genus Gluconacetobacter. Nowadays, the family Acetobacteraceae accommodates twelve genera for the AAB: Acetobacter, Gluconobacter, Acidomonas, Gluconacetobacter, Asaia, Kozakia, Swaminathania, Saccharibacter, Neoasaia, Granulibacter, Tanticharoenia and Ameyamaea (Yamada & Yukphan, 2008; Yukphan et al., 2009, 2008). Table 1 shows the current classication of AAB. In general, AAB belonging to the genus Acetobacter have been found more frequently than those belonging to Gluconobacter (Camu et al., 2007). The main differences between these two genera were both cytological and physiological. The main physiological difference was that Acetobacter oxidized ethanol into acetic acid and, subsequently, completed the oxidation of acetic acid into water and CO2. On the other hand, Gluconobacter species were unable to complete this oxidation of acetic acid (Gonzales, 2005). Other differential characteristics of AAB are shown in Table 2. Although the tests given in Table 2 are used to differentiate AAB genera, these phenotypic tests alone are not really reliable and not recommended (Cleenwerck & de Vos, 2008). As it can be seen from the table, AAB are heterogeneous assemble, comprising both peritrichously and polarly agellated organisms. In the early years, agellation pattern was used in the classication of AAB. The polarly agellated AAB species are classied in the genus Gluconobacter, while the peritrichously agellated species are grouped into the genus Acetobacter (Leifson, 1954). Quinone analyses can also be used to differentiate AAB genera, as a chemotaxonomical method. The genus Acetobacter is characterized chemotaxonomically by Q-9 as a major respiratory quinone, which is quite unique and exceptional, although other genera have Q-10 (Yamada, Aida, & Uemura, 1969). On the other hand, genus-level identication of AAB using phenotypic tests is relatively easy when compared with species level identication (Cleenwerck & de Vos, 2008). AAB have two enzymes, which play a role in oxidation process: alcohol dehydrogenase and aldehyde dehydrogenase. The alcohol dehydrogenase activity of Acetobacter is more stable under acetic conditions than that of Gluconobacter, which explains why Acetobacter produces more acetic acid (Matsushita, Toyama, & Adachi, 1994). Acetic acid resistance of AAB is strain dependent (Nanba, Tamura, & Nagai, 1984). Trcek, Raspor, and Teuber (2000) reported that the resistance to acidic environment (pH 2.5e3.5) and the requirements of acetic acid for growth are variable phenotypic traits in A. europaeus strains. AAB can metabolize a variety of organic acids, such as acetic, citric, fumaric, lactic, malic, pyruvic and succinic acids and this ability brings them important in winemaking (Gonzales, 2005). Different carbohydrates can be used by AAB as carbon sources. Sugar is more preferred as a carbon source by Gluconobacter than Acetobacter because the species of Gluconobacter can obtain energy more efciently by the metabolisation of the sugars via pentose phosphate pathway. They oxidize glucose via two alternate pathways. One operates inside the cell followed by oxidation via the pentose phosphate pathway and second operates outside the cell and involves the formation of gluconic acid and ketogluconic acid (Kulka & Walker, 1954; Olijve & Kok, 1979). The former is carried by NADP-dependent glucose dehydrogenase, and the latter is performed by NADP independent glucose dehydrogenase and is also called as direct glucose oxidation pathway (Kitos, Wang, Mohler, King, & Cheldelin, 1958). Direct oxidation metabolism pathway works only in the presence of >15 mM glucose in the culture medium (Weenk, Olijve, & Harder, 1984). Few species are able to grow at elevated sugar concentration e.g. Gluconacetobacter diazotrophicus species can grow at 30% of D-glucose (Swings, 1992). Glucose tolerance of AAB strains isolated from Traditional Balsamic Vinegar was studied and the results showed that majority of the isolated strains are inhibited by 25% of glucose while ethanol

I.Y. Sengun, S. Karabiyikli / Food Control 22 (2011) 647e656 Table 2 Differential characteristics of the twelve genera of acetic acid bacteria. Characteristic Flagellation Oxidation of ethanol to acetic acid Oxidation of acetic acid to CO2 and H2O Oxidation of lactate to CO2 and H2O Growth on 0.35% acetic acid-containing medium Growth on methanol Growth on D-mannitol Growth in the presence of 30% D-glucose Production of cellulose Production of levan-like mucous substance from sucrose Fixation of molecular nitrgen Ketogenesis (dihydroxyacetone) from glycerol Acid production from: D-Mannitol Glycerol Rafnose Cellular fatty acid type Ubiquinone type DNA base composition (mol% G C) A pe/n /wc / / / / / C18:1 Q-9 52e60 Ac n w w w Nd C18:1 Q-10 63e66 As pe/n /wa / /w / C18:1 Q-10 59e61 Ga pe/n b / / / / / / / / C18:1 Q-10 55e66 G po/n / C18:1 Q-10 55e63 K n w w C18:1 Q-10 56e57 S pe w w Nd Nd Nd Nd Q-10 57e60 Sa n v w Q-10 52e53 N n Nd w w Q-10 63.1 Gr n v w Nd Nd Nd Nd v Nd Q-10 59 T n Am po w w w w

