Abstract
Leuconostocaceae are lactic acid bacteria (LAB) belonging to order Lactobacillales. The family consists of genera Leuconostoc, Weissella, Oenococcus, and Fructobacillus. The genus Leuconostoc was described already in 1878 by van Tieghem. The oldest described species belonging to Oenococcus and Fructobacillus were originally described as Leuconostoc spp. but were later reclassified based on phenotypic and phylogenetic studies. Genus Weissella contains species originally classified as Leuconostoc or Lactobacillus spp.
Like other LAB, Leuconostocaceae are Gram positive, catalase negative, and chemoorganotrophic. They grow in rich media supplemented with growth factors and amino acids and generate energy by substrate-level phosphorylation. Leuconostocaceae ferment glucose heterofermentatively yielding lactic acid, CO2, ethanol, and/or acetate.
Leuconostocaceae are found in environments with high nutrient content, e.g., on green vegetation, roots, and food. Within LAB, Leuconostocaceae are characterized by their adaptable fermentation patterns that enable efficient generation of ATP from carbohydrates and, consequently, enhanced growth. Due to their ability to grow rapidly in rich media under elevated CO2 concentration at moderate temperatures, Leuconostocaceae are competitive in various food environments and contribute to a number of fermentation processes. The diverse fermentation substrates and products of Leuconostocaceae may cause desired or undesired effects on the organoleptic quality of foods.
This contribution is a modified and updated version of previous descriptions of the family (Schleifer, 2009) and the included genera (Björkroth et al., 2009; Björkroth and Holzapfel, 2006; Dicks and Holzapfel, 2009; Holzapfel et al., 2009).
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Keywords
- Lactic Acid Bacterium
- Starter Culture
- Lactic Acid Bacterium Strain
- Leuconostoc Mesenteroides
- Malolactic Fermentation
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.
Taxonomy, Historical and Current
The family Leuconostocaceae belongs to the order Lactobacillales. Since the late 2000s, this family has contained the genera of Fructobacillus, Leuconostoc, Oenococcus, and Weissella. The genus Leuconostoc has been the hub of taxonomic reclassifications leading to description of the three other genera.
Historically, Leuconostoc mesenteroides was first mentioned by Van Tieghem in 1878 (Van Tieghem 1878) in an article called “Sur la Gomme de Sucrerie (Leuconostoc mesenteroides).” The description of the genus Leuconostoc is following today the lines published by Garvie (1986). The taxonomic revisions affecting leuconostocs have mainly been due to implementation of phylogenetic analyses and the studies utilizing polyphasic taxonomy approaches. The first phylogenetic analyses of the 16S rRNA gene sequences (Martinez-Murcia and Collins 1990; Martinez-Murcia et al. 1993) resulted in recognition of three distinct lineages within leuconostocs. They were referred as the genus Leuconostoc sensu stricto, the Leuconostoc paramesenteroides group, and Leuconostoc oenos. A new genus Weissella (Collins et al. 1993) was described to accommodate members of the so-called L. paramesenteroides group (including L. paramesenteroides and some atypical, heterofermentative lactobacilli). In addition, L. oenos has been reclassified as Oenococcus oeni (Dicks et al. 1995). More recently, some atypical leuconostocs of plant origin including Leuconostoc durionis, Leuconostoc ficulneum, Leuconostoc fructosum, and Leuconostoc pseudoficulneum have been assigned to the new genus Fructobacillus (Endo and Okada 2008). After these reclassifications, the genus Leuconostoc includes 13 validly published species names (Table 18.1) with L. mesenteroides as the type species. L. mesenteroides is the only species divided into subspecies which have not been established based on phylogenetic or genomic boarders. According to Vancanneyt et al. (2006), Leuconostoc argentinum (Dicks et al. 1993) is a later synonym of Leuconostoc lactis.
With the exception of Leuconostoc fallax, 16S rRNA gene sequence similarities among the type strains of Leuconostoc spp. are high, varying from 97.3 % to 99.5 % (Björkroth and Holzapfel 2006). 16S rRNA gene sequence analysis further divides leuconostocs into three evolutionary branches including Leuconostoc citreum, Leuconostoc holzapfelii, Leuconostoc lactis, and Leuconostoc palmae in the first branch; L. mesenteroides and L. pseudomesenteroides in the second; and Leuconostoc carnosum, Leuconostoc gasicomitatum, Leuconostoc gelidum, Leuconostoc inhae, and Leuconostoc kimchii in the third branch, whereas L. fallax is genetically more distinct from the other Leuconostoc species (Fig. 18.1).
In addition to the 16S rRNA gene, the loci of housekeeping genes atpA, dnaK, pheS, recN, and rpoA in leuconostocs have been analyzed. The phylogenetic trees constructed on analyses of pheS, rpoA, and atpA loci offered discriminatory power for differentiation of species within the genus Leuconostoc and were roughly in agreement with 16S rRNA gene-based phylogeny (Ehrmann et al. 2009; De Bruyne et al. 2007). Comparative sequencing of the additional phylogenetic markers dnaK and recA confirmed the 16S rRNA gene tree topology in the study describing L. palmae (Ehrmann et al. 2009). Arahal et al. (2008) studied the usefulness of recN locus and concluded that also recN can serve as a phylogenetic marker as well as a tool for species identification. Congruence of evolutionary analyses inside the Leuconostoc–Oenococcus–Weissella clade has been assessed by comparative phylogenetic analyses of 16S rRNA, dnaA, gyrB, rpoC, and dnaK housekeeping genes (Chelo et al. 2007). Phylogenies obtained with the different genes were in overall good agreement, and a well-supported almost fully resolved phylogenetic tree was obtained when the combined sequence data were analyzed using a Bayesian approach.
Within the genus Weissella, several new species have been characterized during the last 5 years, and the genus currently comprises 17 species (Table 18.2). The description for the genus is as published by Collins et al. (1993). The type species is Weissella viridescens (Niven and Evans 1957) which is synonymous to Lactobacillus viridescens.
The genus Weissella was proposed by Collins et al. (1993), and the first species included in this genus comprises species previously classified as Leuconostoc or Lactobacillus. L. paramesenteroides (Garvie 1967a), L. viridescens (Niven and Evans 1957; Kandler and Abo-Elnaga 1966), Lactobacillus confusus (Holzapfel and Van Wyk 1982; Holzapfel and Kandler 1969), Lactobacillus kandleri (Holzapfel and Van Wyk 1982), Lactobacillus minor (Kandler et al. 1983), and Lactobacillus halotolerans (Kandler et al. 1983) kept their specific epithets and were reclassified as Weissella paramesenteroides, W. viridescens, Weissella confusa, W. kandleri, Weissella minor, and Weissella halotolerans, respectively. These species were followed by inclusion of Weissella hellenica (Collins et al. 1993), Weissella thailandensis (Tanasupawat et al. 2000), Weissella cibaria (Björkroth et al. 2002), Weissella soli (Magnusson et al. 2002), and Weissella koreensis (Lee et al. 2002). In addition, Weissella kimchii was proposed by Choi et al. (2002), but it was found as a later heterotypic synonym of Weissella cibaria (Ennahar and Cai 2004). Weissella ghanensis (De Bruyne et al. 2008), Weissella beninensis (Padonou et al. 2010) and Weissella fabaria (De Bruyne et al. 2010), Weissella ceti (Vela et al. 2011), Weissella fabalis (Snauwaert et al. 2013), and Weissella oryzae (Tohno et al. 2012) are the latest species suggested to the genus Weissella.
W. confusa, W. cibaria, W. halotolerans, W. hellenica, W. kandleri, W. koreensis, W. minor, W. paramesenteroides, W. soli, W. thailandensis, and W. viridescens share 93.9–99.2 % 16S rRNA encoding gene sequence similarity (Björkroth et al. 2009). Among the recently described species, sequence similarity analyses (Snauwaert et al. 2013) indicated that W. fabalis type strain shares the highest sequence similarities with the type strains of W. fabaria (97.7 %), W. ghanensis (93.3 %), and W. beninensis (93.4 %). Five main phylogenetic branches exist based on the 16S rRNA encoding gene analyses. W. hellenica, W. paramesenteroides, and W. thailandensis branch together, as do W. cibaria and W. confusa. Two other branches are formed by W. ceti, W. minor, W. halotolerans, and W. viridescens in one branch and W. kandleri, W. koreensis, W. oryzae, and W. soli in another. W. fabali s (Snauwaert et al. 2013), W. fabaria (De Bruyne et al. 2010), and W. ghanensis (De Bruyne et al. 2008) form the fifth branch distinct from the other species within the genus.
