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FEMS Yeast Research, 21, 2021, foab052
https://doi.org/10.1093/femsyr/foab052
Advance Access Publication Date: 2 October 2021
Minireview
MINIREVIEW
Non-conventional yeasts for food and additives
production in a circular economy perspective
Renato L. Binati1,†, Elisa Salvetti1,†, Anna Bzducha-Wr ´
obel2,
Loreta Baˇ
sinskien˙
e3, Dalia ˇ
Ciˇ
zeikien˙
e3, David Bolzonella1and Giovanna
E. Felis1,*,‡
1Department of Biotechnology, University of Verona, Strada Le Grazie 15, Ca’ Vignal 2, 37134 Verona (VR), Italy,
2Department of Food Biotechnology and Microbiology, Institute of Food Sciences, Warsaw University of Life
Sciences, Nowoursynowska 159c St., 02-776 Warsaw, Poland and 3Department of Food Science and
Technology, Kaunas University of Technology, Radvil˙
enu˛ St. 19A, 44249 Kaunas, Lithuania
∗Corresponding author: Department of Biotechnology, University of Verona, Villa Lebrecht, Via della Pieve 70, 37029 San Pietro in C. (VR), Italy. Tel:
+39-045-6835627; E-mail: giovanna.felis@univr.it.
One sentence summary: The potential of non-conventional yeast biodiversity can be increasingly exploited in the food industry through a systematic
bioprospecting at genus-level towards a sustainable innovation.
†The two authors equally contributed to this work
Editor: Cecilia Geijer
‡Giovanna E. Felis, https://orcid.org/0000-0002-6506- 6911
ABSTRACT
Yeast species have been spontaneously participating in food production for millennia, but the scope of applications was
greatly expanded since their key role in beer and wine fermentations was clearly acknowledged. The workhorse for
industry and scientic research has always been Saccharomyces cerevisiae. It occupies the largest share of the dynamic yeast
market, that could further increase thanks to the better exploitation of other yeast species.
Food-related ‘non-conventional’ yeasts (NCY) represent a treasure trove for bioprospecting, with their huge untapped
potential related to a great diversity of metabolic capabilities linked to niche adaptations. They are at the crossroad of
bioprocesses and bioreneries, characterized by low biosafety risk and produce food and additives, being also able to
contribute to production of building blocks and energy recovered from the generated waste and by-products.
Considering that the usual pattern for bioprocess development focuses on single strains or species, in this review we
suggest that bioprospecting at the genus level could be very promising. Candida,Starmerella,Kluyveromyces and Lachancea
were briey reviewed as case studies, showing that a taxonomy- and genome-based rationale could open multiple
possibilities to unlock the biotechnological potential of NCY bioresources.
Keywords: bioprospecting; non-Saccharomyces; food biotechnology; bioprocess; biorenery; taxonomy
INTRODUCTION
The global yeast market was worth of USD 3.9 billion in 2020
and is expected to reach USD 6.1 billion by 2025, showing
a compound annual growth rate of 9.6% during this period
(MarketsandMarketsTM 2020). The food industry is responsible
for the largest share of this fast-developing market and the well-
known ‘conventional’ yeast Saccharomyces cerevisiae remains
for sure the most exploited species. This historical workhorse
secured its leading position in the industry thanks mainly to the
Received: 30 July 2021; Accepted: 27 September 2021
C
The Author(s) 2021. Published by Oxford University Press on behalf of FEMS. All rights reserved. For permissions, please e-mail:
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2FEMS Yeast Research, 2021, Vol. 21, No. 7
ability to withstand multiple stressful conditions in conversion
processes, especially ethanol, osmotic and oxidative stresses,
while showing very efcient fermentation performance. Other
‘non-Saccharomyces’ yeasts species have gained increasing atten-
tion from scientic researchers, industry leaders and consumers
alike. The term ‘non-conventional yeasts’ (NCY) is getting used,
as some authors include Schizosaccharomyces pombe among the
‘conventional’ yeasts, but the boundaries between conventional
and NCY become fuzzier, as the latter gain more importance and
the distinction between traditional and non-traditional appli-
cations is also becoming blurred (Sibirny and Scheffers 2002;
Kręgiel, Pawlikowska and Antolak 2017).
