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D-Fructose Assimilation and Fermentation by Yeasts Belonging to Saccharomycetes: Rediscovery of Universal Phenotypes and Elucidation of Fructophilic Behaviors in Ambrosiozyma platypodis and Cyberlindnera americana

Microbe Division/Japan Collection of Microorganisms, RIKEN BioResource Research Center (RIKEN BRC-JCM), 3-1-1 Koyadai, Tsukuba, Ibaraki 305-0074, Japan
Author to whom correspondence should be addressed.
Microorganisms 2021, 9(4), 758;
Received: 9 December 2020 / Revised: 14 March 2021 / Accepted: 16 March 2021 / Published: 5 April 2021
(This article belongs to the Special Issue Non-Conventional Yeasts)


The purpose of this study was to investigate the ability of ascomycetous yeasts to assimilate/ferment d-fructose. This ability of the vast majority of yeasts has long been neglected since the standardization of the methodology around 1950, wherein fructose was excluded from the standard set of physiological properties for characterizing yeast species, despite the ubiquitous presence of fructose in the natural environment. In this study, we examined 388 strains of yeast, mainly belonging to the Saccharomycetes (Saccharomycotina, Ascomycota), to determine whether they can assimilate/ferment d-fructose. Conventional methods, using liquid medium containing yeast nitrogen base +0.5% (w/v) of d-fructose solution for assimilation and yeast extract-peptone +2% (w/v) fructose solution with an inverted Durham tube for fermentation, were used. All strains examined (n = 388, 100%) assimilated d-fructose, whereas 302 (77.8%) of them fermented d-fructose. In addition, almost all strains capable of fermenting d-glucose could also ferment d-fructose. These results strongly suggest that the ability to assimilate/ferment d-fructose is a universal phenotype among yeasts in the Saccharomycetes. Furthermore, the fructophilic behavior of Ambrosiozyma platypodis JCM 1843 and Cyberlindnera americana JCM 3592 was characterized by sugar consumption profiles during fermentation.

1. Introduction

Physiological tests have long been utilized to characterize yeast species with poor morphological traits. As is similar to the situations in taxonomic studies for the majority of bacteria, physiological properties have been a major feature in distinguishing and identifying yeast species until the era of molecular phylogeny. Although the importance of molecular phylogeny is widely accepted in the field of the systematics of microbes, physiological characterization has been an important aspect of new taxon descriptions. A set of common sugars, alcohols, sugar alcohols, and organic acids has been routinely used for assimilation tests of carbon compounds for yeasts. The fundamental methodology of carbon assimilation test for yeasts was published more than 70 years ago [1] and then standardized in the monograph “The Yeasts, a Taxonomic Study” [2]. In the latest version of the monograph, “The Yeasts, a Taxonomic Study, 5th edition”, published in 2011 [3], assimilation of 36 carbon compounds was routinely profiled for almost all ascomycetous yeast species. However, d-fructose was still not included.
Fructose is a ketonic C6-monosaccharide naturally found in many plants. For instance, grapes are a rich source of sugars, containing equal amounts of glucose and fructose, and their total hexose content typically ranges from 160 to 300 g·L−1 [4]. The ability of Saccharomyces cerevisiae to ferment fructose was well documented in the early 20th century [5]. The presence of fructose in the natural environment, such as in fruits, and its importance as a carbon source have been highlighted in some previous studies, particularly in the field of food microbiology. For instance, fructose serves as the carbon source metabolized by yeasts during grape spoilage [6,7] or wine fermentation [8]. The fructophilic yeasts Zygosaccharomyces rouxii and Z. bailii are involved in canned fruit or fruit juice spoilage [9]. The characteristic fructophilic behavior of Zygosaccharomyces species is associated with the presence of the fructose facilitator Zygosaccharomyces genes, which encode hexose transporters [10]. Despite its ubiquitous presence in the natural environment and despite knowledge of its potential utility as a substrate for fermentation, fructose has not been included in the standard set of assimilation of carbon compounds since the first publication of the monograph, “The Yeasts, a Taxonomic Study”. Consequently, there is still limited data available on the ability of yeasts to assimilate/ferment fructose.
According to Wickerham and Burton (1948) [1] and Miller and Phaff (1958) [11], carbon assimilation tests were perhaps first applied to yeasts by Beijerinck in 1889 [12]. The methods were reexamined by Wickerham and Burton 1948 [1], and then well-establish in the monograph “The Yeasts, a Taxonomic Study” [2], which has long been accepted as the gold standard of characterization for yeasts. Wickerham and Burton 1948 [1] mentioned—“Up to the present time the carbon sources used in assimilation tests in the major attempts at yeast classification have been limited to glucose, fructose, mannose, …” However, fructose was not included in the standard set of carbon assimilation tests in “The Yeasts, a Taxonomic Study” (1952) [2]. This monograph mentioned that tests with fructose had been omitted because, during many years, experiences have taught us that the rule, first formulated by Kluyver, according to which a yeast able to ferment glucose can also ferment fructose and mannose, holds good without a single exception [2] (p. 22); perhaps the “Kluyver” mentioned herein would designate the literature of Kluyver (1912) [13]. Due to this exclusion of fructose from the standard set, studies on fructose fermentation/assimilation have been intermittent since then. In 1985, Konno et al. examined the so-called Kluyver rule using over 200 yeast type strains and reported the results very briefly on half of one page [14]. The authors mentioned that the “Kluyver rule” was generally true, with a special emphasis on Torulopsis halophila (current name: Wickerhamiella versatilis; the strain used in the study was not specified) that was negative for fructose fermentation, despite being positive for glucose fermentation. It is very disappointing that the materials and methods were not described in detail [14]. Therefore, very little detailed information is available about the previous examination of the “Kluyver rule”.
In the course of phenotypic quality control of yeast strains in our culture collection at Microbe Division/Japan Collection of Microorganisms, RIKEN BioResource Research Center (RIKEN BRC-JCM), we confirmed that many strains actually had the ability to ferment fructose. This led to the survey of the capability of a wide variety of yeasts in the Saccharomycetes (Saccharomycotina, Ascomycota) to assimilate/ferment fructose, namely reexamination of the “Kluyver rule” by using JCM strains. Thus, the purpose of this study was to identify the range of yeast species that are capable of utilizing fructose. We also reexamined their ability to assimilate/ferment sucrose. Sucrose is a common disaccharide that can be hydrolyzed by invertase to glucose and fructose [15]. The ability of glucose and sucrose assimilation or fermentation has been examined in almost all known ascomycetous yeast species. Specifically, in the present study, the generality of fructose assimilation or fermentation was evaluated by comparing their positive percentages.
As will be presented hereafter in this paper, universal phenotypes of “fructose assimilation” and “fructose fermentation” of yeasts in the Saccharomycetes (Saccharomycotina, Ascomycota) were rediscovered in this study. The reasons underlying the lack of information about the phenotypes have also been discussed. In addition, fructose and glucose consumption in the fermentation liquid media by two yeast strains, Ambrosiozyma platypodis JCM 1843 and Cyberlindnera americana JCM 3592, was monitored as they exhibited specific fructophilic behaviors. Please note that the term “fructose” in the present paper always indicates d-fructose.

