Molecular Phylogeny of Yeasts from Palm Wine and Enological Potentials of the Drink

Annual Research & Review in Biology

20(3): 1-12, 2017; Article no.ARRB.37748 ISSN: 2347-565X, NLM ID: 101632869

Ogueri Nwaiwu 1* and Martin Itumoh 2

1Alpha Altis, Ingenuity Center, University of Nottingham Innovation Park, Triumph Road, Nottingham, NG7 2TU, United Kingdom. 2Department of Agribusiness and Management, Faculty of Agriculture, Federal University Ndufu Alike Ikwo, Ebonyi State, Nigeria.

Authors’ contributions

This work was carried out in collaboration between both authors. Author ON designed the study, performed the statistical analysis and wrote the first draft of the manuscript. Author MI managed the literature searches. Both authors read and approved the final manuscript.

Article Information

DOI: 10.9734/ARRB/2017/37748 Editor(s): (1) George Perry, Dean and Professor of Biology, University of Texas at San Antonio, USA. Reviewers: (1) Moutawakilou Gomina, University of Parakou, Benin. (2) Hatice Kalkan Yildirim, Ege University, Turkey. (3) Angelo Maria Giuffrè, Università degli Studi Mediterranea di Reggio Calabria, Italy. Complete Peer review History: http://www.sciencedomain.org/review-history/22091

Received 27 th October 2017 th Mini-review Article Accepted 25 November 2017 Published 29 th November 2017

ABSTRACT

Palm wine is consumed around the world and known by various names. Unlike many good quality traditional fermented food and drink in developing countries that have only been marketed in their local communities, palm wine has proved to be a commercial success in that it is now canned or bottled and marketed internationally. Despite these advances, the drink has not been subjected to current technology applied to wines from grapes to improve quality. This review highlights the evolutionary relationships between yeasts isolated from the drink in two continents and the enological potential of the drink. The evolutionary history was inferred by using the Molecular Evolutionary Genetics Analysis (version 7) computer software to construct phylogenetic trees using 34 previously reported curated nucleotide sequences from the D1/D2 domain of 26S rRNA in yeasts isolated from the drink. We found that similar yeast species formed terminal taxa from a common node. However Pichia kudriavzevii species formed two distinct clades which suggest intra-species diversity. One Saccharomyces cerevisiae (accession No. HG425326) had a node distinct from other

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*Corresponding author: E-mail: [email protected];

Nwaiwu and Itumoh; ARRB, 20(3): 1-12, 2017; Article no.ARRB.37748

S. cerevisiae species indicating that the strain may belong to a different lineage. From literature, the enological compounds measured in different types of wines like ethyl acetate, oleic acid, ethanol, and acetic acid are present in palm wine. These primary and secondary metabolites of palm wine from different yeasts confirm the enological potentials of the drink even though higher alcohols and esters appear to be more in some wines when compared to palm wine. Future research may involve more holistic investigations that will elucidate the biochemical pathway of palm wine fermentation products.

Keywords: Phylogeny; evolution; enology; metabolites; palm wine; yeasts.