649

Q-10 66.0

Q-10 65.6

Abbreviations: A, Acetobacter; Ac, Acidomonas; As, Asaia; Ga, Gluconacetobacter; G, Gluconobacter; K, Kozakia; S, Swaminathania; Sa, Saccharibacter; N, Neoasaia; Gr, Granulibacter; T, Tanticharoenia; Am, Ameyamaea; pe, peritrichous; po, polar; n, none; , 90% or more of the strains positive; w, weakly positive reaction; , 90% or more of the strains negative; v, variable; Nd, not determined. a Asaia does not produce acetic acid from ethanol with the exception of one strain producing acid weakly (Yamada et al., 2000). b Overoxidation of acetate to CO2 and H2O depends on acetate concentration in medium. c A. pomorum assimilates methanol weakly (Sokollek et al., 1998b). Table is adapted from Sievers and Swings (2005) with combining data from Loganathan and Nair (2004) (for Swaminathania); Jojima et al. (2004) (for Saccharibacter); Yukphan et al. (2005) (for Neoasaia); Greenberg et al. (2006) (for Granulibacter) Yukphan et al. (2008) (for Tanticharoenia); Yukphan et al. (2009) (for Ameyamaea).

concentration of the cooked and fermented must is less signicant for AAB growth (Gullo et al., 2006). AAB are mesophilic microorganisms and their optimum growth temperature is between 25 and 30  C (Gullo & Giudici, 2008). Thermoresistant properties of AAB isolated from tropical products of Sub-Saharan Africa were studied by Ndoye et al. (2006). In the study, two specic AAB, namely Acetobacter tropicalis and Acetobacter pasteurianus were selected for their ability of growth and acetate production at higher temperature. The advantages of these strains were reported as the considerable reduction of the cooling water expenses and the availability of the strains for traditional vinegar fermentation (Ndoye et al., 2006). Some AAB species can x atmospheric nitrogen. Ga. diazotrophicus, Gluconacetobacter azotocaptans and Ga. johannae are known as nitrogen-xing species. In recent years, S. salitolerans, A. peroxydans and A. nitrogenigens were also identied as nitrogenxing bacteria (Dutta & Gachhui, 2006; Loganathan & Nair, 2004; Muthukumarasamy et al., 2005).
Table 3 Different media used for isolation and/or identication of acetic acid bacteria. Media YPMa Medium (Gullo & Giudici, 2008) Yeast extract Peptone Mannitol Agar GYCb Medium (Gullo & Giudici, 2008) Glucose Yeast extract CaCO3 Agar GYc Medium (Yamada & Yukphan, 2008) Glucose Yeast extract Agar Distilled water
a b c

3. Enumeration, isolation and identication of AAB Enumeration, isolation, identication and preservation of AAB are not easy. It is important how to isolate pure dened strains from various sources of potential habitats. Not all the media support growth of AAB equally and they are selective for one strain to another (Gullo et al., 2006). Although there are lots of media, developed for isolation and/or identication of AAB (Table 3), they mainly consist of the same ingredients with varying proportions, which cause different reactions on the plate. By the way, mainly used incubation condition for the growth of AAB is 30  C for 2e5 days (Seearunruangchai et al., 2004; Yamada & Yukphan, 2008). AAB strains that are able to grow on solid media may have greater metabolic tness. The halo formation that is one of the basic characteristics that associates a given colony to the AAB group (Cleenwerck & de Vos, 2008). Glucose Yeast Extract CaCO3 Medium (GYC) was proposed as a medium that enabled most strains to be recovered in traditional vinegars (Gullo et al., 2006). Environment of

Proportion 0.5% 0.3% 2.5% 1.2% 10.0% 1.0% 2.0% 1.5% 2g 1g 2g 100 ml

Media AE-medium (Yamada et al., 1999) Glucose Yeast Extract Peptone Agar Absolute ethanol Acetic acid Reinforced AE-medium (Zahoor et al., 2006) Glucose Yeast extract Peptone Na2HPO4$H2O Citric acid Ethanol Acetic acid

Proportion 0.5% 0.3% 0.4% 0.9% 3 ml 3 ml 4% 1% 1% 0.338% 0.15% 2%(v/v) 1%(v/v)

Yeast extract peptone mannitol medium. Glucose yeast extract CaCO3 medium. Glucose yeast extract medium.