2. Materials and Methods

2.1. Yeast Strains

Yeast strains used in this study were obtained from RIKEN BRC-JCM. The strains examined for the assimilation/fermentation tests are listed in Table 1. Strain information, including the voucher numbers, isolation source, and GenBank accession numbers of the reference nucleotide sequence, is described in the online strain catalog of RIKEN BRC-JCM (; 16 March 2021). Most of them belonged to the Saccharomycetes (Saccharomycotina, Ascomycota). A few species in the genus Schizosaccharomyces and Saitoella complicata in Taphrinomycotina and Trichosporiella flavificans in Pezizomycotina were also employed. The yeast strains were incubated at 25 °C for precultivation, assimilation, and fermentation, with the exception of Cyberlindnera rhizosphaerae JCM 16499 (8 °C), Debaryomyces coudertii JCM 2387 (15 °C), Kazachstania telluris JCM 5298 (37 °C), and Wickerhamomyces patagonicus JCM 16381 (15 °C).

2.2. Assimilation of Fructose

The assimilation of fructose was examined using the conventional method for yeast identification [3]. Experiments on fructose and sucrose assimilation were performed twice independently using commercially available highly pure reagents obtained from the two different suppliers. Briefly, an aqueous stock solution containing 6.7% (w/v) yeast nitrogen base (YNB, Difco Labs, Thermo Fisher Scientific, Waltham, MA, USA, 239210) and 5% (w/v) fructose (Nacalai Tesque, Inc., Kyoto, Japan, GR grade, cat. 16315-55; FUJIFILM Wako Chemical Corporation, Miyazaki, Japan, GR grade, cat. 147-02765) was filter-sterilized, and 0.2 mL of the sterilized stock solution was mixed with 1.8 mL of sterile distilled water in a sterile glass test tube to prepare a working liquid medium containing 0.67% (w/v) YNB and 0.5% (w/v) fructose. Glucose (Nacalai Tesque, Inc., GR grade, cat. 16806-25) or sucrose (Nacalai Tesque, Inc., GR grade, cat. 30404-45; Kanto Chemical Co.,INC., Tokyo, Japan, GR grade, cat. 37000-01) were also employed instead of fructose in the above-mentioned assimilation medium as a reference. A plain YNB solution was used as a negative control. Yeast culture was prepared on YM agar (2.1% (w/v) of YM broth (Difco Labs., Thermo Fisher Scientific, 271120) plus 2% (w/v) agar (Nacalai Tesque, Inc., cat. 01028-85)) 2–7 days before inoculation and a vigorously grown culture was inoculated into the liquid media. Growth was visually monitored and scored weekly for up to four weeks. Growth was measured according to the above-mentioned monograph with some modifications [3]. Briefly, the degree of growth in the liquid medium was observed by the naked eye after shaking the test tube to disperse the yeast cells. The test tube was placed on a white file card, on which 0.75 mm thick black lines were drawn at intervals of approximately 5 mm. The results were scored as 3+ when the lines were completely obscured, 2+ when the lines appeared as diffused bands, 1+ when the lines were distinguishable but had blurred edges, and negative when the lines were distinct with sharp edges. The results were as follows: Strongly positive (3+ reading developed within 1 week), positive (2+ or 3+ reading developed within 2 weeks), slowly positive (2+ or 3+ reading developed slowly over a period exceeding two weeks), delayed positive (2+ or 3+ reading developed rapidly but after two weeks), weakly positive (1+ reading developed), and negative (little (less than 1+ reading) or no growth).

2.3. Fermentation of Fructose

Fermentation of fructose was also examined by the conventional method for yeast identification [3]. Experiments on fructose and sucrose fermentation were performed twice independently using commercially available highly pure reagents obtained from the two different suppliers. Briefly, 4.5 mL of sterile fermentation basal medium containing 0.45% (w/v) bacto yeast extract (Difco Labs., Thermo Fisher Scientific, 212750), 0.75% (w/v) bacto peptone (Difco Labs., 211677), and ~50 ppm bromothymol blue (Sigma-Aldrich, St. Louis, MO, USA, B8630) was prepared in a glass test tube with a small, inverted Durham tube inside. An aqueous stock solution of 20% (w/v) fructose (Nacalai Tesque, Inc., GR grade, cat. 16315-55; FUJIFILM Wako Chemical Corporation, GR grade, cat. 147-02765) was filter-sterilized, and 0.5 mL of the sterilized stock solution was added to the fermentation basal liquid medium to obtain a final concentration of 2% (w/v) fructose. Glucose (Nacalai Tesque, Inc., GR grade, cat. 16806-25) or sucrose (Nacalai Tesque, Inc., GR grade, cat. 30404-45; Kanto Chemical Co.,INC., GR grade, cat. 37000-01) were also employed instead of fructose in the above-mentioned fermentation medium as a reference. Yeast culture was prepared in the same manner as for assimilation tests, and a vigorously grown culture was heavily inoculated into the liquid media. Filling with gas in the inverted tube (Supplementary Figure S1) was visually monitored and scored about every second day up to one week and then at two and three weeks after inoculation. The results were scored according to the above-mentioned monograph with some modifications as follows [3]: Strongly positive (the Durham tube rapidly filled with gas within three days), positive (more than half of the Durham tube filled with gas within seven days), slowly positive (more than half of the Durham tube filled with gas after more than seven days), delayed positive (more than half of the Durham tube rapidly filled with gas, but only after more than seven days), weakly positive (less than half of the Durham tube filled with gas), or negative (no gas accumulation observed in the Durham tube).