1. INTRODUCTION earlier study in Nigeria it was suggested that S. cerevisiae population is autochthonous [11]. Palm wine is a drink consumed in many parts of However, another study [12] showed that some the world and it is known as a global fermented S. cerevisiae strains of Nigerian palm wine are beverage [1]. It is obtained from palm saps of similar to well characterized reference strains different palm trees and consumption is common (NCTC 1406 and strain S288c) used around the in South America, Africa and Asia. What was world. In Burkina Faso investigators found that B. originally a drink for the poor is now canned, akeassii palm wine contains a specific yeast bottled and marketed internationally. The drink is population of diploid strains different from other consumed by millions of people in West Africa palm wine strains from Ivory Coast, Nigeria and even though the nutritional aspects of the drink is Djibouti Republic [13]. still largely unknown [2]. Apart from direct consumption, palm wine can be distilled to The palm wine production process has been produce a local gin with ethanol content that can explained in a previous report [12] and varies range from 20% [3] to 61.5% v/v [4]. At the from one continent to another. A study by Legras start of palm wine fermentation, common et al. [14] investigated how the yeast species S. bacteria found in the drink includes lactobacillus cerevisiae evolved. The scientists in that study whereas acetic acid bacteria (AAB) are found analyzed the genetic diversity among 651 strains at the end [5]. The yeast Saccharomyces from 56 different geographical origins worldwide cerevisiae ferments sugar in the middle of palm and their genotyping at 12 microsatellite loci wine fermentation to yield metabolites like revealed genotypes that were organized in ethanol. subgroups in popular products consumed around the world namely bread, beer, wine and sake. It In the last 10 years, the use of molecular was found that some of these groups displayed a techniques (26S rDNA sequencing) for combination of alleles that were intermediate identification has revealed the actual yeast between these subgroups and strains genetic species inherent in palm wine and the general diversity was linked with geographical differences consensus is that Saccharomyces yeasts which suggested local domestications. especially S. cerevisiae is the dominant yeast among other naturally occurring microbial flora of There has been increase in the last 5 years on the drink. However, it is now believed that non- identification of microorganisms that ferment Saccharomyces yeasts may have an impact on palm wine, but not much has been done to volatile composition and sensory profile of identify all the secondary metabolites of bacteria fermented beverages [6,7]. New palm wine yeast and yeasts that make up the flavor and aroma of species like Hanseniaspora jakobsenii [8] and the drink. In particular, there are scarcely any Clavispora lusitaniae [9] have been identified detailed study that has used current from the drink and there could be potential for biotechnology analytical tools to elucidate the more yeast species discoveries since the interactions between bacteria and molecular characterization of microorganisms Saccharomyces or non- Saccharomyces yeasts present in the drink has not been fully explored in flavor or aroma generation. Production of the around the world to explain species diversity. It is drink is still small scale and in order to make not yet clear how the yeasts that ferment palm larger volumes and improve the availability of the wine evolved. From literature, it is evident that drink, there is a need to adopt studies and palm wine yeast content varies among the methods that have been used to gain more various regions of the world. A study in Mexico understanding of the fermentation chemistry of [10] failed to produce S. cerevisiae as the different well known wines and spirits made from dominant yeast in a palm wine sample and in an fermentation of other food products especially

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grapes. This approach may include gene esters. These compounds have been confirmed manipulation and full metabolomics assessment. by other palm wine investigators [12,27,28].

The difference between the end products of Many traditional foods have been reported to be fermentation of wine made from grapes and palm interesting and useful as food and for human wine obtained from palm sap is that the former health but no extensive scientific analysis has undergoes several processes to improve quality been carried out on them possibly because they whereas the latter is taken in the form obtained lack a commercial potential. The case of palm from the field. Both types of wine are believed to wine is different in that the drink is now canned contain beneficial anti-oxidants like phenols. The or bottled and sold internationally. Therefore, level varies during wine production [15]. The more studies are required for a better actual level of benefits obtained from understanding of the nature of metabolites from antioxidants in wine is still debated. It has been yeasts in palm wine and how the organisms reported that red wine consumption increases evolved. Microbial research on foods enabled antioxidant status and decreases oxidative stress technological developments in Japan in the past in the circulation of both young and old humans [29]. Therefore, more studies may lead to [16] while another study pointed out that application of current biotechnology analytical antioxidants like resveratrol in red wines in low methods for further research in flavors of the doses, has no beneficial effect [17]. The drink and may result in sustained production of antioxidant profile of palm wine is not well improved varieties of palm trees and post- studied. However, a study on humans that harvest fermentation of palm wine with different consume the drink regularly revealed that flavors. Also, it has been pointed out that consumption of the drink may deplete the body’s traditional food fermentation for products like antioxidants against free radical attacks and palm wine represents an extremely valuable render the body in a state of oxidative stress [18]. cultural heritage and may harbor undiscovered Generally, epidemiological evidence suggests strains [1]. It was emphasized that holistic that the potential health benefits of approaches for identification are of interest to phytochemical constituents in grapes include food microbiologists. protection against oxidative damage, anti- diabetic, anti-cholesterol, and anti-platelet The phylogeny of palm wine yeasts using functions [19,20]. molecular characteristics has not been well reported in literature. This review summarizes The outline by Walker and Stewart [21] shows the phylogenetic relationships of curated yeasts that after fermentation of sugars by S. cerevisiae isolated from palm wine from two continents and in fermented beverages, further distillation of the highlights the winemaking or enological fermented mix can be performed to produce potentials of the drink. matured spirits like whiskey or non-matured spirits like gin. Currently palm wine is only 2. PALM WINE YEAST PHYLOGENY distilled into non-matured spirits. The maturing of the drink and its distillate by fortification with In order to elucidate the relationships between other microorganisms is yet to be explored palm wine yeasts from West Africa and South commercially. The application of metabolic America, phylogenetic analysis was carried out. engineering of S. cerevisiae to palm wine We used curated yeast sequences covering the production has not been performed. It is worth D1/D2 domain of the 26S rRNA of yeast strains exploring because the organism is known as an obtained from previous reports. This included effective cell factory for metabolite production sequences from reports of palm wine produced [22]. in Burkina Faso [5] and Nigeria [12] both in West Africa and Mexico, South America [10]. First, a Previous studies carried out on palm wine multiple sequence alignment (MSA) was volatiles using GC-MS [23] and proton transfer constructed with the curated sequences reaction-mass spectrometry [24] show that palm mentioned above by using multiple sequence wine is a reservoir of several flavor and aroma comparison by log expectation (MUSCLE) volatiles found in well-known red and white wines described by Edgar [30] after which five [25] and other formulated wines [26]. Common phylogenetic trees were constructed using groups of flavor and aroma volatiles found in Molecular Evolutionary Genetics Analysis palm wine by the aforementioned investigators (MEGA; version 7) tool developed by Kumar et include alcohols, carboxylic acids, phenols and al. [31]. The MSA tool MUSCLE was used