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the isolates is also important for selecting the isolation of suitable media. It is reported that isolates from cider or wine vinegar fermentations grew readily in Reinforced AE-Medium (RAEMedium) while AE-Medium proved most suitable for the cultivation of strains isolated from spirit vinegar fermentations (Sokollek et al., 1998a). In a liquid medium such as wine with high alcohol content, the presence of free SO2 and the low availability of oxygen subject the microorganisms to serious stress and they probably need some recovery before they can grow on a solid medium with a different carbon source. In fact, oxygen enrichment has been proposed as a way of improving cultivability, or of putting an end to the VBNC status (Millet & Lonvaud-Funel, 2000). Rapid method for total, viable and non-viable AAB determination was developed by Baena-Ruano et al. (2006) as a possible option, using the direct counting in a Neubauer chamber as well as an epiuorescence staining technique, using the live/dead BacLight Bacterial Viability Kit, has been studied in their work. The advantages of this method reported as follows: (i) it is a reliable, rapid, easy and yields both viable and total bacteria in only one step, (ii) samples are easy to prepare and easy to differentiate because of the high degree of contrast between the green color of the viable bacteria and the red color of the dead cells, (iii) BackLight stain does not produce background uorescence. Cultivation and maintenance of AAB in pure culture is one of the greatest hurdles, especially for strains isolated from high acetic acid level source (Sievers, Sellmer, & Teuber, 1992). The use of 20% malt extract as cryo protectant was effective for the preservation of all AAB strains (Sokollek et al., 1998a). Ndoye, Weekers, Diawara, Guiro, and Thonart (2007) used 20% mannitol as cryoprotectant to detect the survival and preservation properties of thermoresistant AAB after freezeedrying process and found that freeze-dried cells could be conserved at 4  C for at least 6 months without loss of viability. Few ecological studies have analyzed the main AAB species involved in the process, while all studies have been conducted with cultivable strains only. The availability of a reliable and fast technique for AAB enumeration is very useful in the food industry, in which AAB are used as biotechnological agents or in which AAB may spoil food product (Torija, Mateo, Guillamon, & Mas, 2010). 3.1. Molecular techniques Classical microbiological taxonomy has traditionally used morphological, physiological and biochemical differences among the species to discriminate between them while physiological methods
Table 4 Name of molecular techniques. Name of molecular technique PCR-RFLP of the 16S rDNA/ PCR-RFLP of the 16Se23S rDNA Internally Transcribed Spacer (ITS) DNAeDNA Hybridizations Denaturing Gradient Gel Electrophoresis (DGGE)/ Temporal Temperature Gradient Gel Electrophoresis (TTGE) Fluorescence In Situ Hybridization (FISH) Real-Time PCR (RT-PCR) Nested PCR Epiuorescence Filter Technique RT-PCR with TaqManeMGB probe Amplied Fragment Length Polymorphism (AFLP) DNA Fingerprinting Random Amplied Polymorphic DNA-PCR (RAPD-PCR) Enterobacterial Repetitive Intergenic Consensus-PCR (ERIC-PCR) Repetitive Extragenic Palindromic-PCR (REP-PCR) Reference

would not be able to distinguish the currently described species (Gonzales, 2005). On the other hand, quantication of AAB in solid media has some limitations such as time requirement, inability to detect VBNC cells. Miniaturized phenotypic systems which were initially developed for the groups of bacteria (e.g. Enterobacteriaceae), such as ID32C, API 20 NE (bioMerieux) and RapID NH (Remel) were also used for the identication of AAB without much success (Cleenwerck & de Vos, 2008). Finally, new techniques have been developed using molecular approaches to overcome the disadvantages of culturing and identication of AAB (Gonzalez, Hierro, Poblet, Mas, & Guillamon, 2006). Recently, the principles of currently applied methodology for characterization of AAB are summarized by Cleenwerck and de Vos (2008). These techniques are summarized in Table 4. DNAeDNA hybridization values play a key role in species delineation. Several methods have been used to measure the DNA relatedness among bacteria such as microplate method, the membrane method, spectrophotometer initial renaturation method (Cleenwerck & de Vos, 2008). Lisdiyanti et al. (2001) delineated Acetobacter species, isolated from Indonesian sources by DNAeDNA hybridization data and Cleenwerck, Vandemeulebroecke, Janssens, and Swings (2002) conrmed the ndings of Lisdiyanti et al. (2001). On the other hand, recently, a discrepancy, resulting in different taxonomic conclusions was found between the DNA relatedness values reported by Dellaglio et al. (2005) and Lisdiyanti, Navarro, Uchimura, and Komagata (2006) with strains of Gluconacetobacter. PCR-RFLP of the 16S rDNA and 16Se23S rDNA combining the different restriction endonucleases, allow the identication of the AAB in a shorter period of time, compared with the timeconsuming techniques (such as DNAeDNA hybridization). The use of these techniques for AAB differentiation is proposed for routine laboratory analysis because of its easiness, the general use of a single PCR and limited restriction analysis, and for the low cost as compared to the techniques used to identify the novel AAB species (Gonzalez, Guillamon, et al., 2006; Trcek, 2005). Ruiz, Poblet, Mas, and Guillamon (2000) used this method for the identication of AAB isolated from wine fermentations. In the study, the same degree of distinction as that for the 16S rDNA analysis was obtained within reference strains of AAB by PCR-RFLP of the 16Se23S rDNA ITS. However, 16Se23S rDNA ITS restriction patterns of strains isolated from wine did not mach those of any of the reference strains. Thus, it is concluded that PCR-RFLP of the 16Se23S rDNA ITS is not a useful method to identify isolates of AAB at the species level, although it may be an adequate method to detect intraspecic differentiation (Ruiz et al., 2000).