2.4. Sugar Consumption during Fermentation

Sugar consumption by A. platypodis JCM 1843, C. americana JCM 3592, and S. cerevisiae JCM 7255 in the fermentation liquid media was monitored, as the former two strains exhibited apparent fructophilic behaviors during fermentation (see Section 3.2.).
Fermentation liquid media were prepared in the same manner as described in Section 2.3 with the following modifications. The total amount of medium was 7 mL in a glass test tube to allow a series of liquid medium sampling, and bromothymol blue was not added to the media to avoid interference with absorbance at 340 nm in the subsequent measurement using a spectrophotometer. Three kinds of fermentation media were prepared: (i) 2% (w/v) fructose, (ii) 2% (w/v) glucose, and (iii) 2% (w/v) fructose plus 2% (w/v) glucose (final concentrations in the media). To prepare the fructose–glucose mixed medium (iii), an aqueous stock solution of 20% (w/v) fructose (Nacalai Tesque, Inc.) plus 20% (w/v) glucose (Nacalai Tesque, Inc.) was filter-sterilized, and then 0.7 mL of the sterilized stock solution was added to 6.3 mL of the fermentation basal liquid medium.
Strains JCM 1843, JCM 3592, and JCM 7255 were cultured on YM agar at 25 °C for 2–3 days, and the freshly prepared culture was incubated in the basal fermentation medium at 25 °C for 2 days. The three fermentation media (i), (ii), and (iii) were inoculated with the culture and incubated at 25 °C without shaking. Inoculation was done in quadruplicates. The fermentation medium was sampled after gentle mixing by pipetting at approximately 12 h intervals for JCM 7255 and approximately 12–48 h intervals for JCM 1843 and JCM 3592. The sampled media were centrifuged to remove cells, and the supernatant was heated at 90 °C for 10 min to deactivate enzymes and then stored at −20 °C for measuring the fructose and glucose concentrations.
The concentration of fructose and glucose in the fermentation media was measured and calculated using an enzymatic test kit d-glucose/d-fructose (Boehringer Mannheim/R-Biopharm, Darmstadt, Germany, cat. 10 139 106 035) following the manufacturer’s instructions with some modifications. The absorbance of the solution in a 96-well microplate was measured at 340 nm using a spectrophotometer Multiskan SkyHigh (Thermo Fisher Scientific).

3. Results

3.1. Assimilation of Fructose

All 388 strains tested had the ability to assimilate fructose as well as glucose, utilizing fructose as the sole carbon source (Table 1). Sucrose was assimilated by fewer yeast strains than those capable of assimilating fructose; 229 (59.0%) out of the 388 strains assimilated sucrose (including strains of positive reaction delayed, slowly, and weakly positive).

3.2. Fermentation of Fructose

Three hundred and two (77.8%) out of the 388 strains had the ability to ferment glucose, and most of these strains could also ferment fructose (Table 1), with the exception of Sporopachydermia quercuum JCM 9486, which fermented glucose but not fructose. In contrast, Ambrosiozyma platypodis JCM 1843 showed a stronger and quicker positive reaction to fructose than to glucose. A preference for fructose was also observed; Cyberlindnera americana JCM 3592 fermented fructose well, but not glucose. Thus, 302 (77.8%) of the 388 strains had the ability to ferment fructose. These observations of JCM 9486, JCM 1843, and JCM 3592 were reproduced in three independent trials (Supplementary Table S1).
Similar to the results of assimilation, the number of strains capable of fermenting sucrose (99 strains) was much lower than that of strains capable of fermenting glucose/fructose. In addition, all the strains fermenting sucrose were capable of fermenting both glucose and fructose.

3.3. Sugar Consumption during Fermentation

Sugar consumption by A. platypodis JCM 1843 and C. americana JCM 3592 in the fermentation liquid media was monitored using only 2% fructose or 2% glucose (sugar solo fermentation), or both 2% fructose and 2% glucose (sugar duo fermentation). Figure 1 shows the time-course consumption profiles of fructose and glucose, where the amount of sugars at 0-h (sampled immediately after inoculation) was set as 100%.
In A. platypodis JCM 1843 and C. americana JCM 3592, the sugar consumption profiles were similar to each other in both sugar solo fermentation and sugar duo fermentation. Fructose was more rapidly consumed than glucose in sugar solo fermentation. On the contrary, fructose consumption was substantially slower in sugar duo fermentation than in sugar solo fermentation; instead, glucose consumption was observed before fructose consumption.
Saccharomyces cerevisiae JCM 7255 rapidly consumed both fructose and glucose, which were almost used up at 36 h in both sugar solo/duo fermentation. Glucose consumption was always more rapid than fructose consumption. Fructose consumption in sugar duo fermentation was apparently less rapid than in sugar solo fermentation.