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because it is rated among the top 10 widely used grape juice by yeast [35]. Metabolites produced and has been shown to produce very good during wine fermentation may be primary or alignments [32,33]. secondary. The primary metabolites are involved in growth whereas secondary metabolites are not To determine strains close to wine yeasts, one important to maintain cell life. The profile control sequence (Accession No. JX423566.1) knowledge of metabolites is essential for which was reported [12] to have a 100% identity functional genomics and search for new match with a wine yeast was included. A compounds that may be used as biotechnology sequence found in the bacteria strain products [36]. The production of primary Gluconacetobacter saccharivorans (Accession compounds which includes ethanol, glycerol, No. HE979557) isolated from palm wine [5] was acetic acid and secondary metabolites like fatty also added as an out group. The statistical acids, esters, and higher alcohols contributes methods used for constructing the trees included hugely to the flavor and aroma of wines [37]. The neighbor joining, minimum evolution, maximum chemical components usually found in grape parsimony, unweighted pair group method with wines have been reported to be present in palm arithmetic mean (UPGMA), and maximum wine. In enology, S. cerevisiae is the yeast likelihood. Evolutionary distances were computed mainly used [38] and it is commonly found in using the maximum composite likelihood model palm wine. According to a study with 70 different and test of reliability was carried out by strains, it was found that the organism appeared bootstrapping [34] with 1000 replicates in all to enhance antioxidant and phenolic compounds cases. The neighbor joining and minimum content in red wines used for that study [39]. evolution methods had the same topology after phylogenetic trees construction and all the 5 It has been reported that S. cerevisiae can be trees constructed showed virtually the same manipulated genetically to give a desired product monophyletic groups. For brevity, the UPGMA [40]. However, there is evidence that non- (Fig. 1) is shown. The tree expectedly showed a Saccharomyces yeasts like Pichia sp. found in different root source for the bacteria species grapes [41] and palm wine [42] can produce used as an out-group. other compounds like glycerol rather than alcohol after sugar fermentation [43] and improve the The yeast species containing the S. cerevisiae flavor of wines. Specific non-Saccharomyces positive control sequence (wine yeast) originated yeasts highlight how vital strain selection is, from the same node as other S. cerevisiae because these organisms can secret enzymes species. Overall, similar yeast species formed and also produce secondary metabolites which terminal taxa from a common node. However aid stability and color in wine [44]. The common Pichia kudriavzevii species formed two distinct chemical compound classes [26] that can be clades which suggest intra-species diversity. In found in wines are listed in Table 1. These particular P kudriavzevii (accession No. compounds (Nos 1-6) are also found in palm HG425333) from Nigeria formed a separate wine except C13-Norisoprenoids and terpenes clade with a strain (accession No. KF241564) which are not widely reported in palm wine from Mexico. This needs further investigation to possibly because they are found mainly in ascertain how they differ with other strains of P. grape skin [45]. The occurrence of terpenes in kudriavzevii . One S. cerevisiae (accession No. palm wine in the studies of Uzochukwu et al. HG425326) had a node distinct from other S. [23] and Lasekan [24] may be due to cerevisiae species indicating that the strain may environmental contamination from palm or wild belong to a different lineage. Intra- species fruits. The four most common chemical groups diversity of other palm wine microorganisms has found in palm wine include ethyl acetate, oleic been reported [5,13] and the bootstrap values acid, ethanol, and acetic acid. It appears that suggest that intra-species diversity may be more the number of esters can vary in palm saps in S. cerevisiae species than other yeast genera because a Nigerian [23] palm sap (E, Table 1) like Pichia and Candida . had more esters than the Canadian [26] wine (A, Table 1) and Malaysian [28] palm sap 3. ENOLOGICAL QUALITIES OF PALM (C, Table 1). WINE: COMPOUNDS OF PALM WINE FOUND IN WINES 3.1 Ethyl Acetate