Gonzalez, Guillamon, et al. (2006), Ruiz et al. (2000), Sievers, Lorenzo, Gianotti, Boesch, and Teuber (1996), Trcek and Teuber (2002); Trcek (2005) Cleenwerck et al. (2002), Lisdiyanti et al. (2001) Andorra, Landi, Mas, Guillam n, and Esteve-Zarzoso (2008), De Vero et al. (2006); De Vero and Giudici (2008), Haruta et al. (2006), Ilabaca et al., 2008; Lopez et al. (2003) Blasco, Ferrer, and Pardo (2003), Franke et al. (1999), Franke-Whittle, OShea, Leonard, and Sly (2005) Andorra et al. (2008), Gammon et al. (2006), Gonzalez, Hierro, et al. (2006) Gonzalez, Hierro, et al. (2006) Du Toit et al. (2005), Mesa, Macias, Cantero, and Barja (2003) Torija et al. (2010) Cleenwerck et al. (2009) Bartowsky et al. (2003), Nanda et al. (2001) Gonzales (2005), Nanda et al. (2001), Vegas et al. (2010) Gonzales (2005)

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AAB presence in Chilean vinegars was analyzed by using 16S rRNA gene, obtained by PCR amplications of DNA and bacterial composition was analyzed by RFLP-PCR of 16S rRNA gene, Temporal Temperature Gradient Gel Electrophoresis (TTGE) separation of amplicons containing region V3eV5 of 16S rRNA gene and cloning of those amplicons (Ilabaca, Navarrete, Mardones, Romero, & Mas, 2008). The result of the study showed that TTGE allows a quick insight into overall and rough diversity, while cloning allows enumeration of different species and observation of ne molecular diversity. Thus, both methods complement each other in offering a view of quantitative microbial diversity. Gluconacetobacter xylinus, Gluconacetobacter europaeus and Gluconacetobacter intermedius could not be differentiated with the methods used, because of the sequence similarity of these species. PCR-DGGE technique, which is useful to test the diversity of the bacterial community as TTGE, was used to determine the microbial population of rice vinegar and traditional balsamic vinegar (De Vero et al., 2006; Haruta et al., 2006). De Vero and Giudici (2008) reported that species, which are recovered from vinegar fermentation and mainly distributed in the genera Acetobacter, Gluconobacter and Gluconacetobacter, can be grouped more frequently by PCR-DGGE. On the other hand, the limitation of DGGE methods is that the identied species cannot be quantied. Only few studies developed methods for AAB quantication. Most of the quantication methods such as Fluorescence in situ hybridization (FISH), Epiuorescence and real-time PCR (RT-PCR) have been designed to detect the presence and quantify AAB as a group, without identication at the species level. However, recently, Torija et al. (2010) developed a rapid and specic quantitative PCR to identify and quantify some AAB species present in wine and vinegar matrices. To do so, they designed TaqManeMGB probes as highly sensitive and specic tool for A. pasteurianus, Acetobacter aceti, Gluconacetobacter hansenii, Ga. europaeus and Gluconobacter oxydans, which are the main species detected in wine and vinegar, from the 16 S rRNA gene. The reliability of the primers and probes designed to detect different species of AAB were conrmed by using previously identied 40 AAB strains with RFLPsePCR of 16S rRNA gene and 16S rRNA gene sequencing (Table 5). RAPD-PCR (randomly amplied polymorphic DNA) has successfully been used to differentiate A. pasteurianus strains isolated from spoiled red wine (Bartowsky, Xia, Gibson, Fleet, & Henschke, 2003) and to characterize AAB in rice vinegar (Nanda et al., 2001). Amplication of repetitive bacterial DNA elements through the polymerase chain reaction (rep-PCR ngerprinting) using the (GTG)5 primer ((GTG)5-PCR ngerprinting), was found a promising genotypic tool for rapid and reliable speciation of AAB (De Vuyst et al., 2008). On the other hand, amplied fragment length polymorphism (AFLP) DNA ngerprinting is found suitable for accurate identication and classication of a broad range of AAB, as well as for