4. Discussion

The results of this study are very simple; all the yeast strains tested could assimilate glucose, and glucose fermenters were fructose fermenters, with a few exceptions. This strongly suggests that the utility of fructose is universal among yeasts in the Saccharomycetes. Positive reactions in assimilation and fermentation of fructose should be regarded as universal phenotypes rediscovered by this survey. We employed approximately 380 species of yeasts belonging to the Saccharomycetes. This accounts for almost one-third of the described ascomycetous yeast species. As we used a taxonomically wide variety of yeasts, there is no doubt about the generality of the positive reactions in the fructose assimilation/fermentation tests, at least for the Saccharomycetes. Thus, the “Kluyver rule” was confirmed on the whole.
We searched the capability of assimilation/fermentation of other common sugars by ascomycetous yeasts, based on the data in the monograph “The Yeasts, a Taxonomic Study, 5th edition” [3] (Table 2). As shown in Table 2, the percentage of assimilating/fermenting sucrose was 59.0%/25.5% in this study, whereas it was 60.7%/24.2% in the monograph, suggesting that the selection of yeast species employed in this study was unbiased. Judging from the higher positive percentages for both assimilation and fermentation of fructose compared to those of the other sugars, it is safe to say that fructose is an easy-to-use carbon source for the yeasts.
The ability to ferment fructose by brewer’s yeast was well-known as early as in the first half of the 20th century, particularly in the context of “selective fermentation” observed in a mixture of glucose and fructose ([5,16] and the literature cited therein). However, yeast taxonomists have not paid serious attention to fructose. To the best of our knowledge, no recent work, except one, has employed fructose to characterize new yeast species [17]. In a recent publication, fructose was used to prepare an enrichment medium for the isolation of highly osmotolerant yeasts from natural substrates, as its solubility is much higher than that of glucose; unfortunately, assimilation/fermentation of fructose was not determined in the characterization of new species [18].
Why have such simple phenotypes largely neglected until now? The reasons would be: (1) fructose was not selected in the standard set of physiological characterization throughout the monograph “The Yeasts, a Taxonomic Study”; (2) physiological profile has been used mostly just as a key for yeast taxonomy; thus, fructose has been out of focus even though it occurs abundantly in the natural environment, such as in honey and fruits. Probably due to such a historical background, most of the recent researchers excluded physiological tests of fructose from the description of new yeast species, likely without paying attention to the “Kluyver rule”.
In the present work, some strains exhibited fructophily during fermentation, preferring fructose, as a substrate for fermentation, to glucose. As stated in the results section, A. platypodis JCM 1843 and C. americana JCM 3592 appeared to be fructophilic in the regular fermentation test (Table 1). Furthermore, JCM 1843 and JCM 3592 demonstrated a fructophilic behavior, as determined by sugar consumption profiles in sugar solo fermentation, and this is contradictory to the pattern of sugar consumption by S. cerevisiae JCM 7255, which always preferred glucose to fructose (Figure 1). Initially, we hypothesized that JCM 1843 and JCM 3592 might exhibit a fructophilic behavior even in sugar duo fermentation (mixed fermentation), similar to Zygosaccharomyces species [19]. However, to our surprise, fructose consumption appeared to be suppressed in sugar duo fermentation (Figure 1). It is remarkable that glucose fermentation by JCM 1843 and JCM 3592 seemed to be activated by the presence of fructose in the medium. To the best of our knowledge, this is a new “irregular” pattern of sugar consumption profile. Further molecular biological investigations are required to clarify the mechanism underlying this phenomenon.
In contrast to A. platypodis and C. americana, S. quercuum JCM 9486 exclusively prefers glucose over fructose, and this is similar to the case reported previously for W. versatilis [14]. The reason for this exception, however, remains unknown. These specific preferences of sugar may be related to their lifestyles in the natural environment, which is a fascinating research theme from the viewpoint of yeast ecology. For instance, A. platypodis and C. americana likely inhabit a fructose-rich environment, and therefore, possess potent fructose transporter(s). Furthermore, the fructophilic behavior in A. platypodis and C. americana would be adaptive to such an environment.
Zygosaccharomyces rouxii and Z. bailii were reported to be fructophilic [19], although a clear fructophilic reaction was not observed in our simple experiments. In a previous study, Z. bailii was found to first ferment fructose and then glucose in a medium containing both glucose and fructose [19]. The experimental conditions in the present study differed from those in the previous one. As the fermentation test was performed using either glucose or fructose separately in the present study, the priority of sugar utilization remained unknown. Additional yeast strains exhibiting a fructophilic phenotype may be found if fermentation tests using a medium containing both glucose and fructose are performed. Later, fructose transporters in the plasma membrane of the Zygosaccharomyces yeasts were studied with molecular biological interests in their fructophilic behavior [20,21,22]. In addition, the mechanism of fructose fermentation has been well investigated on a molecular basis in the wine yeast S. cerevisiae [4]. S. cerevisiae contains at least 20 transporters associated with hexose uptake [23]. Glucose uptake is facilitated by hexose transporters [24]. Following its uptake into the cell cytoplasm, glucose is phosphorylated to glucose-6-phosphate, subsequently isomerized to fructose-6-phosphate, and finally metabolized through the glycolytic pathway [25]. Fructose is transported by the hexose transporter (HXT) family of proteins [26] and directly phosphorylated to fructose-6-phosphate by hexokinases, such as Hxk1 and Hxk2 [27]. Our data indicate that most of the yeasts belonging to the Saccharomycetes would exhibit fructose transporters and express specific hexokinases that metabolize fructose to fructose-6-phosphate. Indeed, a novel proton-coupled fructose transporter, Frt1, has been identified in Kluyveromyces lactis [28]. The mechanism of fructose uptake and its subsequent metabolism would be further investigated from the viewpoint of molecular biology using a wider variety of ascomycetous yeast species. Novel fructose transporters may be identified by exploring FRT1 gene analogs using the draft genome sequences of ascomycetous yeasts.
In this study, we aimed to survey a wide variety of yeast species belonging to Saccharomycetes; thus, a single strain of each species was tested for its ability to assimilate and ferment fructose, except A. platypodis (JCM 1843 and JCM 1796) and C. americana (JCM 3592 and JCM 3593). Although the fructophilic behavior was less apparent in JCM 1796 and JCM 3593 than in JCM 1843 and JCM 3592, respectively (Table 1), both A. platypodis and C. americana preferably fermented fructose. Additional reference strains should be surveyed for fructose assimilation and fermentation, particularly for A. platypodis, C. americana, S. quercuum, and W. versatilis, to conclude the exceptions are species-specific. In addition, we should examine the assimilation/fermentation profiles of basidiomycetous yeasts in future studies to determine whether fructose assimilation/fermentation is a universal phenotype in yeasts irrespective of their taxonomic position.
Lastly, it is suggested that tests for fructose should be resurrected in the standard set of physiological characterization for yeasts in the Saccharomycotina subphylum in order not to miss the special characteristics of yeasts.

Supplementary Materials

The following are available online at, Figure S1: Gas filling in a Durham tube in the fermentation liquid medium, Table S1: (a) Growth in the assimilation media containing each sugar, (b) Filling of gas in Durham tube in the fermentation media containing each sugar.

Author Contributions

Conceptualization, R.E.; methodology, R.E.; validation, R.E. and M.O.; investigation, M.H. and R.E.; resources, M.H., M.O. and R.E.; data curation, R.E.; writing—original draft preparation, R.E.; writing—review and editing, M.O., M.H. and R.E.; visualization, R.E.; supervision, M.O.; project administration, R.E. and M.O.; funding acquisition, R.E. and M.O. All authors have read and agreed to the published version of the manuscript.


This research was partially funded by JSPS KAKENHI Grant Number 19K06160 to R.E. and 19H05689 to M.O.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Data supporting results can be found in Supplementary Table S1.