In most cases unless otherwise stated the term In most palm wine studies, ethyl acetate is one of ‘wine’ is applied to product of fermentation of the esters that are dominant. Esters are highly

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valued in wine making because of the sweet intracellular after catalysis by an acyl transferase smelling aroma it brings to wines and beer [46]. [52]. The genes that encode synthesis of acetate Among other wines, ethyl acetate is found in red ester like ethyl acetate are well characterized [47] white [48] and durian wines [49]. It is also a and the biochemical pathways of the compound key aroma compound in apple [50] and bilberry synthesis are well studied [53]. This knowledge syrup wines [51]. Fermentation with brewer’s can be applied to palm wine fermentation to yeast has shown that esters are formed generate higher ester concentrations.

Fig. 1. Evolutionary history of yeast strains with verified sequences covering the D1/D2 domain of the 26S rRNA from previous reports using the UPGMA method. Species with accession numbers beginning with HG obtained from Nigeria [12], HE- from Burkina Faso [5] and KF from Mexico [10] were included. The bootstrap test (1000 replicates) is shown next to the branches. The tree is drawn to scale, and the analysis was carried out with 34 nucleotide sequences

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Table 1. Major chemical compound classes of wine from Canada (A) compared with volatiles from palm wine reported in four different studies (B – E)

Wine volatiles Number of wine compounds A B C D E 1. Esters 13 10 3 10 14 2. Fatty Acids 2 2 NS NS NS 3. Alcohols NS 6 4 2 2 4. Carboxylic Acids NS 2 1 7 4 5. Acyloins NS 1 1 1 1 6. Phenols 2 1 NS** 2 1 7. C13-Norisoprenoids 1 0 0 0 0 8. Terpenes 7 0 0 1 2 9. Other Products* 6 NS 1 23 N/A *Compounds that appeared to be derivatives were grouped into volatiles of Other Products; **NS = not stated; N/A = not applicable A = Canadian wine study [26]; palm reports: B [12], C [28], D [27] and E [23]