the determination of intraspecic genetic diversity (Cleenwerck, de Wachter, Gonzalez, de Vuyst, & de Vos, 2009). Real-time PCR and nested PCR for enumerating and detecting AAB were studied and no signicant differences were found between real-time PCR and the traditional techniques (colony and microscope counting). Nested PCR is also found useful for detecting AAB in environmental samples (Gonzalez, Hierro, et al., 2006). Although real-time PCR is accurate, it is also an expensive and complex technique. Restriction Fragment Length Polymorphism (RFLP) of amplied 16S rDNA, and amplication by polymerase chain reaction of Enterobacterial Repetitive Intergenic Consensus (ERIC-PCR), Repetitive Extragenic Palindromic (REP-PCR) and (GTG)5-rep-PCR techniques were successfully used to identify AAB in wine and wine vinegar (Gonzalez, Hierro, Poblet, Mas, & Guillamon, 2005; Vegas et al., 2010). Both ERIC-PCR and (GTG)5rep-PCR were used for typing AAB at the strain level and the results of both techniques were found similar, although ERIC-PCR yielded slightly higher polymorphism (Vegas et al., 2010). It can be seen that there are many methods to identify AAB species. These group of bacteria strongly correlated at the phylogenetic level and have phenotypic characteristics that are similar to one another. Therefore, a polyphasic study is the recommended technique for an accurate identication of AAB strains (Cleenwerck & de Vos, 2008). 4. Sources of AAB AAB are widespread in nature and a large number of strains of AAB have been isolated from variety of sources (Table 6). As it can be seen from the table, AAB belonging to the genus Acetobacter have been isolated more frequently than those of Gluconobacter while occurrence of Acidomonas, Kozakia, Swaminathania, Saccharibacter, Neoasaia, Granulibacter, Tanticharoenia and Ameyamaea strains is rather rare in common isolation sources. For example, the isolation sources of Acidomonas methanolica are quite unique. It could not be isolated from owers and fruits. Acidomonas strains isolated mostly from sludge (Uhlig, Karbaum, & Steudel, 1986; Urakami, Tamaoka, Suzuki, & Komagata, 1989). Yamada et al. (1999) were isolated sixty-four of AAB from Indonesian sources such as fruits, owers and fermented foods and identied them as Acetobacter strains (fortyve isolates), Gluconacetobacter strains (eight isolates) and Gluconobacter strains (eleven isolates). AAB were also isolated from fruits collected in Thailand. Isolates, belong to A. pasteurianus were found in fruits of apple, banana, grape, guava, jack fruit, jujube, kafr lime, langsat, longkong, longan, mango, mangosteen, orange, papaya, peach, pineapple, passion fruit, rose apple, rambutan, rakam, sapodilla, star gooseberry, strawberry, sugar apple, tamarind, water melon, tomato and palm juice, while Acetobacter orientalis and Gluconacetobacter liquefaciens were found in star fruits and palm juice, respectively (Seearunruangchai et al., 2004).

Table 5 Species identication of AAB strains isolated during vinegar acetication by different techniques. Origin of the isolates Wine vinegar (France) Traditional balsamic vinegar (Italy) Wine vinegar (France) Traditional balsamic vinegar (Italy) Submerged vinegar (Spain) Wine vinegar (Spain) Wine vinegar (Spain)
a

Number of isolates 19 2 4 7 6 1 1

RFLPsePCR 16S rRNA gene A. pasteurianus A. pasteurianus Ga. europaeus Ga. europaeus Ga. europaeus G. oxydans Ga. intermedius

RT-PCR with TaqManeMGB probe A. pasteurianus A. pasteurianus Ga. europaeus Ga. europaeus Ga. europaeus G. oxydans Nda

No detection by any of ve MGB probes tested.Table is taken from Torija et al. (2010).

652 Table 6 Isolation sources of acetic acid bacteria. Sources Coffea arabica Coffee plants Fermented cocoa bean Species Ga. diazotrophicus

I.Y. Sengun, S. Karabiyikli / Food Control 22 (2011) 647e656

Reference Jimenez-Salgado et al. (1997), Madhaiyana et al. (2004) Fuentes-Ramrez et al., 2001

Tropical fruits (coconut, mango, guava, sapodilla etc.)

Rotting apple Corn roots Cherry (Prunus sp.) Strawberry Grape Dried fruit Flowers (ixora, lantana etc.)