Oenococcus oeni, type species of the genus Oenococcus, had been formerly classified as Leuconostoc oenos (Garvie 1967b). The genus Oenococcus currently includes two species, which are Oenococcus kitaharae and O. oeni. O. oeni was formerly classified as Leuconostoc oenos and reclassified as a member of the novel genus Oenococcus (Dicks et al. 1995). A candidate of novel Oenococcus species might have been isolated from bioethanol fermenting tank (Lucena et al. 2010), which has not been characterized at a time of writing (September, 2012). Originally, the species O. oeni was considered as a genetically homogeneous organism based on the sequencing of rRNA operon (Jeune and Lonvaud-Funel 1997; Zavaleta et al. 1996). However, recent study by Bridier et al. (2010) found diverse genetic groups in the species by multilocus sequence typing (MLST) with sequences of several housekeeping genes. Reclassification of L. oenos into the genus Oenococcus was carried out based on its unique phylogenetic position, physiological characteristics, total soluble cell protein analysis, and several biochemical characteristics by Dicks et al. (1995). Already in 1993 Martinez-Murcia et al. (1993) showed by comparison of both 16S and 23SrRNA sequences that L. oenos does not belong to the same line of descent with the L. sensu stricto organisms or L. paramesenteroides group of species (the current genus Weissella). The second species, O. kitaharae, was described from compost of distilled shochu residue in Japan (Endo and Okada 2006). These two species share 96.0 % similarity based on 16S rRNA gene sequence. Sequence similarities with other members of family Leuconostocaceae are less than 85 %. The high level of phylogenetic divergence of the genus Oenococcus compared to that of the other lactic acid bacteria might be explained by the absence of the mismatch mutation repair system in oenococci, which causes a high mutation rate, an excess of recombination, and a rapid genetic evolution (Marcobal et al. 2008). Based on pheS sequences, Oenococcus spp. still belong to the family Leuconostocaceae but share different relationships with the other genera when compared to 16S rRNA gene sequence analyses. Sequence similarity of partial pheS gene between the two Oenococcus spp. is approximately 75 % and less than 70 % between Oenococcus spp. and other members in the family Leuconostocaceae. Related to the phylogeny, an interesting debate over its evolution speed has occurred. Because of a long branch in the 16S rRNA phylogenetic tree, O. oeni is regarded as “rapidly evolving” species (Yang and Woese 1989). This hypothesis was at first questioned based on data generated by rpoB gene sequences (Morse et al. 1996), but supported by comparative genome analyses of different species of lactic acid bacteria (LAB), including O. oeni (Makarova et al. 2006).
In addition to the 16S rRNA gene phylogeny, analysis with pheS (De Bruyne et al. 2010) and recN (Arahal et al. 2008) loci has been done. Congruence of evolutionary relationships inside the Leuconostoc–Oenococcus–Weissella clade has been assessed by phylogenetic analyses of 16SrRNA, dnaA, gyrB, rpoC, and dnaK (Chelo et al. 2007) housekeeping genes. Phylogenies obtained with the different genes were in overall good agreement, and a well-supported, almost fully resolved phylogenetic tree was obtained when the combined data were analyzed in a Bayesian approach.
The genus Fructobacillus currently includes five species. They are F. durionis (Leisner et al. 2005), F. ficulneus (Antunes et al. 2002), F. fructosus (Kodama 1956), F. pseudoficulneus (Chambel et al. 2006), and F. tropaeoli (Endo et al. 2011). With the exception of F. tropaeoli, these species were formerly classified as Leuconostoc species (Endo and Okada 2008). Fructobacillus fructosus, type species of the genus Fructobacillus, had been firstly classified as Lactobacillus fructosus based on morphological and physiological characteristics and later reclassified to Leuconostoc fructosum based on its phylogenetic position (Kodama 1956; Antunes et al. 2002). Leuconostoc fructosum was re-reclassified to F. fructosus based on physiological and morphological characteristics and its phylogenetic position (Endo and Okada 2008). Based on the 16S rRNA gene sequences, Fructobacillus species are phylogenetically separated into two subclusters. The first subcluster contains F. fructosus and F. durionis (97.9 % sequence similarity), and the second contains Fructobacillus ficulneus, F. pseudoficulneus, and F. tropaeoli (98.0–99.2 % sequence similarities). The sequence similarity between the two groups ranges from 94.2 % to 99.4 %. Fructobacillus species has been also genetically characterized based on sequences of 16S–23S rRNA gene intergenic spacer regions (ISR), rpoC and recA. Phylogenetic analysis based on the ISR and rpoC gene shows similar clustering to that based on 16S rRNA gene, but phylogenetic analysis based on recA gene shows different clustering (Endo and Okada 2008; Endo et al. 2011).
Molecular Analyses
Classification of the members of the family Leuconostocaceae using adequate molecular methods gives faster and more consistent and reliable results than schemes based on phenotypic characters. The molecular analyses have provided deeper insights into the phylogeny of the already assigned taxons within Leuconostocaceae and led to reclassification of species. In addition to the taxonomy and phylogeny, the motivation of many molecular studies has been more practical: to distinguish and identify relevant strains among closely related isolates. For the molecular characterization of Leuconostocaceae, various methods with differing resolving capacity have been reported and proposed; some have proven applicable for species identification, while others provide high discriminatory power and detail strain characterization. The choice of method depends on the scope and purpose of the study as well as on the availability of laboratory facilities. A summary of common molecular methods and their relative performances in differentiation of Leuconostocaceae is discussed below. In many studies cited, the results of two or more molecular methods have been combined to achieve better discrimination and more accurate clustering of the given set of isolates. However, only few studies report systematic comparison of different molecular methods and discuss their limitations for characterizing Leuconostocaceae.
DNA–DNA Hybridization Studies
DNA–DNA hybridization assays have been included in many studies to determine interspecies relationships among Leuconostoc and Weissella species and to reveal whether two isolates should be classified in the same species. Since many closely related species of Fructobacillus, Leuconostoc, or Weissella share high 16S rRNA gene sequence similarity, DNA–DNA hybridization experiments have been necessary to support a proposal for a novel species status.
DNA Fingerprinting
DNA fingerprinting using pulsed field gel electrophoresis (PFGE) and an appropriate restriction endonuclease provides high level of discrimination, allowing differentiation of closely related strains that are indistinguishable by other methods. Several investigators have used PFGE typing for characterizing Leuconostocaceae from dairy, meat, vegetable, and wine-related sources. These studies have demonstrated the success of PFGE typing in differentiating strains in a specific ecosystem or monitoring the presence of particular strains in a mixed population. For instance, PFGE typing has been used in several studies to study strain heterogeneity of O. oeni population during malolactic fermentation of wine (Sato et al. 2001; Vigentini et al. 2009; Zapparoli et al. 2012) as well as during an in-plant investigation of a ham spoilage problem to pinpoint potential sources of harmful L. carnosum contamination (Björkroth et al. 1998).
Another commonly used DNA fingerprinting technique is ribotyping or restriction fragment length polymorphism (RFLP) analysis of 16S and 23S rRNA genes where the detection of ribotyping fingerprint is accomplished by hybridization with probes. Numerical analysis of ribotyping has been included in polyphasic taxonomy studies on Leuconostoc (Björkroth et al. 2000), Fructobacillus (Chambel et al. 2006) and Weissella (Björkroth et al. 2002) and found to provide species level identification with some intraspecies variation. Subsequently, ribotyping has been applied to detect and identify individual species or strains of Leuconostocaceae from various food, animal, and environmental sources. Although ribotyping provides discriminatory capacity for species identification, PFGE appears to be superior for strain differentiation (Björkroth et al. 1998; Vihavainen and Björkroth 2009).
PCR-Based DNA Fingerprinting Methods
Analysis of (fluorescent) amplified fragment length polymorphism (FAFLP or AFLP) fingerprints is another highly discriminatory characterization tool which has proven useful in the differentiation of Leuconostoc (De Bruyne et al. 2007) and Weissella species (De Bruyne et al. 2008, 2010). Furthermore, AFLP has been found valuable in typing of O. oeni strains (Cappello et al. 2008, 2010).