NCY include several species already well-known and
exploited, e.g. Yarrowia lipolytica,Pichia kudriavzevii,Debary-
omyces hansenii,Candida utilis (now Cyberlindnera jadinii,see
below) and Kluyveromyces marxianus (Navarrete and Mart´
ınez
2020). A non-exhaustive list of NCY genera is reported in
Tab le 1together with the number of papers available in PubMed
(https://pubmed.ncbi.nlm.nih.gov, accessed in May 2021)
referring to biotechnological applications.
Food-related NCY could be promising candidates for bio-
prospecting, at the crossroad of bioprocesses (related to food
or feed and ingredient productions) and bioreneries. Indeed,
yeasts are widely used in the elaboration of food and feed prod-
ucts, commonly found in the production of fermented foods
and beverages, functional foods, food additives and ingredients
(Arevalo-Villena et al. 2017; Rai, Pandey and Sahoo 2019; Tofalo
et al. 2020; Zhou, Semumu and Gamero 2021). Further, food
wastes (FWs) and agri-food by-products could be used as sub-
strates for bioconversions and production of biobased molecules
such as lactic acid and succinic acid (Pleissner et al. 2016;Liet al.
2019) and Volatile Fatty Acids (VFAs), important building blocks
for the chemical industry (Strazzera et al. 2018; Do, Theron and
Fickers 2019; Llamas et al. 2020).
Due to their use in food, some NCY species are also
included in the Qualied Presumption of Safety (QPS) list by
the European Food Safety Authority (EFSA). Besides Saccha-
romyces species (S. bayanus,S. cerevisiae,andS. pastorianus), the
QPS list by EFSA includes 17 species: Candida cylindracea,Cyber-
lindnera jadinii (anamorph C. utilis), D. hansenii (anamorph Can-
dida famata), Hanseniaspora uvarum (anamorph Kloeckera apicu-
lata), Kluyveromyces lactis (anamorph Candida spherica), K. marx-
ianus (anamorph Candida kefyr), Komagataella pastoris, Koma-
gataella phaf, Ogatae angusta, S. pombe,Wickerhamomyces anoma-
lus (anamorph Candida pelliculosa), Xanthophyllomyces dendrorhous
(anamorph Phafa rhodozyma),Y. lipolytica and Zygosaccharomyces
rouxii (EFSA 2018,2021a,b;itmustbenoticedhere,thattheterm
‘anamorph’, still used in EFSA documents, no longer has any sta-
tus (McNeill and Turland 2011) and the term ‘synonym’ should
be used instead). This could be seen as an advantage for biopro-
cesses, as safe microorganisms could contribute to the sustain-
ability of the process itself, e.g. being less risky for operators. The
QPS status granted by EFSA is comparable to the Generally Rec-
ognized as Safe (GRAS) status given by the United States Food
and Drug Administration (FDA) to safe microorganisms (Deck-
ers et al. 2020). Further, some species are reported in the Inter-
national Dairy Federation inventory of microbial food cultures
with safety demonstration in fermented food products (FIL-IDF
2018).
As for safety, genome sequencing is a powerful tool that
can reveal the presence of genes such as virulence factors
or genes conferring resistance towards antifungal drugs; this
applies to natural biodiversity (EFSA 2021c) and Genetically Mod-
ied Microorganisms (GMM; EFSA 2011). GMM can be obtained by
multiple molecular biology techniques to produce new ingredi-
ents, to improve the yield of existing processes, or to adapt an
interesting metabolism to new applications (Hanlon and Sewalt
2021).
Genome sequencing is also the most important tool to pro-
vide information on the biotechnological potential of microor-
ganisms, including NCY, and on the taxonomic placement of
strains.
The usual pattern for bioprocess development focuses on
single strains in certain species. Indeed, expertise built on the
model species is precious for biotechnology, as genetic tools,
nutrition characteristics and process parameters can be nely
tuned to improve yields and product quality at their maximum.
Indeed, different strains of the same species could be exploited
with relatively low effort, and expertise on a specic group
of microorganisms provides an efcient way to maximize the
results minimizing the efforts of designing new processes for
new products, e.g. by engineering specic strains with appropri-
ate tools.