Flowers of red ginger Pollen Beer

Ga. azotocaptans, Ga. johannae A. pasteurianus, Ardhana and Fleet (2003), A. syzgii or Carr et al. (1979), A. lovaniensis-like and De Vuyst et al. (2008), A. tropicalis-like; Lagunes-Glvez et al. (2007), A. syzygii, Nielsen et al. (2007), Schwan A. pasteurianus, and Wheals (2004) A. tropicalis, A. malorum, G. oxydans A. aceti, A. pasteurianus A. lovaniensis A. orleanensis, Lisdiyanti et al. (2003) A. lovaniensis, A. syzygii, A. indonesiensis, A. cibinongensis, A. tropicalis, A. orientalis, G. oxydans, G. frateurii, Ga. hansenii, F. aurantia A. malorum Cleenwerck et al. (2002) G. azotocaptans Menhaz, Weselowski, and Lazarovits (2006) G cerinus Yamada and Akita (1984) G. frateurii Mason and Claus (1989) G. oxydans, Joyeux et al. (1984), A. aceti Gonzales (2005) Ga. liquefaciens Yamada et al. (1997) A. orleanensis, Lisdiyanti et al. (2003), A. indonesiensis, Yukphan et al. (2009) A. syzygii, A. orientalis, G. oxydans, G. frateurii, As. bogorensis, As. siamensis, As. indonesiensis, F. aurantia Am. chiangmaiensis Sa. oricola A. cerevisiae A. pasteurianus, G. oxydans Ga. diazotrophicus Ga. sacchari K. baliensis G. diazotrophicus, A. peroxydans Sw. salitolerans Jojima et al. (2004) Cleenwerck et al. (2002), Skerman, McGowan, and Sneath (1980) Yamada et al. (1997) Franke et al. (1999) Lisdiyanti et al. (2003) Muthukumarasamy et al. (2005) Loganathan and Nair (2004)

known as a spoiling agent of beer and wine. Gluconobacter spp., which are resistant to preservatives such as sorbic acid, benzoic acid, and dimethyldicarbonate, are the most frequently encountered cause of bacterial spoilage of soft drinks at low pH (Raspor & Goranovic, 2008). When basic hygienic and technical procedures are not correctly performed, AAB produce acetic acid in beverages under aerobic/microaerophilic conditions and cause low pH and ethanol content, pack swelling, vinegary off-avors, turbidity and ropiness (Guizani & Mothershaw, 2006; Odhav, 2004; Stratford & Capell, 2003). Cultures of AAB are used in the commercial production of vinegar. The oxidation of ethanol to acetic acid, which is important in vinegar production, is the best known characteristics of AAB. However, these bacteria also oxidize glucose to gluconic acid, galactose to galactonic acid, arabinose to arabonic acid, and so on. This property of underoxidation is exploited in the manufacture of ascorbic acid (vitamin C). Ascorbic acid can be formed from sorbose, but chemical synthesis of sorbose is difcult. It is, however, conveniently obtainable from AAB, which oxidize sorbitol (a readily available sugar alcohol) only to sorbose, a process called bioconversion. Another interesting property of some AAB is their ability to synthesize cellulose. The formed cellulose does not differ signicantly from that of plant cellulose, with the exception that it is pure and not mixed with other polymers and is formed as a matrix outside the wall where the bacteria become embedded in the species of AAB grow in an unshaken vessel. They form a surface pellicle of cellulose in which the bacteria develop (Madigan & Martinko, 2006). Researchers that focused on the isolation and identication of AAB, have mainly investigated vinegar, wine, cocoa and coffee as a research material because of the industrial values they have. These studies are summarized below: 5.1. AAB in vinegar The best known industrial application of AAB is vinegar production. Several types of vinegars are produced worldwide; they differ for raw materials, technologies and use (Solieri & Giudici, 2009). There are two well dened methods to produce vinegar: the traditional and the submerged. In the submerged method, which has a short production time (24e48 h), AAB are submerged in the liquid and oxygen is constantly added constantly. In traditional method also called as surface culture method AAB grow on the media surface where oxygen concentration is high. Therefore, acetic acid production takes long time and resulting vinegar is of high quality (Tesfaye, Morales, Garca-Parrilla, & Troncoso, 2002). In traditional methods, oxidation is started by seed-vinegar, also called mother of vinegar, an undened starter culture obtained from previous vinegar. Few ecological studies of AAB in vinegars have been made, and those were mainly focused on industrial vinegars, persimmon vinegar, rice vinegar, wine vinegar and traditional balsamic vinegar (Vegas et al., 2010). In the early studies, AAB isolated from vinegar fermentations were identied as Acetobacter acidophilum, (Wiame, Harpigny, & Dothey, 1959), Acetobacter polyoxogenes (Entani, Ohmori, Masai, & Suzuki, 1985), A. hansenii and A. pasteurianus (Kittelmann, Stamm, Follmann, & Triiper, 1989). However, studies focused on identication of AAB are spread on a wide period of time with a signicant gap between older papers and current AAB taxonomy (Table 7). The population dynamics of AAB in traditional wine vinegar, which is obtained by spontaneous wine acetication, was studied by Vegas et al. (2010). In this study, the main species throughout the process was found as A. pasteurianus which has been mentioned in a previous study in traditional wine vinegar (Ilabaca et al., 2008) and rice vinegar production (Haruta et al., 2006; Nanda et al., 2001).

Sugarcane roots Mealy bug from sugar cane Palm brown sugar, ragi Wetland rice Wild rice

Abbreviations: A.: Acetobacter, G.: Gluconobacter, Ga.: Gluconacetobacter, K.: Kozakia, As.: Asaia, Am.: Ameyamaea, Sa.: Saccharibacter, Sw.: Swaminathania, F.: Frateuria (this genus differently classied into the Gammaproteobacteria).