Amplified ribosomal DNA restriction analysis (ARDRA) is a technical variation of ribotyping comprising of restriction enzyme analysis of PCR amplicons from the rrn operon. Several ARDRA procedures targeting to different regions of the rrn operon have been reported; some give limited resolution being mainly applicable for rapid first-stage screening of isolates, while others provide discriminatory power allowing reliable species identification of Leuconostocaceae. For instance, 16S-ARDRA has been used for identification of species of Leuconostocaceae from grape must and wine (Rodas et al. 2003) and fermented sausages (Bonomo et al. 2008). Protocols for 16S-ARDRA employing genus-specific primers for Weissella (Jang et al. 2002) and Leuconostoc (Jang et al. 2003) have been developed to allow identification of Weissella and Leuconostoc species among other phylogenetically related lactic acid bacteria in food. Furthermore, a 16S–23S rRNA spacer ARDRA method has been developed for identification of lactic acid bacteria and proved useful in identifying Leuconostoc species from meat (Chenoll et al. 2003, 2007).
Fingerprinting using randomly amplified polymorphic DNA (RAPD) is another PCR-based tool applied for molecular typing of Leuconostoc, Weissella, and O. oeni. Various studies have demonstrated the success of RADP in monitoring O. oeni strains during winemaking (Bartowsky et al. 2003; Reguant and Bordons 2003; Zapparoli et al. 2000). Other workers have analyzed RAPD fingerprints to differentiate species and strain of Leuconostoc and Weissella from various sources (Aznar and Chenoll 2006; Cibik et al. 2000; De Bruyne et al. 2008; Ehrmann et al. 2009; Nieto-Arribas et al. 2010; Padonou et al. 2010).
Repetitive element palindromic PCR (REP-PCR) with the (GTG)5 primer has been applied for high-throughput screening of large collections of lactic acid bacteria isolates in numerous studies. Numerical analysis of REP-PCR patterns has been reported to be suitable for species identification and for genotypic characterization of Leuconostoc (Bounaix et al. 2010a; Vancanneyt et al. 2006) and Weissella (Bounaix et al. 2010b; Padonou et al. 2010).
DNA Sequencing-Based Analysis
Sequence analysis of 16S rRNA gene or its variable regions are widely applied strategies for classification of lactic acid bacteria and have been used for identification of Leuconostocaceae from various sources. In addition to 16S rRNA gene sequence analysis, phylogenetic analysis of partial sequences of several protein-coding genes such as dnaA, dnaK, gyrB, pheS, recN, rpoA, or rpoC has been reported to be highly discriminatory, allowing differentiation of species and strains within the family Leuconostocaceae (Arahal et al. 2008; Chelo et al. 2007; Ehrmann et al. 2009; De Bruyne et al. 2007, 2010). Furthermore, multilocus sequence typing (MLST) schemes have been proposed and applied for O. oeni (de las Rivas et al. 2004; Bilhere et al. 2009; Bridier et al. 2010). These studies have demonstrated that MLST is a powerful method for typing of O. oeni strains and provides data that can be used for studying genetic diversity, population structure, and evolutionary mechanism of this organism.
Protein Profiling
In addition to various DNA-based molecular techniques, analysis of whole-cell protein pattern by sodium dodecyl sulfate-polyacrylamide gel electrophoresis (SDS-PAGE) has proven useful in the differentiation of closely related Leuconostoc and Weissella and has been widely applied for identification of Leuconostocaceae (Dicks et al. 1990; Björkroth et al. 2002; De Bruyne et al. 2007, 2008, 2010). In addition, matrix-assisted laser desorption/ionization time-of-flight mass spectrometry (MALDI-TOF MS) has been increasingly studied and applied for the identification and typing of lactic acid bacteria. This method is based on the analysis of the structural differences of microbial cells; the mass spectra mainly reflect the heterogeneity of ribosomal proteins and, thus, give a specific profile for each organism. A MALDI-TOF MS profiling method has also been reported for the family Leuconostocaceae (De Bruyne et al. 2011). The results have demonstrated that MALDI-TOF MS profiling is a rapid, cost-effective, and reliable method, allowing classification of most species of Fructobacillus, Leuconostoc, and Weissella (De Bruyne et al. 2011; Snauwaert et al. 2013).
Genomes
Within the family Leuconostocaceae, seven Leuconostoc genomes, one Oenococcus genome, and one Weissella genome have been completed (Table 18.3). In addition, 11 Leuconostoc genomes, 14 Oenococcus genomes, five Weissella genomes, and one Fructobacillus genome are available as draft genomes made up of a few to many contigs. From genome mapping, the genome size of Leuconostocaceae genomes has been estimated to range in size from 1.4 to 2.2 Mb (Chelo et al. 2010), and all completely sequenced genomes also fall within that size range. As noted previously, most Leuconostocaceae strains do contain plasmids, although spontaneous curing of plasmids frequently occurs when these strains are maintained in laboratory conditions (Brito and Paveia 1999).
The analysis of the pan genomes within the homogeneous genera Fructobacillus, Leuconostoc, Oenococcus, and Weissella has shown that the core genome within one species comprises between 67 % and 80 % of a genome (Borneman et al. 2012b; Johansson et al. 2011). This is in agreement with the core genome proportion of 60 % in the highly divergent species Lactobacillus casei (Broadbent et al. 2012). The size of the supragenome for a species is directly proportional to number of sequenced strains until a saturation level is reached. The saturation level corresponds to the size of the complete supragenome and can be calculated when sufficient number of strains have been sequenced (Boissy et al. 2011). The size of the supragenomes characterized for LAB species is two to three times of the size of any individual genome (Boissy et al. 2011; Borneman et al. 2012b; Broadbent et al. 2012).
It has been shown that there is a good correlation between experimentally determined DNA–DNA hybridization (DDH) and digital DDH, calculated from sequence alignment of the genome sequences (Konstantinidis and Tiedje 2005; Auch et al. 2010). This is also the case for the genomes of Leuconostocaceae, although the genomes and experimental DDH are not obtained from the same strains in all cases.
All fully sequenced Leuconostocaceae genomes contain complete or partial prophages. The prophages of Oenococcus have been well characterized (São-José et al. 2004), and they all use tRNA genes as attachment sites in the genome (Borneman et al. 2012b). Genomes from Fructobacillus and Leuconostoc all have four rrn operons, while genomes from Oenococcus have two rrn operons. Weissella have previously been shown to have between six and eight rrn operons (Chelo et al. 2010), but the only completed Weissella genome, W. koreensis, actually have five rrn operons. The rrn operons are usually distributed around the chromosome, except for L. gasicomitatum and L. gelidum, where all four rrn operons are concentrated on the last quarter of the chromosome.
Phenotypic Analyses
Leuconostocaceae are Gram positive, asporogenous, nonmotile (with the exception of Weissella beninensis), chemoorganotrophic, facultative anaerobic, and catalase negative. They are unable to reduce nitrate and grow in rich media supplemented with growth factors and amino acids. Leuconostocaceae generate energy by substrate-level phosphorylation. Glucose is fermented heterofermentatively via 6-phosphogluconate/phosphoketolase pathway yielding lactic acid, CO2, ethanol, and/or acetate. Glucose-6-phosphate dehydrogenase and xylulose-5-phosphoketolase are the key enzymes of the pathway (Garvie 1986). Earlier it was thought that Leuconostocaceae do not have enzyme fructose 1,6-biphosphate aldolase required for homolactic fermentation, but the genomic analyses have shown that the genes encoding this enzyme are relatively common within the family. The main morphological, metabolic, and chemotaxonomic characters of the genera of Leuconostocaceae are shown in Table 18.4.
Leuconostoc AL van Tieghem (1878), 198AL emend. mut. char. Hucker and Pederson (1930), 66AL
Leuconostoc cells are spherical to ellipsoidal but may also resemble short rods, especially when grown in glucose medium or on solid medium. Cells are often seen in pairs or short chains. True cellular capsules are not formed. Some strains produce extracellular dextran, which forms an electron-dense coat on the cell surface.
Leuconostocs develop visible colonies usually only after three to five days of incubation at 25–30 °C. Colonies on commonly used LAB media are smooth, round, grayish white, and less than 1 mm in diameter. Unlike other leuconostocs, most of the Leuconostoc citreum strains are able to form yellow-pigmented colonies (Farrow et al. 1989).