The authors thank Yuma Yoshihashi for his assistance to refer the book “The Yeast, a Taxonomic Study, 2nd revised and enlarged edition” edited by J. Lodder.

Conflicts of Interest

The authors declare no conflict of interest. The funders had no role in the design of the study, in the collection, analyses, or interpretation of data, in the writing of the manuscript, or in the decision to publish the results.


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Figure 1. Sugar consumption profiles in the fermentation liquid media. The green square and blue circle indicate the percentage of fructose and glucose concentrations, respectively, compared with the initial amount of each sugar at 0 h. The left three graphs show sugar consumption by yeasts incubated in only 2% fructose or 2% glucose in the fermentation media. The right three graphs show sugar consumption by yeasts incubated in the fermentation medium containing both 2% fructose and 2% glucose. The bar on the symbols indicates standard deviation. Asterisk (*) indicates a significant difference between fructose and glucose percentages (Welch’s t-test, p < 0.01).
Figure 1. Sugar consumption profiles in the fermentation liquid media. The green square and blue circle indicate the percentage of fructose and glucose concentrations, respectively, compared with the initial amount of each sugar at 0 h. The left three graphs show sugar consumption by yeasts incubated in only 2% fructose or 2% glucose in the fermentation media. The right three graphs show sugar consumption by yeasts incubated in the fermentation medium containing both 2% fructose and 2% glucose. The bar on the symbols indicates standard deviation. Asterisk (*) indicates a significant difference between fructose and glucose percentages (Welch’s t-test, p < 0.01).
Microorganisms 09 00758 g001
Table 1. Fructose assimilation and fermentation profiles of Saccharomycetes yeasts.
Table 1. Fructose assimilation and fermentation profiles of Saccharomycetes yeasts.
SpeciesJCM no.AssimilationFermentation
Saccharomycetes, Saccharomycotina
Cephaloascus fragrans7613++--- 1- 1
Candida aaseri1689+++/s---
Candida albicans1542+ST+ST+ST+ST+ST-
Candida atlantica9548+ST+ST+STw/-w/--
Candida atmosphaerica9549+ST+ST+ST++-
Candida boleticola1500++-+ST+ST-
Candida buinensis9453+ST+ST+ST+ST+ST-
Candida conglobata2373++-+ST+ST-
Candida dendronema1803++++ST+ST-
Candida diddensiae9598+++++-
Candida fluviatilis9552+++++-
Candida friedrichii9553+++++-
Candida glaebosa1590+ST+ST+-- 1- 1
Candida insectamans9611++----
Candida insectorum9457+++++-
Candida lyxosophila7532++++ST+-
Candida maltosa1504+ST+ST++ST+ST+ST
Candida multigemmis9559+++++-
Candida oleophila1620++++ST+ST-
Candida palmioleophila5218+++-- 1- 1
Candida membranifaciens9450+ST+ST+ST+++
Candida naeodendra1509++++ST+ST-
Candida neustonensis14892+ST+ST+ST+++/s
Candida parapsilosis1612+ST+++ST+ST-
Candida pseudoglaebosa2168+++++-
Candida saitoana1438+ST++---
Candida santamariae1816++-+ST+ST-
Candida schatavii1778+ST+ST-ss-
Candida sojae1644++++ST+ST+
Candida tammaniensis10730++++ST+ST-
Candida thasaenensis17817++++ST+ST+
Candida tropicalis1541+ST+ST+ST+ST+ST+ST
Candida trypodendroni10731+++++-
Candida psychrophila2388++--- 1- 1
Candida viswanathii9567++++ST+ST-
Candida xestobii9569+++---
Candida zeylanoides1627++----
Danielozyma ontarioensis10729++++++
Debaryomyces coudertii2387++-++-
Debaryomyces hansenii1990+ST+ST+ST+/s+/s+/s
Debaryomyces maramus1528+++w/-w/-w/-
Debaryomyces nepalensis2095+ST+ST+ST+++
Debaryomyces prosopidis9913++++/ss/ws/w
Debaryomyces udenii7855+ST+ST+ST+/d+d/w
Kurtzmaniella fragi1791+ST+ST+ST+ST+ST-
Kurtzmaniella natalensis1445++++ST+ST-
Kurtzmaniella quercitrusa9832++++ST+ST-
Lodderomyces elongisporus1781+ST+ST+ST++-
Meyerozyma guilliermondii10735+ST+ST+ST+++
Millerozyma acaciae10732+ST+ST-+ST+ST-
Millerozyma farinosa10734+ST+ST-+ST+ST-
Millerozyma koratensis12576+ST+ST+ST+++
Priceomyces carsonii8121+ST+ST+-- 1- 1
Priceomyces castillae10733++ST----
Priceomyces fermenticarens9589+ST+ST----
Priceomyces haplophilus1635+ST+ST--- 1- 1
Priceomyces medius10737++----
Priceomyces melissophilus1707+ST+ST+ST-- 1- 1
Scheffersomyces coipomensis8916+ST+ST++ST+ST-
Scheffersomyces ergatensis9599+ST+ST++ST+-
Scheffersomyces insectosa9842++++ST+ST-
Scheffersomyces lignosum9837+ST+++ST+ST-
Scheffersomyces segobiensis10740++++ST+ST-
Scheffersomyces shehatae9840++s+ST+ST-
Scheffersomyces spartiniae10741++++ST+ST-
Scheffersomyces stipitis10742++++ST+ST-
Schwanniomyces capriottii6177+ST+ST+ST+ST+ST+ST
Schwanniomyces etchellsii3656+ST+ST+ST+ST+ST-