3.2 Oleic Acid probably due to the controlled manner production is carried out with established standards. Oleic acid is found in the cytoplasm of S. cerevisiae and is listed as the most widely Polyphenolic antioxidants are believed to be distributed and abundant fatty acid in nature [54]. beneficial to health and are present in wines [60]. It has been reported that ethanol tolerance in S. Phenolic compounds are believed to be cerevisiae is dependent on cellular oleic acid antifungal, antiviral and anti-bacteria [61]. content [55]. Three strains of S. cerevisiae have Phenolic content may depend on the wine origin been analysed during hypoxic growth in a sugar- [62]. The characteristics of phenols from palm rich medium lacking lipid nutrients and it was wine are unknown and needs to be investigated. found that lack of lipids may have a negative effect on yeast viability [56]. This analysis was 3.4 Carboxylic Acids and Acyloins confirmed by Landolfo et al. [57] after it was shown that lipid nutrients facilitate a reduction of Acetic acid bacteria (AAB) can cause spoilage intracellular oxidative damage to membranes and and affect the quality of wine [63]. They originate proteins. Another factor that could affect oleic from infected grapes [64] and the main carboxylic acid abundance is temperature. It has been acid formed is acetic acid [65]. In palm wine demonstrated that temperature can affect the processing, AAB is responsible for the vinegar lipid composition of S. cerevisiae and S. taste due to production of acetic acid at the end kudriavzevii during wine fermentation [58]. Palm of fermentation and a previous characterization wine is currently not processed under cold [5] showed a predominance of Acetobacter storage and the effects of temperature or cold species. In that characterization, a high level of storage processing on flavor and aroma is not diversity was observed at the intra-species level known. and it was suggested that Acetobacter species may have a determinant role in the later stages 3.3 Ethanol and Phenols of palm wine fermentation. Acetoin belongs to the compound class acyloins which are organic Ethanol is the alcohol that is easily detected in compounds containing an alpha hydroxy ketone. wines and palm wine. The distinct aroma is It has a pleasant buttery odor and is a recognizable by most people and the compound component of the butanediol cycle in varies in concentration of wines and palm wine microorganisms where it is used in the cytoplasm from different regions of the world. Yeasts of yeasts as an external energy store [54]. The resistance to ethanol in palm wine and wines is compound appears to have an aroma function in generally recognized to be the reason the wines and palm wine. organism dominates during beverage fermentation. This has been attributed in part to 3.5 Quantity of Alcohols and Esters in yeast’s physiological characteristics which were Palm Wine and Standard Wines not modified throughout the adaptation to human-manipulated fermentative environments According to Stribny et al. [66], acetate esters [59]. Wines contain more ethanol than palm wine and higher alcohols produced during

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fermentation by yeast significantly contributes to [73] and fruit wines from mango [74], pine apple the aroma character of alcoholic beverages. The [75] and water melon [76] with promising results. report highlighted that the major component of However, these efforts in the laboratory have not aromatic higher alcohols is 2-phenylethanol that been translated to commercial success even can be generated from aromatic amino acid though the technology to make this possible is phenylalanine [67]. A comparison of the palm now available. It has been shown that industrial wine samples from a previous report [12] with the yeasts can be bred for direct commercial alcohol and ester content of some wines application [77] and the ATF 1 genes responsible described by Cheng et al. [68] showed that the for sweet smelling esters in Saccharomyces higher and primary alcohols were generally lower species [78] can be altered to make new or in various palm wine samples (Fig. 2). The Italian improved flavors. This can be applied to palm Riesling wine had the highest amount of 2- wine production by selection of novel strains for phenylethanol and ethyl acetate whereas 1- better aroma and flavor. The authors are not propanol and ethyl octanoate occurred highest in aware of any country that has approved the use cabernet sauvignon wine. The wine processing of genetically modified (GM) yeasts for palm wine method used may have caused these production. However, application of GM yeast to differences. Also the generation of alcohols and palm wine production may be commercially esters can be affected by pH, temperature, relevant in that the fermentation period of palm substrate concentration [69] and fermentation wine may be extended or delayed to produce a medium gas-liquid balance [70]. Furthermore, desired flavor. the yeast strains used for fermentation may determine the flavor compounds produced A previous report [79] has shown that production [71]. of primary and secondary metabolites is complex and requires creative designs to develop new 4. PROSPECTS OF VINTAGE PALM WINE technology. These new methods in addition to enological parameters optimization has enabled A previous investigation explored the possibilities standardization of fermented foods in developed of fermenting palm wine in a controlled countries [80]. Yang et al. [81] has suggested environment [72] by using a model that that if traditional fermented foods are promoted compared well with experimental results. Some with high throughput biotechnologies, the other studies have been carried out by using industrialization of local fermented food will yeasts from Nigerian palm wine to make beer increase.

Fig. 2. Comparison of some alcohols and esters content in palm wine (Pw) samples from previous reports. Samples from two different types of trees [12] namely Elaeis sp. (E) and Raphia sp. (R) were compared with different types of wine [68]

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