The optimal growth temperature is between 20 °C and 30 °C, although most species are able grow at 37 °C. Growth at 4 °C or below has been reported for L. gelidum, L. carnosum, and L. gasicomitatum (Holzapfel et al. 2009). Some psychrotrophic strains grow poorly at 30 °C (Björkroth et al. 2000). Leuconostocs are non-acidophilic and prefer an initial medium pH of 6.5. Most of the species are unable to grow at pH 4.8. Growth is uniform, except when cells in long chains sediment. In stab cultures, growth is concentrated in the lower two thirds. Growth on surface plates is poor under aerobic conditions, but is stimulated when incubated anaerobically.
All leuconostocs produce predominantly d(−) enantiomer lactic acid from glucose and are unable to hydrolyze arginine. Leuconostoc species are difficult, sometimes impossible, to distinguish by phenotypic routine testing. Many reactions are strain dependent or are, on the other hand, shared between the different species (Table 18.1). Only L. mesenteroides subsp. cremoris can be easily distinguished from the other leuconostocs owing to its poor carbohydrate fermentation capability. Sugars most helpful for the differentiation of Leuconostoc species are l-arabinose, melibiose, and d-xylose.
Leuconostoc spp. metabolize glucose heterofermentatively via 6-phosphogluconate/phosphoketolase pathway, yielding lactic acid, CO2, ethanol, and/or acetate. Characteristics to the pathway are that hexoses are initially oxidized to pentoses resulting in generation of NAD(P)H. Under anaerobic conditions, NAD+ is regenerated by reduction of acetyl-CoA to ethanol in a process that does not produce ATP. However, if other means to oxidize NAD(P)H are available, acetyl-CoA can be converted to acetate which doubles the amount ATP produced per unit of hexose consumed. In the presence of oxygen, strains of L. mesenteroides use NADH oxidases and NADH peroxidases as alternative mechanisms to regenerate NAD+ (Condon 1987). Leuconostocs are also able to re-oxidize NAD(P)H by using pyruvate, fructose, or citrate as electron acceptors. The cofermentation of several metabolites increases the production of ATP and, subsequently, the growth rate (Zaunmüller et al. 2006). Citrate metabolism was also reported to form proton motive force across the cell membrane in L. mesenteroides (Marty-Teysset et al. 1996) which may contribute to the enhanced growth.
Most Leuconostoc species have genes encoding bd-type cytochrome oxidase, and they do respire in the presence of heme and oxygen (Brooijmans et al. 2009; Johansson et al. 2011; Sijpesteijn 1970). Respiration enables higher biomass production than fermentation (Brooijmans et al. 2009).
Under reducing conditions, leuconostocs may ferment citrate and hexose to diacetyl and acetoin which are important flavor compounds in dairy products. The amount of diacetyl produced is strain dependent (Walker and Gilliland 1987). In a study by Schmitt et al. (1997), Leuconostoc mesenteroides subsp. mesenteroides produced diacetyl as a result of cofermentation of xylose and citrate but not from glucose and citrate. Xylose reduced the activity of lactate dehydrogenase in comparison to glucose, meaning that less pyruvate was converted to lactate in the presence of xylose. Instead, pyruvate was converted to diacetyl/acetoin. In comparison to glucose, xylose may reduce lactate dehydrogenase activity because generation of pyruvate from xylose generates less NAD(P)H, meaning that less reducing power is available for the formation of lactate from pyruvate, a reaction catalyzed by lactate dehydrogenase. Instead of diacetyl/acetoin, surplus pyruvate formed from citrate could be also converted to acetic acid with a coupled generation of ATP, but this pathway seems not to be beneficial under acidic conditions (Schmitt et al. 1997).
Fermentation of pentoses via phosphogluconate/phosphoketolase pathway generates less NAD(P)H than fermentation of hexoses. Thus, acetyl-CoA produced from pentoses can be converted to acetate without a need of an external electron acceptor for the regeneration of NAD+. Despite the supposed benefits of pentose fermentation, many Leuconostoc species seem to be unable to ferment the common pentoses L-arabinose, ribose, or d-xylose, when provided as the sole carbon source (Table 18.1). The reason for this is not known. Some leuconostocs are able to co-metabolize pentoses together with other carbon sources, e.g., xylose together with citrate (Schmitt et al. 1997).
Fructose is fermented by all Leuconostoc spp., except by some strains of L. mesenteroides subsp. cremoris. If fructose is used as an electron acceptor, mannitol is formed. The regeneration of NAD(P)H by fructose enables the production of acetate instead of ethanol which results in gain of ATP and enhanced growth. Interestingly, this process has been investigated as a means to produce d-mannitol from fructose by leuconostocs at industrial scale (Kiviharju and Nyyssölä 2008; von Weymarn et al. 2003).
Citrate and malate are the organic acids most frequently fermented by Leuconostoc spp. Acetate and tartrate are not utilized. Malate is converted into l(+)-lactate and CO2 by L. mesenteroides subsp. mesenteroides. Leuconostocs do not metabolize sugar alcohols other than mannitol. Glycogen and starch are generally not degraded with the exception of L. miyukkimchii that is able to metabolize starch (Lee et al. 2012b).
Many leuconostocs are able to form dextran from sucrose, and this property has been used as one criterion differentiating the species. However, dextran production among L. gelidum and L. carnosum is strains dependent. The ability to form dextran is often lost when serial transfers are made in media of increasing salt concentrations (Pederson and Albury 1955). Dextran production from sucrose is dependent on the growth medium (Pederson and Albury 1955).
Little is known about the production of biogenic amines by leuconostocs. No tyramine formation was detected in strains of Leuconostoc isolated from fresh- and vacuum-packaged meat (Edwards et al. 1987). Some strains of L. mesenteroides subsp. mesenteroides, subsp. cremoris, and Leuconostoc paramesenteroides are known to produce tyramine and tryptamine (Bover-Cid and Holzapfel 1999; de Llano et al. 1998; Moreno-Arribas et al. 2003).
The major fatty acids recorded for Leuconostoc spp. are myristic (C14:0), palmitic (C16:0), palmitoleic [C16:1(9)], oleic [C18:1(9)], and dihydrosterculic acid [C19-cyc(9)] (Schmitt et al. 1989; Shaw and Harding 1989; Tracey and Britz 1989). Leuconostoc spp. differ from Oenococcus spp. and Fructobacillus spp. in containing oleic acid, and not vaccenic [C18-1(11)] acid, as the dominant C18:1 fatty acid (Tracey and Britz 1989). L. carnosum and L. gelidum are clearly differentiated based on their fatty acid profiles (Shaw and Harding 1989).
The interpeptide bridge of the peptidoglycan in leuconostocs consists either Lys-Ser-Ala2 or Lys-Ala2.
Weissella VP Collins et al. (1993, 595); emend. Padonou et al. (2010)
The genus Weissella harbors two different morphological types: the short rods and the ovoid-shaped cocci. Some strains, e.g., in W. minor, are pleomorphic. Weissella colonies are 1–2 mm in diameter, white to creamish white, smooth, circular, and convex after 3–4 days of anaerobic growth. Weissellas are nonmotile with the exception of W. beninensis, the only motile species belonging to Leuconostocaceae. W. beninensis has peritrichous flagella (Padonou et al. 2010).
Weissellas are heterofermentative lactic acid bacteria and share most of the metabolic properties with leuconostocs. Unlike leuconostocs, some Weissella species produce DL lactic acid from glucose (Table 18.2). Most weissellas are able to hydrolyze arginine. Growth occurs at 15 °C, with some species growing at 42–45 °C. All species are able to grow at 37 °C and most species are able to grow at pH 4.8.
Phenotypic tests have been traditionally used to identify Weissella species. Cell morphology has some diagnostic value. Hydrolysis of arginine is a simple biochemical test for differentiation. A battery of ten sugars was recommended by Collins et al. (1993) to be used in combination with other phenotypic tests for identification. Among some weissellas, and particularly W. confusa, dextran production appears to be a common and a widespread feature.
Similar to leuconostocs, some weissellas have genes encoding bd-type cytochrome oxidase required for heme-dependent respiration (Kim et al. 2011c), but functional respiration chain is yet to be reported for weissellas.
Literature describing the production of biogenic amines by Weissella spp. is scarce. Weissella halotolerans W22 combines an arginine deaminase pathway and an ornithine decarboxylation pathway, which results in generation of biogenic amine putrescine and proton motive force (Pereira et al. 2009).
The cell wall peptidoglycan in weissellas is based on lysine as dipeptide, and, with the exception of W. kandleri, all contain alanine or alanine and serine in the interpeptide bridge. In addition, the interpeptide bridge of W. kandleri (Lys-l-Ala-Gly-l-Ala2) contains glycine (Holzapfel and Van Wyk 1982).