5. Benecial effects of AAB in foods Although AAB can be isolated from various natural sources, they are frequently isolated in alcoholic juices such as hard cider or wine, or from beer. AAB can play not only a positive role in the production of selected foods and beverages, but they can also spoil other foods and beverages, such as wine, beer, soft drinks, and fruits. AAB of the genera Acetobacter and Gluconobacter are

I.Y. Sengun, S. Karabiyikli / Food Control 22 (2011) 647e656 Table 7 AAB species isolated from different kinds of vinegar. Source Rice vinegar Industrial vinegar Species A. pasteurianus Ga. europaeus A. oboediens, A. pomorum A. intermedius Ga. entanii Ga. europaeus, Ga. hansenii Ga. xylinus, A. acet, A. pasteurianus Ga. europaeus, Ga. hansenii A. pasteurianu, A. malorum A. pasteurianus, Ga. europaeus Reference

653

Haruta et al. (2006), Nanda et al. (2001) Boesch, Trcek, Sievers, and Teuber (1998), Schller, Hertel, and Hammes (2000), Sievers et al. (1992), Sokollek et al. (1998b), Yamada et al., 1997

Traditional balsamic vinegar

Gullo et al. (2006), Gullo and Giudici (2006)

Traditional wine vinegar

Ilabaca et al. (2008), Vegas et al. (2010)

Abbreviations: A.: Acetobacter; Ga.: Gluconacetobacter.

Vegas et al. (2010) observed that Ga. europaeus was proliferated when the acetic acid concentration was appropriate, in their study. Thus, it is concluded that the starting strains were better prepared to survive at low acetic acid concentrations and high ethanol, whereas the ones that nished the acetication might be more acetic acid tolerant. They also reported that the longer operating of wine vinegar may lead to a greater diversity of AAB strains, which improves the chances of a good acetication. Using AAB as a starter culture in the production of vinegar may lead to an improved fermentation process and an enhanced product quality (Gullo & Giudici, 2008). Zahoor, Siddique, and Farooq (2006) reported that, in Pakistan, a mixed culture of Acetobacter is used for the production of acetic acid but no attention is given towards its proper maintenance and culture is contaminated with other kinds of microorganisms. So for that reason, they conducted a research to isolate a pure culture of A. aceti for vinegar production and produced vinegar from the pure culture obtained, under controlled conditions, which has better organoleptic properties than commercial vinegar. Although vinegar is used for giving taste to foods, it is also used for sanitizing effect, especially for salad vegetables, which are consumed raw (Sengun & Karapinar, 2004, 2005a, 2005b). It is reported that AAB, that produce acetic acid during the fermentation period, are mainly responsible from the sanitizing effect of vinegar (Costa, Thomaz-Soccol, Paulino, & de Costa, 2009; Karapinar & Gonul, 1992a, 1992b). 5.2. AAB in cocoa Characteristic avor of cocoa is developed through a fermentation of cocoa beans. At the beginning of fermentation yeast and LAB are dominated because of the low pH value and the high sugar content of the pulp while AAB predominate with temperature rises and alcohol accumulates (Biehl & Ziegleder, 2003; Nielsen et al., 2007; Thompson, Miller, & Lopez, 2001). Growth behaviour of AAB during different stages of cocoa fermentation was studied by many researchers. Nielsen et al. (2007) reported that Acetobacter syzygii, A. pasteurianus and A. tropicalis were the predominant AAB during Ghanaian cocoa fermentation. Similar fermentation was investigated by De Vuyst et al. (2008) and A. pasteurianus, A. syzgii or A. lovaniensis-like and A. tropicalis-like strains were identied from Ghanaian cocoa bean fermentation. A. pasteurianus and A. aceti strains have been reported to form a signicant part of the AAB community during cocoa fermentations in Ghana (heap), Indonesia (box) and Brazil (box) (Ardhana & Fleet, 2003; Carr, Davies, & Dougan, 1979; Schwan & Wheals, 2004). A. lovaniensis was isolated from the cocoa fermentation in the Dominican Republic as the predominating AAB (Lagunes-Glvez, Loiseau, Paredes, Barel, & Guiraud, 2007). Although Acetobecter spp. were mainly isolated from cocoa productions as predominant