Schwanniomyces occidentalis var. occidentalis8123+ST+ST+ST+ST++
Schwanniomyces occidentalis var. persoonii8127++++++
Schwanniomyces polymorphus var. africanus7443+ST+ST+ST+ST+ST+ST
Schwanniomyces polymorphus var. polymorphus3647+ST+ST+ST+ST+ST+
Schwanniomyces pseudopolymorphus3652+ST+ST+ST+ST+ST+ST
Schwanniomyces vanrijiae3657+ST+ST+STwww
Schwanniomyces yamadae6191++++ST+ST-
Wickerhamia fluorescens1821++++ST+ST+
Yamadazyma akitaensis10738+ST+ST+ST++-
Yamadazyma kitorensis31005+ST+STs++-
Yamadazyma mexicana1835+ST+ST+ST++-
Yamadazyma nakazawae7529+ST+ST+ST+ST+ST-
Yamadazyma philogaea10739+++++-
Yamadazyma scolyti3654+++++-
Yamadazyma takamatsuzukensis15410+++++-
Yamadazyma tenuis9827+ST++++-
Yamadazyma triangularis9449+++w/-w/--
Yamadazyma tumulicola15403+ST+ST+++-
Dipodascus aggregatus31687++----
Dipodascus australiensis31688++----
Dipodascus eriense3912++-+/sw/--
Dipodascus fermentans2468++-+ST+ST-
Dipodascus ingens9471++----
Dipodascus ovetensis3706++----
Dipodascus reessii1943++--- 1- 1
Dipodascus tetrasperma6361+ST+ST-+ST+ST-
Geotrichum rectangulatum1750+ST+-+ST+ST-
Babjevia anomala5988++--- 1- 1
Lipomyces kononenkoae5989+++---
Lipomyces lipofer3769+++---
Lipomyces smithiae8928+++-- 1- 1
Lipomyces spencermartinsiae5990+++---
Lipomyces starkeyi5995+++---
Lipomyces suomiensis7660++--- 1- 1
Lipomyces tetrasporus6000+++-- 1- 1
Myxozyma geophila5220++--- 1- 1
Myxozyma kluyveri7661++w-- 1- 1
Myxozyma lipomycoides5198++--- 1- 1
Myxozyma melibiosi5194++--- 1- 1
Myxozyma mucilagina1834+++-- 1- 1
Myxozyma neglecta5197++--- 1- 1
Myxozyma udenii8927+++-- 1- 1
Aciculoconidium aculeatum13354+++ss-
Clavispora fructus1513++-+ST+ST-
Clavispora lusitaniae7533++++ST+ST-
Candida akabanensis9115+ST+ST+ST+ST+ST+ST
Candida auris15448+ST+ST+ST+++
Candida haemulonii3762+ST+ST+ST+ST+ST+
Candida intermedia1607+ST+++ST+ST+ST
Candida melibiosica9558++++ST+ST-
Candida mogii1611++++ST+ST+ST
Candida pseudointermedia1592+ST+ST+ST+ST+ST+ST
Candida fukazawae1641++++ST+ST-
Candida fungicola10142+ST+ST+ST---
Candida mesenterica2368+++---
Candida musae1598++++ST+ST-
Candida oregonensis1811+ST+ST++ST+ST-
Candida pseudohaemulonii12453+ST+ST+ST+ST++
Candida tsuchiyae1638+ST+ST+ST+ST+ST+
Hyphopichia burtonii3708++++++
Hyphopichia fennica9849++++ST+ST+
Hyphopichia gotoi10145++++ST+ST+ST
Hyphopichia homilentoma1507+ST+++ST+ST-
Hyphopichia khmerensis13262+ST+ST+ST+++
Hyphopichia pseudoburtonii16346++++ST+ST+
Hyphopichia rhagii9839+ST+ST+ST+ST+ST+ST
Metschnikowia agaves31832++++/s+/s-
Metschnikowia kofuensis12563+++/s++-
Metschnikowia lunata1798++++ST+ST-
Metschnikowia reukaufii7534+++++-
Metschnikowia torresii1845+ST+ST-+ST+ST-
Metschnikowia viticola12561+++++-
Komagataella pastoris3650+ST+ST-+ST+ST-
Phaffomyces opuntiae1836++--- 1- 1
Phaffomyces thermotolerans1837++--- 1- 1
Candida ethanolica9588++-s/-s/--
Candida inconspicua9555++-++-
Candida pseudolambica9830+ST+ST-+ST+ST-
Candida rugopelliculosa1593++-+ST+ST-
Candida silvatica9828++----
Dekkera anomala31686+ST+ST++ST+ST+
Dekkera bruxellensis11407++++ST+ST+ST
Kregervanrija fluxuum3646++-+/s+/s-
Pichia cactophila1830++-+/s+/w-
Pichia exigua1829++-ww-
Pichia heedii1833++-+/w+/w-
Pichia kluyveri var. kluyveri11403++-+ST+ST-
Pichia membranifaciens1442++-ww-
Pichia myanmarensis12922+ST+ST+ST+ST+ST+
Pichia nakasei1699+ST+ST-+ST+ST-
Pichia occidentalis1711+ST+-+ST+ST-
Pichia rarassimilans14993++-ss-
Pichia terricola1709+ST+-++-
Saturnispora ahearnii10726++ST-+ST+ST-
Saturnispora besseyi1706+ST+-+ST+ST-
Saturnispora dispora1795++-+ST+ST-
Saturnispora diversa1848++-+ST+ST-
Saturnispora saitoi1793+ST+ST-+ST+ST-
Saturnispora silvae6352+ST+-+/s+/s-
Saturnispora zaruensis1515+ST+-+ST+ST-
Candida castellii9550++-+ST+ST-
Candida glabrata3761++-+ST+ST-
Issatchenkia orientalis1710+ST+ST-+ST+ST-
Kazachstania aerobia31691++-+ST+ST-
Kazachstania bulderi31689++++ST+ST+
Kazachstania exigua1790++++ST+ST+
Kazachstania humilis9852++-+ST+ST-
Kazachstania servazzii5179++-+ST+ST-
Kazachstania telluris5298++-+ST+/w-
Kazachstania transvaalensis5178++-+ST+ST-
Kazachstania unispora5180++-+ST+ST-
Kluyveromyces marxianus9556++++ST+ST+ST
Kluyveromyces nonfermentans10232++----
Lachancea kluyveri7257++++ST+ST+ST
Lachancea thermotolerans19085++++ST+ST+
Lachancea waltii10745++++ST+ST+ST
Saccharomyces bayanus7258++++ST+ST+ST
Saccharomyces cerevisiae7255++++ST+ST+ST
Saccharomyces pastorianus7256++++ST+ST+ST
Tetrapisispora arboricola10813++-+ST+ST-
Tetrapisispora iriomotensis10810++-+ST+ST-
Tetrapisispora namnaoensis12664++-+ST+ST-
Tetrapisispora nanseiensis10811++-+ST+ST-
Torulaspora delbrueckii31684++-+ST+ST-