Fatty acid profiles can be used to differentiate weissellas. Applying a rapid gas chromatographic method, Samelis et al. (1998) could differentiate between W. viridescens, W. paramesenteroides, W. hellenica, and some typical arginine-negative Weissella isolates from meats on the basis of their cellular fatty acid composition. W. viridescens synthesized eicosenoic (C20:1) acid, while the other two species did not. Unlike W. paramesenteroides, W. hellenica and W. viridescens contained zero to low amounts of cyclopropane fatty acids with 19 carbon atoms, i.e., dihydrosterculic [C19cycl(9)], or lactobacillic acid [C19cycl(11)].
Oenococcus VP Dicks et al. (1995) emend. Endo and Okada (2006)
Oenococcus species are Gram positive and nonmotile, ellipsoidal to spherical in shape. Growth in broth is slow and usually uniform. Colonies usually develop only after 5 d and are less than 1 mm in diameter.
The optimal growth temperature is between 20 °C and 30 °C. Oenococci prefer anaerobic conditions for growth. They produce d-(−)-lactate, CO2, and ethanol or acetate from glucose (Table 18.5) via a pathway not yet fully elucidated. In most species, both NAD and NADP may serve as coenzymes of the glucose-6-phosphate dehydrogenase, but in O. oeni, only NADP is required (Garvie 1975). Fermentation profiles of the different O. oeni strains vary greatly despite the genetically homogeneous nature of this species.
O. oeni is an important organism for malolactic fermentation (MLF) in wine and has several specific characteristics to inhabit in wine, e.g., acidophile and the ability to grow in medium containing 10 % of ethanol. These characteristics differentiate O. oeni from other Leuconostocaceae, including O. kitaharae. O. kitaharae is not acidophilic, cannot tolerate 10 % ethanol, and does not perform MLF (Endo and Okada 2006).
The citrate metabolism in O. oeni is conducted only when fermentable carbohydrates (e.g., glucose) are available. The cofermentation of citrate and glucose in O. oeni is physiologically important for the organism, as co-metabolism of citrate–glucose enhances the ATP synthesis and, consequently, increases the growth rate and biomass yield (Ramos and Santos 1996; Liu 2002).
O. kitaharae does not perform MLF. A stop codon has been found in the gene encoding malolactic enzyme in O. kitaharae (Borneman et al. 2012a; Endo and Okada 2006).
Some O. oeni strains may produce biogenic amines in wine (Bonnin-Jusserand et al. 2011; Izquierdo Cañas et al. 2009; Lucas et al. 2008). Gardini et al. (2005) reported tyramine formation by a strain of O. oeni isolated from Italian red wine. The formation of putrescine from arginine by some strains could be demonstrated (Guerini et al. 2002). However, e.g., Moreno-Arribas et al. (2003) could not detect any potential among O. oeni strains to form biogenic amines. Production of histamine by O. oeni has been extensively analyzed with contradictory results (Garcia-Moruno and Muñoz 2012).
Eighteen fatty acids are associated with O. oeni (Tracey and Britz 1987, 1989). The numerical analysis of the fatty acids showed four clusters defined at . = 0.920, with five strains unassigned. On the basis of the amounts of oleic acid [C18-1(9)] and C19-cyclopropane fatty acids, the strains of O. oeni could also be distinguished from each other. For the majority of O. oeni strains, the result obtained with the cellular fatty acid analysis confirmed the phenotypic relationships.
Fructobacillus VP Endo and Okada (2008)
Fructobacilli are Gram-positive and nonmotile rods. They produce lactate, acetate, CO2, and trace amounts of ethanol from glucose (Table 18.5). Produced lactate is mainly D-isomer. Fructobacillus species prefer fructose over glucose as a carbon source. Aerobic culturing or the presence of pyruvate enhances their growth on glucose (Endo and Okada 2008). Because of the characteristics, they are classified as fructophilic LAB (Endo et al. 2009, 2011). They are usually osmotolerant and grow with 30 % (w/v) fructose, except F. tropaeoli. Fructobacillus spp. are usually poor sugar fermenters, and some of them metabolize only fructose, glucose, and mannitol. On the agar medium, they do not grow on glucose under anaerobic conditions if external electron acceptors are not supplied.
The cell wall peptidoglycan type of F. ficulneus is A3α. The predominant fatty acids in F. ficulneus and F. fructosus are C16:1(9), C16:0, C18:1(9), and C18:1(11) (Antunes et al. 2002).
Isolation, Enrichment, and Maintenance Procedures
Leuconostoc and Weissella
Leuconostoc and Weissella are isolated using rich media such those routinely used for culturing lactic acid bacteria, including All-Purpose Tween (Evans and Niven 1951), MRS (De Man et al. 1960), and Rogosa SL (Rogosa et al. 1951). A review by Schillinger and Holzapfel (2011) discusses in detail the selective and semi-selective media available and applied for isolation of lactic acid bacteria from different habitat such as meat or dairy products. If psychrotrophic species, such as L. carnosum, L. gasicomitatum, L. gelidum, and L. inhae, are expected to occur in the sample, an incubation temperature of 25 °C is recommended. For cultures on solid medium, an anaerobic atmosphere is recommended, while liquid cultures can be maintained in aerobic conditions.
Overall, neither selective agents nor growth conditions have been identified that allow growth and selective isolation of Leuconostoc or Weissella while inhibiting other lactic acid bacteria. Although selective and differential media for detection and enumeration of Leuconostoc have been proposed, they may give unreliable results in cases of samples with large numbers of Pediococcus and Lactobacillus which share many physiological and metabolic properties with Leuconostoc spp. Inclusion of vancomycin (30 μg/mL) in a growth medium may assist the selective isolation of Leuconostoc and Weissella from mixed bacterial populations. However, as some Pediococcus and Lactobacillus spp. are also resistant to vancomycin, this strategy is not entirely selective, and the identities of the isolates recovered need to be confirmed.
Oenococcus
O. oeni is well known to need a specific growth factor. Tomato juice or grape juice is usually added to the medium to supply the growth factor. The pH of the medium is set at 4.8, as the species has a unique acidophilic characteristic. The species hardly grow under aerobic conditions and prefer anaerobic conditions. Several media have been developed to isolate because of the importance of the species in industry, and acidic tomato broth (ATB) might be one of the most well-used medium for isolation and culture of O. oeni (Garvie 1967b; Garvie and Mabbitt 1967). Björkroth and Holzapfel (2006) have summarized the several media for isolation of O. oeni from wine.
O. kitaharae has growth characteristics different from those of O. oeni. Tomato juice or grape juice does not favor the growth of O. kitaharae, and low pH prevents its growth. The organism needs a medium rich in nutrients and anaerobic conditions for maximum growth (Endo and Okada 2006). It was originally isolated using MRS agar containing inhibitors of aerobic fungi (sodium azide and cycloheximide). The growth was very slow and weak in MRS broth and MRS agar. Additional nutrients, e.g., half-strength brain heart infusion (BHI) broth, and anaerobic conditions are required to enhance the growth rate and biomass yield of this bacterium.
Fructobacillus
As Fructobacillus species possess very unique physiological characteristics, selective enrichment isolation can be conducted (Endo et al. 2009). Fructobacillus species prefer fructose over glucose and grow very slowly on glucose under static conditions. They cannot metabolize glucose under anaerobic conditions. However, the presence of external electron acceptors, e.g., pyruvate or oxygen, enhances the growth of Fructobacillus species. Thus, enrichment culturing on fructose, e.g., FYP broth (Endo et al. 2009), under aerobic conditions favors their growth, as other LAB usually prefer anaerobic conditions. To inhibit the growth of aerobic bacteria and fungi in enrichment broth, sodium azide and cycloheximide are very useful. The enrichment can be streaked onto the FYP agar and incubated under aerobic conditions for further selection. Certain oxygen-tolerant LAB, e.g., Lactobacillus plantarum, L. brevis, and Leuconostoc spp., may grow as well, but they can be easily differentiated from Fructobacillus species based on the poor glucose utilization of Fructobacillus species. Because of their unique characteristics, Fructobacillus species are regarded as fructophilic LAB. Differentiation of Fructobacillus species from Lactobacillus kunkeei, which is also a fructophilic species, requires carbohydrate fermentation patterns or molecular approaches.