AAB, Gluconobacter spp. were also found in cocoa fermentations (Biehl & Ziegleder, 2003; Nielsen et al., 2007). 5.3. AAB in coffee Coffea arabica (arabica) and C. canephora (robusta), which are dominant Coffea species, are processed by wet or dry methods (Schwan & Wheals, 2003). The microbiota involved in dry processing are much more varied and complex than those found during wet fermentation, but the role of microorganisms found in coffee fermentation by natural processing is still unknown (Silva, Batista, Abreu, Dias, & Schwan, 2008). Microbial prole of AAB in coffee fermentation was studied by Silva et al. (2008), Silva, Schwan, Dias, and Wheals (2000). In these studies, bacteria, yeast and lamentous fungi were isolated during coffee processing, while no AAB were identied. On the other hand, two species within the genus Gluconacetobacter, associated to coffee plants, were described in Mexico: Ga. johannae and Ga. azotocaptans (Fuentes-Ramrez et al., 2001). Ga. diazotrophicus, which is known as nitrojen-xing AAB, were also isolated from coffee plants (C. arabica L.) (Jimenez-Salgado et al., 1997; Madhaiyana et al., 2004). 5.4. AAB in wine AAB play a negative role in winemaking since they increase the volatile acidity of wines. They can survive in the various phases of alcoholic fermentation and it is very important to control their presence and ulterior development to obtain good quality wines (Gonzalez, Hierro, et al., 2006). Du Toit and Lambrechts (2002) investigated the occurrence of AAB in South African red wine fermentations. The initial AAB numbers were found ranging from 106e107 (for 1998 must) to 104e105 cfu/ml (for the 1999 must), decreasing 102e103 cfu/ml in musts having a low pH (3.6) and increasing during fermentation. Many researchers have identied different strains of AAB, found in wine fermentations (Table 8). Growth behaviour of AAB during different stages of vinication was studied by Gonzalez et al. (2005). G. oxydans was found predominant species in fresh must and the rst stages of fermentation. On the other hand, only few species survived the transfer from grapes to must and the ones that did were mostly A. aceti species. It is reported that the anaerobic conditions of the alcoholic fermentation make conditions unsuitable for the growth of AAB. When the wine is transferred from fermentation tanks to other storage vessels, agitation and aeration processes encourage the growth of surviving AAB populations (Drysdale & Fleet, 1988). Bacterial spoilage has also recently been reported to occur in packaged wine such as vertically upright bottles (Bartowsky et al., 2003). This is visually evident as a distinctive ring of bacterial biomass that is deposited on the neck of the bottle at the interface between the

654 Table 8 AAB species isolated from different kinds of wine. Source Bottled red wine Red wine fermentation Dao region of Portugal red wine South African red wine Austrian wine White wine

I.Y. Sengun, S. Karabiyikli / Food Control 22 (2011) 647e656

Species A. pasteurianus G. oxydans, Ga. hansenii, A. aceti A. nitrogenigens A. oeni G.oxydans, A. pasteurianus, A. hansenii, A. liquefaciens A. tropicalis G.oxydans, A. pasteurianus, A. aceti

Reference Bartowsky et al. (2003) Gonzales (2005) Dutta and Gachhui (2006) Silva et al. (2006) Du Toit and Lambrechts (2002) Silhavy and Mandl (2006) Joyeux et al. (1984)

wine and the air headspace. Higher temperature of wine storage and higher wine pH favored the development and the metabolism of AAB (Joyeux, Lafon-Lafourcade, & Ribereau-Gayon, 1984). The factors affecting the development of AAB during the winemaking process are the pH of the must and wine, the temperature, the ethanol concentration and the dissolved oxygen in the media (Drysdale & Fleet,1988). In red wines, AAB were studied during aging in barrels and enumeration on plate counts showed that the level of population was closely linked to the dissolution of oxygen. However it is also found that they were always present even in the absence of oxygen in very low levels, which means that a large proportion of the population was in VBNC when deprived of oxygen (Funel, 2005). It is reported that the presence of these strictly aerobic bacteria in grape must and during wine maturation can be controlled by eliminating, or at least limiting oxygen, as essential growth factor. The effects of SO2, which is used as an antioxidant and antimicrobial agent during winemaking, on the survival and growth of AAB have not been well investigated. A recent study demonstrated that low concentrations of SO2 (0.35 mg/l molecular SO2) were found to have minimal effect on viability and cultivability of an A. pasteurianus strain, whereas higher concentrations were effective (1.2 mg/l molecular SO2) (Du Toit, Pretorius, & Lonvaud-Funel, 2005). Ubeda and Briones (1999) screened 68 samples of ltered and unltered wines for the presence of AAB and observed that 13% of the unltered wines contained AAB while ltered samples were not containing them. Although exclusion by sterile ltration is a possible control measure, membrane fouling, cost and time delays can limit application with red wines. Blanketing wine with an inert gas such as carbon dioxide, and ensuring that storage containers are completely lled with wine to minimize contact the headspace of air can be applied to prevent the growth of AAB (Bartowsky & Henschke, 2008). 6. Conclusion The classication of AAB has not been fully established yet. The taxonomic resolution of molecular techniques used for the characterization of AAB is not clear. Polyphasic analysis is recommended as the best approach for classifying this group of bacteria. Researchers mainly focused on wine and vinegar associated AAB which have a great importance in food industry. They are responsible for vinegar fermentation producing acetic acid from ethanol while they are found in wine in a detrimental way. Isolation, cultivation and preservation difculties restrict the usage of AAB in vinegar production as a starter culture. Future studies should overcome these disadvantages and focus on the starter culture selection and process set up for better process control in vinegar production. References
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