Torulaspora pretoriensis3662++++ST+ST+
Zygosaccharomyces rouxii7619++w/-+ST+STs
Zygosaccharomyces rouxii22060++-+ST+ST-
Zygosaccharomyces siamensis16825++-+ST+STs/w
Zygotorulaspora mrakii1800++++ST+ST+
Hanseniaspora opuntiae31690++-+ST+ST-
Candida fragicola1589++-+ST+ST-
Saccharomycopsis capsularis7619++w/-+ST+STs
Saccharomycopsis crataegensis1700++-++-
Saccharomycopsis fibuligera7609++++ST+ST+
Saccharomycopsis javanensis3707++--- 1- 1
Saccharomycopsis malanga7620++-+/s+-
Saccharomycopsis selenospora7616++----
Saccharomycopsis synnaedendra7607++--- 1- 1
Saccharomycopsis vini7623++++++
Blastobotrys adeninivorans8914+ST+ST+ST+ST++/s
Blastobotrys arbuscula2926++-+ST+-
Blastobotrys aristata2929++s+ST+ST-
Blastobotrys capitulata2934++-+ST+ST-
Blastobotrys chiropterorum9597+++---
Blastobotrys elegans2931++-++/w-
Blastobotrys gigas2927++-+ST+-
Blastobotrys nivea2933++s++-
Blastobotrys parvus9487++s---
Blastobotrys proliferans2928+++++-
Blastobotrys terrestris8913+++---
Candida santjacobensis8924+++++-
Groenewaldozyma auringiensis9593++-+ST+-
Groenewaldozyma salmanticensis8896++++ST+ST+ST
Middelhovenomyces petrohuensis8922+++---
Middelhovenomyces tepae10265++sw--
Sugiyamaella castrensis9585+++w/---
Sugiyamaella paludigena9614+++---
Sugiyamaella valdiviana9565++++/ww/--
Trichomonascus ciferrii7621+++---
Wickerhamiella azyma1691+++---
Wickerhamiella domercqiae9478+++/w-- 1- 1
Wickerhamiella galacta8257++----
Wickerhamiella hasegawae12559++-++/w-
Wickerhamiella kazuoi12558++----
Wickerhamiella pararugosa1512++--- 1- 1
Wickerhamiella sorbophila1514++----
Wickerhamiella spandovensis9562++++STww
Wickerhamiella vanderwaltii9615++----
Wickerhamiella versatilis8065++++ST+ST+ST
Zygoascus biomembranicola31007++-+ST+-
Barnettozyma salicaria3653++---- 1
Barnettozyma wickerhamii21961+ST+ST+ST++-
Candida berthetii9594++-++-
Candida danieliae17247+ST+ST++ST+-
Candida dendrica9605++-++/s-
Candida easanensis12476+++/s++-
Candida eppingiae17241+ST+ST+ST+ST+ST-
Candida freyschussii9850+++/s++-
Candida maritima9612++++++
Candida montana2323++--- 1- 1
Candida nakhonratchasimensis12474++++ST+ST+ST
Candida norvegica8897++----
Candida pattaniensis12475+ST+ST+ST+ST+ST+
Candida pseudoflosculorum17242+ST+ST+ST+ST+ST+ST
Candida quercuum1587+ST+++/w+-
Candida robnettiae17243+ST+ST+ST+ST+ST-
Candida silvicultrix9831++++ST+ST+ST
Candida solani2339++++ST+ST-
Candida vartiovaarae3759++++ST+ST+
Cyberlindnera americana3592+++-+/s-
Cyberlindnera americana3593+++ws-
Cyberlindnera amylophila1702++++ST+ST-
Cyberlindnera bimundalis3591++++/s+/s-
Cyberlindnera fabianii3601+ST+++ST+ST+ST
Cyberlindnera jadinii3617++++ST+ST+ST
Cyberlindnera japonica11402+++ss/w-
Cyberlindnera mississippiensis1703+ST+++ST+ST-
Cyberlindnera mrakii3614++-+ST+ST-
Cyberlindnera petersonii3619++++++
Cyberlindnera rhizosphaerae16499++s+++
Cyberlindnera rhodanensis3649+ST+ST+ST+ST+ST-
Cyberlindnera samutprakarnensis17816++++ST+ST+ST
Cyberlindnera subsufficiens3625++++++
Starmera amethionina1831++-ss-
Starmera pachycereana1832++----
Starmera quercuum3659++-++-
Starmera stellimalicola3546++-+ST+ST-
Wickerhamomyces anomalus3585+ST+ST+ST+ST+ST+ST
Wickerhamomyces bisporus3590+++ww-
Wickerhamomyces bovis3640+ST+ST+ST+ST+ST-
Wickerhamomyces canadensis3597+ST+ST+ST-- 1- 1
Wickerhamomyces chaumierensis17246+ST+ST+ST+ST+ST-
Wickerhamomyces ciferrii3599+ST+ST+ST++ST+
Wickerhamomyces mucosus6814++++ST+ST-
Wickerhamomyces patagonicus16381++----
Wickerhamomyces pijperi11406++-+ST+ST-
Wickerhamomyces silvicola3627+ST+ST++ST+ST-
Wickerhamomyces subpelliculosus3631+ST+ST++ST+ST+ST
Wickerhamomyces sydowiorum9455+ST+ST+ST++ST+
Saccharomycetales incertae sedis
Ambrosiozyma cicatricosa7598+ST+++/s+/s+/s
Ambrosiozyma kamigamensis14990+++/s++-
Ambrosiozyma kashinagicola15019++-++-
Ambrosiozyma llanquihuensis8918++-++-
Ambrosiozyma monospora7599++++ST+ST+/w
Ambrosiozyma neoplatypodis14992++-++-
Ambrosiozyma oregonensis1797+ST++++-
Ambrosiozyma philentoma7600++++/d+d/w
Ambrosiozyma platypodis1843+++w+-
Ambrosiozyma platypodis1796++++/s+-
Ambrosiozyma pseudovanderkliftii15025++s++-
Ambrosiozyma vanderkliftii15029+ST+ST++ST+STw
Babjeviella inositovora10736+++---
Candida arabinofermentans10727++-++-
Candida blankii8259++++/sww
Candida boidinii9604++-+ST+ST-
Candida chilensis1693+++++-
Candida cylindracea9586++-++-
Candida digboiensis12330+++---
Candida entomophila9607++++ST+ST+ST
Candida incommunis8258+++++-
Candida insectalens9610++----
Candida krabiensis12266++----
Candida maris9853++----
Candida methanosorbosa9620++-++-
Candida nanaspora9590++-+ST+ST-