Maintenance Procedures
Most cultures on liquid or solid media remain viable for at least two to three weeks at 4–6 °C. Longer maintenance is in glycerol (10–20 % v/v) or dimethyl sulfoxide (10 % v/v) suspension at −20° (for months) or preferably at −70 °C or lower (for several years). Cultures are also well preserved in liquid nitrogen or by lyophilization (freeze-drying).
Ecology
Leuconostocs are associated with plants and decaying plant material. They have been detected in green vegetation and roots (Hemme and Foucaud-Scheunemann 2004; Mundt 1967) and in various fermented vegetable products, such as cucumber, kimchi, cabbage, and olives (Kim and Chun 2005; Mäki 2004). In addition to plant-originated material, leuconostocs are frequent in foods of animal origin, including raw milk and dairy products, meat, poultry, and fish (Kim and Chun 2005; Björkroth and Holzapfel 2006). However, healthy warm-blooded animals, including humans, are rarely reported to carry Leuconostoc in the microbiota of their gut or mucous membranes, whereas leuconostocs have been recovered from the intestines of fish (Williams and Collins 1990).
L. carnosum, L. gasicomitatum, and L. gelidum have often been associated with food spoilage (Schillinger et al. 2006). Some modified atmosphere packaged meat- and vegetable-based foods have been prone to leuconostoc spoilage manifesting as bulging of the packages, off-odors and smells, and color changes. In addition to the publications cited in this paragraph, leuconostocs have been frequently reported to belong to microbiota of various fermented foods (see section Application).
O. oeni usually predominates at the end and after alcoholic fermentation in fermenting wine and plays a key role in the MLF. This is because of high resistance to SO2 and ethanol in the organism as compared to other bacteria. SO2 is added to wine as an antioxidant and to prevent the growth of undesirable microorganisms (Amerine et al. 1980). In the work by Carreté et al. (2002), the presence of 2 mM of SO2 had no impact on MLF by O. oeni, but 5 mM of SO2 caused considerable delay on MLF. Cell growth is not necessary to conduct MLF (Carreté et al. 2002). O. oeni is also a responsible organism for MLF in ciders (Sánchez et al. 2012). The cider isolates were separated from wine isolates based on the results of MANOVA analysis of PFGE (Bridier et al. 2010). This is generally supported by MLST (Bridier et al. 2010), suggesting that O. oeni strains have had habitat-specific evolution. Quite recently, an interesting study which found DNA of O. oeni in cocoa bean fermentation by metagenomic approach was reported (Illeghems et al. 2012).
O. kitaharae was originally isolated from a compost of distilled shochu residue in Japan (Endo and Okada 2006). The species was also isolated from the wastewater of a starch factory in Japan (Dr. Tomohiro Irisawa, personal communication). The preferred habitat of O. kitaharae is still uncertain, but compost, wastewater, sludge, and sewage are possible niches.
The habitats of Weissella species are variable and the sources of isolation suggest environmental (soil, vegetation) origin. W. viridescens, W. halotolerans, and W. hellenica have been associated with meat and meat products. W. viridescens may cause spoilage of cured meat due to green discoloration (Niven and Evans 1957), and it also is a prevailing spoilage LAB in Spanish blood sausage called Morcilla de Burgos (Koort et al. 2006; Diez et al. 2009; Santos et al. 2005). W. viridescens is considered somewhat heat resistant (Niven et al. 1954) which is not a common property for a LAB.
W. cibaria, W. confusa, W. koreensis, and W. oryzae have been detected in fermented foods of vegetable origin (Björkroth et al. 2002; Lee et al. 2002), whereas W. confusa has been associated with Greek salami (Samelis et al. 1994), Mexican pozol (Ampe et al. 1999), and Malaysian chili bo (Leisner et al. 1999). Weissella cibaria and W. confusa have also been associated with various types of sour doughs (Galle et al. 2010; Katina et al. 2009; Scheirlinck et al. 2007; De Vuyst et al. 2002). W. soli (Magnusson et al. 2002) is the only species known to originate in soil, but W. paramesenteroides has also been detected in soil (Chen et al. 2005). In addition, weissellas have been isolated from sediments of a coastal marsh (Zamudio-Maya et al. 2008) and lake water (Yanagida et al. 2007).
W. ghanensis, W. fabaria, and W. fabalis were detected in traditional heap fermentations of Ghanaian cocoa bean (De Bruyne et al. 2008, 2010; Snauwaert et al. 2013). W. beninensis (Padonou et al. 2010) originates from submerged fermenting cassava. Weissellas in food fermentations are further discussed in section “Application” of this chapter.
W. ceti was isolated from beaked whales (Mesoplodon bidens); nine isolates were obtained from different organs of four animals (Vela et al. 2011).
Fructobacillus species can be found in several fructose-rich niches, e.g., fresh flowers and fruits. F. fructosus and F. tropaeoli were originally isolated from fresh flowers (Kodama 1956; Endo et al. 2011), and F. ficulneus and F. pseudoficulneus were originally found in ripe figs (Antunes et al. 2002; Chambel et al. 2006). Endo et al. (2009) also isolated a F. fructosus strain from a flower and F. pseudoficulneus strains from a banana peel and a fig. Moreover, Fructobacillus species have been found in several fermented foods produced from fruits. F. durionis was originally isolated from tempoyak, a Malaysian acid-fermented condiment made from the pulp of the durian fruit (Leisner et al. 2005). Several Fructobacillus species have been found in cocoa bean fermentation (Nielsen et al. 2007; Papalexandratou et al. 2011a, b) and wine (Mesas et al. 2011). Moreover, F. fructosus has been found from guts of several fructose-related insects, i.e., bumblebees, fruit flies, and giant ants (He et al. 2011; Koch and Schmid-Hempel 2011; Thaochan et al. 2010). This is highly interesting as Fructobacillus species do not grow on glucose under anaerobic conditions. They can grow well on fructose under anaerobic conditions.
Pathogenicity and Clinical Significance
Some Leuconostoc species have caused infections, but most of the patients had received vancomycin, had an underlying disease, or were premature babies. These bacteria are not a risk for healthy individuals, and leuconostocs are considered as GRAS organisms (Schillinger et al. 2006). All leuconostocs are intrinsically resistant to vancomycin and other glycopeptide antibiotics; the first clinical reports were published in 1984–1985 (Buu-Hoi et al. 1985; Huygens 1993; Orberg and Sandine 1984: Elisha and Courvalin 1995).
W. confusa has been detected in the normal human intestinal microbiota (Stiles and Holzapfel 1997; Walter et al. 2001; Tannock et al. 1999). W. cibaria and W. confusa have been detected in clinical samples of humans and animals (Björkroth et al. 2002). W. confusa has been associated with bacteremia (Olano et al. 2001; Harlan et al. 2011; Salimnia et al. 2011; Lee et al. 2011a) and endocarditis (Flaherty et al. 2003) in humans. As in the case of Leuconostoc infection, the infection is mainly due to the natural resistance of these species to vancomycin and an underlying disease or immunosuppression of the host. In addition to human cases, W. confusa has been documented as a cause for a systemic infection in a non-immunocompromised primate (Cercopitheus mona) (Vela et al. 2003), and unknown Weissella strains were isolated from a diseased rainbow trout in China (Liu et al. 2009).
Oenococcus and Fructobacillus species have not been associated with disease in humans or animals.
Application
Meat
As commercial starter organisms for meat fermentations, leuconostocs are not as important as some Lactobacillus and Pediococcus spp. (Holzapfel 1998). However, leuconostocs and weissellas are repeatedly found in fermented meat products (Albano et al. 2009; Aymerich et al. 2006; Babic et al. 2011; Ben Belgacem et al. 2009; Benito et al. 2007; Danilovic et al. 2011; Kesmen et al. 2012; Papamanoli et al. 2003; Parente et al. 2001; Samelis et al. 1994; Tu et al. 2010), although at lower levels than lactobacilli. L. mesenteroides and W. viridescens are the species most often encountered in fermented meats, but L. carnosum, L. gelidum, L. pseudomesenteroides, W. confusa, and W. paramesenteroides are also reported. Weissellas and leuconostocs are associated with the production of bacteriocins (Hastings et al. 1994) which could be of importance in the fermentation process and may contribute to the microbiological safety of the final product.
Dairy
In contrast to the lactococci, leuconostocs are not competitive growers or important producers of lactic acid in milk. The ability of certain strains to produce the flavor compound diacetyl, however, has led to their frequent incorporation into mixed strain starter cultures in products like buttermilk, butter, and quarg (cream cheese). Leuconostocs form functional associations with lactococci that ferment lactose efficiently to lactate. The subsequent acidification creates favorable conditions for the production of diacetyl from citrate by citrate-lyase-positive Leuconostoc strains (Vedamuthu 1994). Strain 91404 of L. mesenteroides subsp. cremoris was selected by Levata-Jovanovic and Sandine (1997) as an aroma producer in the preparation of experimental cultured buttermilk on the basis of its low diacetyl reductase activity, citrate utilization, and high diacetyl production under acidic conditions, and also because of its growth characteristics and its compatibility with Lactococcus strains. Fortification of ripened buttermilk with sodium citrate resulted in a significant increase of diacetyl and acetoin production during buttermilk storage at 5 °C for 2 weeks. Surplus of citrate, low pH of 4.5–4.7, a sufficient number of active, non-growing aroma producers, air incorporation during curd breaking, and low storage temperatures stimulated citrate metabolism and enhanced flavor during the 2 weeks of storage. Optimal development of L. mesenteroides subsp. cremoris appears to be dependent on the manganese content of the milk, and with values <15 μg/L, it may be outcompeted in a mixed strain starter culture. The ratio of L. mesenteroides subsp. cremoris to Lactococcus lactis in mixed culture is also dependent on the incubation temperature: warmer than 25 °C favors L. lactis (Hemme and Foucaud-Scheunemann 2004).
L. mesenteroides subsp. cremoris plays an important role in the desired CO2 formation in the cheeses such as Gouda and Edam where it comprises ca. 5 % of a typical starter culture, as compared to 2–3 % for Tilsiter (Zickrick 1996). Cogan et al. (1997) studied 4,379 isolates from 35 artisanal dairy products, including 24 artisanal cheeses, and identified 10 % of the LAB strains as Leuconostoc spp. The reported proportions of Leuconostoc spp. in LAB communities found in artisanal cheeses typically vary between 1 % and 10 % (Campos et al. 2011; Fontana et al. 2010; Menendez et al. 2001; Samelis et al. 2010). Nieto-Arribas et al. (2010) characterized technical properties of 27 Leuconostoc isolates from Manchego cheese in order to test their potential as dairy starter cultures. Majority of the isolates belonged to L. mesenteroides, although W. paramesenteroides and Leuconostoc lactis were also found. All isolates grew at high concentrations of NaCl (4.0–4.5 %). They had poor acidifying capacity, no lipolytic activity, and poor capacity to produce diacetyl from citrate. Several isolates showed proteolytic activity. Most of the isolates were considered unsuitable as starter cultures because they grew poorly at pH 4.3.
Weissellas are rarely isolated from cheeses. W. thailandensis was a minor part of the halotolerant lactic acid bacteria community in two types of Mexican cheeses that contained 5–6 % of NaCl (Morales et al. 2011). W. paramesenteroides was found to be the dominant species of LAB in “dadih,” a traditional fermented milk in Indonesia (Hosono et al. 1989). Zakaria et al. (1998) reported W. paramesenteroides as one of three predominating LAB species in dadih with different strains of W. paramesenteroides having different influences on its viscosity and curd syneresis.
Kefir is milk drink fermented with kefir grains that consist of bacteria and yeasts. L. mesenteroides has been reported to be part of the predominating microbiota in kefir strains together with lactobacilli and yeasts (Hsieh et al. 2012; Kowalczyk et al. 2011; Lin et al. 1999). The use of L. mesenteroides in formulated starter cultures for kefir production has also been reported (Duitschaever et al. 1987; Marshall and Cole 1985).
It is known that leuconostocs play a minor role in most traditional milk fermentations. Beukes et al. (2001) collected 15 samples of conventionally fermented milk from households in South Africa and Namibia and found that genera Leuconostoc, Lactococcus, and Lactobacillus predominated the microbial communities. Of the leuconostoc isolates, 83 % were identified as L. mesenteroides subsp. dextranicum. L. citreum was a minor group. In traditional Chinese yak milk products investigated by Bao et al. (2012), L. mesenteroides subsp. mesenteroides predominated. Yu et al. (2011) identified LAB isolated from several traditional fermented dairy products in Mongolia. Of the 668 isolates, 43 (6.4 %) were identified as Leuconostoc lactis or L. mesenteroides.
Foods and Beverages of Plant Origin
L. mesenteroides subsp. mesenteroides plays an important role in the fermentation of vegetables such as sauerkraut and cucumbers. Although not the dominant species on cabbage at the time of shredding, L. mesenteroides subsp. mesenteroides initiates the fermentation of sauerkraut and is then succeeded by the more acid-tolerant lactobacilli (Pederson 1930; Stamer 1975). The same microbial succession was observed during fermentation of cucumbers or other pickles as well as olives (Vaughn 1985). Kimchi, a traditional Korean food, is produced by the lactic fermentation of vegetables such as Chinese cabbage, radishes, and cucumbers. Like in sauerkraut fermentation, Leuconostocs such as L. citreum, L. gelidum, L. kimchii, and L. mesenteroides dominate the early stages of fermentation, followed by lactobacilli (Choi et al. 2003; Kim et al. 2000a, b; Lee et al. 1997), while some Weissella-like strains were reported for the midstage of fermentation (Choi et al. 2003).
The sequence of LAB in vegetable fermentations is mainly dependent upon the initial load, growth rates, and salt and acid tolerances (Daeschel et al. 1987). Leuconostocs are apparently better adapted to plant materials and initiate growth more rapidly than most of the other LAB. Some leuconostocs, e.g., L. mesenteroides subsp. mesenteroides, L. citreum, L. gelidum, and L. kimchii, may be favored by their ability to utilize a wide selection of plant carbohydrates, such as l-arabinose, d-xylose, and sucrose (Table 18.1). Furthermore, vegetables contain citrate and fructose, which can be utilized by leuconostocs as electron acceptors for faster growth (Zaunmüller et al. 2006). Carbon dioxide produced by leuconostocs replaces the air and creates an anaerobic atmosphere that inhibits aerobic bacteria (Steinkraus 1983).
The concentration of NaCl added to vegetables in the fermentation process affects the composition of bacterial community. L. mesenteroides subsp. mesenteroides is less salt tolerant than the other LAB involved in vegetable fermentation (Vaughn 1985). In salt stock pickles, the initial salt concentration is two- to threefold higher than that employed in sauerkraut, and L. mesenteroides subsp. mesenteroides therefore plays a less-active role in pickle fermentations (Stamer 1988).
Another important factor determining the composition of the bacterial community is the fermentation temperature. Kimchi is often fermented at chilled temperatures (−1 °C to 10 °C) which favors psychrotrophic bacteria (Eom et al. 2007), like L. gasicomitatum and L. gelidum. W. koreensis was identified as the species best adapted at kimchi fermentation at −1 °C (Cho et al. 2006).
Although most of the vegetable fermentations are “spontaneous,” the inclusion of Leuconostoc strains into starter cultures appears beneficial for the fermentation process and for the development of desirable sensory traits. Using a vegetable juice medium (VJM), Gardner et al. (2001) selected LAB strains for mixed starter cultures to be used in lactic acid fermentation of carrot, beet, and cabbage. Compared to spontaneous fermentation, the inoculation of the vegetables with selected mixed starter cultures accelerated acidification and produced a more stable product. Starter cultures consisting of psychrotrophic L. mesenteroides have been successfully applied to accelerate the fermentation of kimchi at +4 °C (Jung et al. 2012d). According to Eom et al. (2007), L. mesenteroides and L. citreum starter cultures can be used to enhance the production of prebiotic oligosaccharides in kimchi-like foods fermented at low temperatures.
L. mesenteroides and L. citreum may be part of predominating LAB community in artisanal wheat sourdough (Corsetti et al. 2001; Robert et al. 2009) and distinctively influences the bread taste (Lönner and Prove-Akesson, 1989). W. cibaria and W. confusa are also found, although at lesser proportions (Minervini et al. 2012; Robert et al. 2009). Several leuconostocs and weissellas have been introduced to wheat sourdough for the production of exopolysaccharides from sucrose. This is considered as a means to improve the shelf life, volume, and nutritional value of bread without additives. W. cibaria and W. confusa strains are potential starter cultures for wheat and sorghum sourdoughs due to their high capacity for the production and exopolysaccharides without strong acidification (Galle et al. 2010; Katina et al. 2009).