Candida nemodendra9855++-s/-w/--
Candida nitratophila9856++-++-
Candida ovalis9444++-+ST+ST-
Candida pini9826++/s-+/s+/s-
Candida sake2951+ST+++ST+ST-
Candida savonica9561++-++-
Candida sequanensis9841++-+ST+ST-
Candida silvanorum1804++++ST+ST-
Candida sithepensis12265++-+ST+ST-
Candida sonorensis1827++-+ST+ST-
Candida sophiae-reginae8925+ST+ST++ST+ST-
Candida sorboxylosa1536+ST+ST-++-
Candida succiphila9445++-+ST+ST-
Citeromyces matritensis2333++++ST+ST+ST
Citeromyces siamensis11522++++ST+ST+ST
Diutina catenulata1604+ST+-++-
Diutina rugosa1619+ST+--- 1- 1
Kuraishia capsulata1991++-++-
Nadsonia commutata10138++--- 1- 1
Nadsonia fulvescens var. fulvescens9992++-+ST+ST-
Nadsonia starkeyi-henricii11408++----
Nakazawaea anatomiae9547++-++-
Nakazawaea holstii3608+++/s+ST+ST-
Nakazawaea ishiwadae9451++++ST+ST-
Nakazawaea peltata9829++++ST+ST-
Nakazawaea populi9833++s+ST+ST-
Nakazawaea wickerhamii9568++-+ST+ST-
Ogataea angusta3635++++ST+ST-
Ogataea glucozyma3607++-+ST+ST-
Ogataea henricii3611++--- 1- 1
Ogataea kodamae11404++-+/s+/s-
Ogataea methanolica10240++-+ST+ST-
Ogataea methylivora22142+++++-
Ogataea minuta3622++-++ST-
Ogataea naganishii22078+++++-
Ogataea nonfermentans3615++---- 1
Ogataea philodendri22070++----
Ogataea pignaliae9836++-+ST+ST-
Ogataea pini3655++-s/-s/--
Ogataea salicorniae10744++-+ST+ST-
Ogataea siamensis12264++++/s+/s-
Ogataea thermomethanolica12984+++++-
Ogataea trehalophila3651+ST+ST-+ST+ST-
Pachysolen tannophilus31685++-+ST+ST-
Peterozyma toletana3658+ST++++-
Saprochaete japonica2451+ST+ST-+ST+ST-
Sporopachydermia cereana9480++----
Sporopachydermia lactativora9485++--- 1- 1
Sporopachydermia quercuum9486++-+--
Starmerella apicola9592++++++
Starmerella apis8256+ST+ST+-w-
Starmerella bombi9595++++ST+ST+
Starmerella bombicola9596++++ST+ST+ST
Starmerella etchellsii8066++-+s/w-
Starmerella floricola9439++++ST+ST+ST
Starmerella geochares9851++++++/s
Starmerella gropengiesseri8255+++++w
Starmerella lactis-condensi9472++++ST+ST+ST
Starmerella magnoliae1446++++++
Starmerella stellata9476++++ST+ST+ST
Starmerella vaccinii9446++++++
Suhomyces tanzawaensis1648+++s/w+/w-
Teunomyces kruisii1779++++ST+ST-
Trigonopsis cantarellii8260++-+ST+ST-
Trigonopsis variabilis1823++--- 1- 1
Trigonopsis vinaria1813++--- 1- 1
Yarrowia deformans1694++--- 1- 1
Yarrowia keelungensis14894+ST+ST----
Yarrowia lipolytica2320+ST+ST--- 1- 1
Yarrowia yakushimensis12782+ST+ST----
Saitoella complicata7358+++---
Schizosaccharomyces japonicus8264++++ST+ST+ST
Schizosaccharomyces octosporus8261++w++w
Schizosaccharomyces pombe8274++++ST+ST+ST
Trichosporiella flavificans1506++-+ST+ST-
1 Fermentation test examined once; +ST, strongly positive; +, positive; d, delayed positive; s, slowly positive; w, weakly positive; -, negative; a diagonal line “/” indicates “or”.
Table 2. Percentage of yeast species in the Ascomycota capable of assimilating/fermenting common sugars.
Table 2. Percentage of yeast species in the Ascomycota capable of assimilating/fermenting common sugars.
SugarsThis StudyThe Yeasts *
Glucose100% (388/388)77.8% (302/388)100% (827/827)72.8% (602/827)
Fructose100% (388/388)77.8% (302/388)ndnd
Sucrose59.0% (229/388)25.5% (99/388)60.7% (502/827)24.2% (200/827)
Galactosentnt65.4% (541/827)30.6% (253/827)
Trehalosentnt70.0% (579/827)30.1% (249/827)
Maltosentnt56.8% (470/827)18.3% (151/827)
Raffinosentnt28.5% (236/827)13.8% (114/827)
* Data collected from “The Yeasts, a Taxonomic Study, 5th edition” [3]; “v (variable)” counted as positive; the percentages were calculated on the number of species basis. nt, not tested; nd, no data.
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Endoh, R.; Horiyama, M.; Ohkuma, M. D-Fructose Assimilation and Fermentation by Yeasts Belonging to Saccharomycetes: Rediscovery of Universal Phenotypes and Elucidation of Fructophilic Behaviors in Ambrosiozyma platypodis and Cyberlindnera americana. Microorganisms 2021, 9, 758.

AMA Style

Endoh R, Horiyama M, Ohkuma M. D-Fructose Assimilation and Fermentation by Yeasts Belonging to Saccharomycetes: Rediscovery of Universal Phenotypes and Elucidation of Fructophilic Behaviors in Ambrosiozyma platypodis and Cyberlindnera americana. Microorganisms. 2021; 9(4):758.

Chicago/Turabian Style

Endoh, Rikiya, Maiko Horiyama, and Moriya Ohkuma. 2021. "D-Fructose Assimilation and Fermentation by Yeasts Belonging to Saccharomycetes: Rediscovery of Universal Phenotypes and Elucidation of Fructophilic Behaviors in Ambrosiozyma platypodis and Cyberlindnera americana" Microorganisms 9, no. 4: 758.

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