L. mesenteroides subsp. mesenteroides is also predominant and responsible for initiating the fermentation of many traditional lactic acid-fermented foods in the tropics. High numbers of L. mesenteroides subsp. mesenteroides were isolated from starchy products like cassava (Okafor 1977) or kocho, an African acidic fermented product from false banana (Ensete ventricosum; Gashe 1987). Strains of L. mesenteroides subsp. mesenteroides have been found to produce a highly active linamarase, which hydrolyzes the cyanogenic glucoside linamarin present in cassava (Okafor and Ejiofor 1985). Gueguen et al. (1997) purified and characterized an intracellular β-glucosidase from a strain of L. mesenteroides isolated from cassava. When grown on an arbutin-containing medium, it was found to produce an intracellular β-glucosidase. Its cyanogenic activity was suggested to be of potential interest in cassava detoxification, by hydrolyzing the cyanogenic glucosides present in cassava pulp. W. confusa was identified as one of the LAB predominating in highly complex microbial communities in Lafun, an African traditional cassava food (Padonou et al. 2009).
Hancioglu and Karapinar (1997) studied the microflora of Boza, a traditional fermented Turkish beverage, prepared by yeast and lactic acid fermentation of cooked maize, wheat, and rice flours. Among the 77 LAB strains isolated during the fermentation, W. paramesenteroides (25.6 %), L. mesenteroides subsp. mesenteroides (18.6 %), W. confusa (7.8 %), L. mesenteroides subsp. dextranicum (7.3 %), and O. oeni (3.7 %) were found. L. mesenteroides and Fructobacillus durionis were part of a complex microbial community in palm wine made of Borassus akeassii (Ouoba et al. 2012). Palm wine was fermented at 21–30 °C and had pH of 3.5–4.1 and ethanol content of 0.3–2.7 %. L. palmae was originally isolated from palm wine by Ehrmann et al. (2009).
L. mesenteroides subsp. mesenteroides is also involved in the fermentation of seeds of the African oil bean tree (Antai and Ibrahim 1986) and of cocoa (Ostovar and Keeney 1973; Passos et al. 1984). Lefeber et al. (2011) tested metabolic activities of various cocoa-specific Lactobacillus, Leuconostoc, Weissella, and Fructobacillus strains in cocoa pulp simulation medium and concluded that citric acid converting, mannitol-producing, heterofermentative, and/or fructose-loving LAB strains are particularly adapted to cocoa pulp matrix. Of the investigated strains, those belonging to Lactobacillus fermentum were considered to be the most suitable for the process. Illeghems et al (2012) considered Leuconostoc mesenteroides to be only an opportunistic member of the fermentation process wherein a succession of microbial activities of yeasts, LAB, and acetic acid bacteria takes place. Several Fructobacillus species have been commonly seen in spontaneous cocoa bean fermentation carried out in different countries (Ecuador, Brazil and Ghana) (Camu et al. 2007; Papalexandratou et al. 2011a, b), suggesting that they play certain key roles for the fermentation. Possible roles might be fructose fermentation and oxygen consumption (Papalexandratou et al. 2011a, b).
L. mesenteroides subsp. mesenteroides is also involved in the submerged fermentation of coffee berries, practiced in some highland regions, and by which the oligosaccharide concentration decreases and monosaccharides increase, with a concomitant improvement in coffee quality (Frank and Dela Cruz 1964; Jones and Jones 1984; Müller 1996). Avallone et al. (2001) found that LAB, predominated by L. mesenteroides, and yeasts were the microbes mainly responsible for the coffee fermentation. Leuconostoc holzapfelii was originally isolated from Ethiopian coffee fermentation (De Bruyne et al. 2007).
Some leuconostocs, lactobacilli, and pediococci are associated with the early stages of fermenting grape must (juice). Oenococcus oeni, however, has been reported as the most important and desirable species among the LAB involved in winemaking thanks to its key role in the secondary fermentation of wine, also referred to as the “malolactic fermentation” (MLF). By their high resistance to SO2 and ethanol, O. oeni may be present in relatively high numbers at the end of the alcoholic fermentation. At this stage, they play the major role in the production of microbiologically stable wines by converting l-malic acid to l(+)-lactic acid and CO2, decreasing wine acidity by 0.1–0.3 units (Davis et al. 1985; Wibowo et al. 1985). This deacidification is particularly desirable for high-acid wine produced in cool-climate regions (Liu 2002). Lactobacillus spp. and Pediococcus spp. found in wine can also conduct MLF, but, however, these organisms sometimes cause spoilage problems by production of several undesirable volatile compounds (Bartowsky 2009). Some strains of O. oeni are also unsuitable for the MLF. Edwards et al. (1998) identified two O. oeni strains that were associated with sluggish and/or stuck fermentations and that were found to slow down some alcoholic fermentations. Better control over the MLF can be achieved by inoculating wines with a selected O. oeni strain (Nielsen et al. 1996; Rodríguez-Nogales et al. 2012) commercially available in the major wine-growing areas of industrialized countries.
Besides the MLF, citrate metabolism by O. oeni is also regarded as important for quality of wine because of the large quantity of citrate in grape juice. Citrate is generally transformed to lactate, acetate, diacetyl, acetoin, and 2,3-butanediol. These chemicals have an impact on quality of wine both positively and negatively (Bartowsky and Borneman 2011).
In addition to wine, MLF by O. oeni is important in fermentation of apple cider. Herrero et al. (2001) used O. oeni immobilized in alginate beads for controlled malolactic fermentation of cider. The rates of malic acid consumption were similar to conventional fermentation, but a lower acetic acid content and higher concentration of alcohols were detected with immobilized cells. These features were considered to have beneficial effects on the sensory properties of cider (Herrero et al. 2001). Nedovic et al. (2000) succeeded in improving cider quality and to accelerate the process by continuous fermentation with coimmobilized yeast and O. oeni cells.
Dextran Production
Dextran is a glucose polymer that has many applications in medicine, separation technology, and biotechnology. The ability of L. mesenteroides subsp. mesenteroides to produce dextrans from sucrose has been exploited for the production of commercially valuable dextran on an industrial scale. In addition to dextran, leuconostocs are able to produce different types of glucose polymers (glucans) such as alternans and levans from sucrose (Cote and Ahlgren 1995). Glucans are synthesized from sucrose by large extracellular glucosyltransferase enzymes, commonly named glucansucrases. Glucosidic bond synthesis occurs without the mediation of nucleotide-activated sugars and cofactors are not necessary (Monchois et al. 1999). Glucansucrases differ in their ability to synthesize glucans with different types of glucosidic linkages (Kralj et al. 2004).
Dextransucrase is economically the most important glucansucrase. It is mainly produced by L. mesenteroides subsp. mesenteroides. To develop strategies for improved dextransucrase production, Dols et al. (1997) studied dextran production in relation to the growth and energetics of L. mesenteroides NRRL B-1299 during metabolism of various sugars. For sucrose-grown cultures, they found that a large fraction of sucrose is converted outside the cell by dextransucrase into dextran and fructose without supporting growth. The fraction entering the cell is phosphorylated by an inducible sucrose phosphorylase and converted to glucose-6-phosphate (G-6-P) by a constitutive phosphoglucomutase and to heterofermentative metabolites (lactate, acetate, and ethanol). Sucrose was found to support a higher growth rate than the monosaccharides.
In the presence of efficient monomer acceptors, like maltose or isomaltose, dextransucrase catalyzes the synthesis of low molecular weight oligosaccharides instead of high molecular weight dextran (Monchois et al. 1999). Some gluco-oligosaccharides have prebiotic properties, meaning that their industrial production is of interest. The structure and chain length of oligosaccharides can be tailored by changing the concentrations of sucrose and acceptor carbohydrate in the medium (Lee et al. 2008).
Maina et al. (2008) studied the production of gluco-oligosaccharides and linear dextran by W. confusa E392 and L. citreum E497. The gluco-oligosaccharides were characterized by α-(1→2) linked branches that are associated with probiotic properties. In addition, W. confusa E392 was found to be a good alternative to widely used L. mesenteroides B-512F in the production of linear dextran. Interestingly, dextransucrases of Weissella form a distinct phylogenetic group within glucansucrases of other lactic acid bacteria (Amari et al. 2012a).
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Nieminen, T.T., Säde, E., Endo, A., Johansson, P., Björkroth, J. (2014). The Family Leuconostocaceae . In: Rosenberg, E., DeLong, E.F., Lory, S., Stackebrandt, E., Thompson, F. (eds) The Prokaryotes. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-30120-9_208
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