In the last decade, we have witnessed the description of new
species in agri-food and environmental microbiology, revealing
an impressive biodiversity ecologically widespread with a pos-
sibly unprecedented biotechnological potential. In this oceanic
diversity, the existing taxonomic approach, devised to order and
name species, could be useful to highlight novel bioprospect-
ing candidates above species level. In fact, strains belong-
ing to different species, but in the same genus (if coherently
delineated), could represent a ‘compromise’ between already
available tools, which must be adapted to new strains, but a
different genomic background, which could have the poten-
tial to develop disruptive innovations. As ecology of species
also shapes physiology, and genomes contain all the infor-
mation capacity of the strains, then an updated approach,
where accurate taxonomy and genomics combine to reveal the
potential for novel metabolic pathways, could give an impor-
tant contribution to both basic research and biotechnological
innovation. Therefore, genera could be promising groups for
bioprospecting.
This review covers four genera belonging to phylum Ascomy-
cota, namely Candida,Starmerella,Kluyveromyces and Lachancea,
as case studies. In particular, Candida and Kluyveromyces include
species among the most widely used, while Starmerella and
Lachancea have been described based on the characteristics of
species formerly included in Candida and Kluyveromyces, respec-
tively. For each genus, the characteristics and applications of the
most used species are reported rst, to enlarge then the perspec-
tive to the number of species included in the respective genus,
that could be targeted in bioprospecting. Data also show that
the taxonomical reconsideration of the most numerous genera
could lead to the recognition of smaller and more homogeneous
groups that could be more easily studied, giving a new boost to
biotechnological discovery process.
Genus Candida
The genus Candida represents species for which a sexual cycle
has not been documented, spread among distinct phylogenetic
clades. The polyphyletic, multifaceted nature of Candida covers
a variety of species of diverse origins and provides little infor-
mation regarding evolutionary relationships. It should be noted
that the classication of Candida species was revised in recent
years and some of the species were transferred to other gen-
era/species based on analysis of and comparison between dif-
ferent molecular markers (Daniel, Lachance and Kurtzman 2014;
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Binati et al. 3
Tab le 1. Overview of information available for selected genera of ascomycetous non-conventional yeasts. Mycobank column records the number of valid names for the respective genus names
(genus name itself and valid species names). All other columns contain the number of papers retrieved in PubMed (https://pubmed.ncbi.nlm.nih.gov, accessed on May 2021), using the genus as
search term, alone or in combination with keywords related with the scope of the present review. Genera selected as case studies are underlined.
Genus name Mycobank
‘Genus
Name’
AND
‘Food’
AND ‘Fer-
mentation’
AND
‘Biotech-
nology’
AND
‘Collection’
AND ‘Bio-
diversity’
AND ‘Bio-
process’
AND
‘Waste’
AND ‘Sus-
tainable’
AND
‘Bioren-
ery’
AND
‘Volatile
Fatty Acids’
Saccharomyces 460 139 569 6628 9233 9624 1434 435 500 671 534 140 107
Candida 755 74 146 3084 204 3697 1176 477 233 394 182 26 33
Schizosaccharomyces 35 13 116 188 168 756 119 14 6 7 15 2 0
Pichia 225 11 036 1554 1948 2454 123 147 231 151 82 27 11
Kluyveromyces 39 2985 546 675 440 33 69 79 68 35 18 4
Yarr owi a 11 2019 411 327 485 42 29 92 113 80 22 10
Hansenula 82 1343 75 130 261 18 2 15 14240
Debaryomyces 103982375202963572729832
Zygosaccharomyces 10870340622110721231311401
Metschnikowia 7753518516965335507711
Hanseniaspora 2548627328053227135200
Torulaspora 3740723423145163638101
Brettanomyces 232961731163910722000
Meyerozyma 9206716243123198420
Starmerella 43 189 68 91 44 7 19 4 3 12 1 1
Lachancea 11180719428171513000
Non-conventional
yeasts
1093943458745451
Non-Saccharomyces
yeasts
27616522554132424100
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4FEMS Yeast Research, 2021, Vol. 21, No. 7
Kurtzman et al. 2018;Table2). However, a general reorganization
of the genus needs to be planned and achieved.
The two most well-known and studied species are C. utilis
and C. guilliermondii. However, those two names are not up-to-
date, being Cy. jadinii and Meyerozyma guilliermondii the current
ones, respectively.For this reason, description of the two species
is not included here, and relevant information can be retrieved
elsewhere (Sousa-Silva et al. 2021;Yanet al. 2021).
The genus Candida includes important pathogenic species
belonging to Candida clade/Lodderomyces clade and CTG clade
(the last lineage contains fungal species with non-standard
genetic code that switched CUG codon from leucine to ser-
ine and occurs in at least 75 Candida species), as well as non-
pathogenic yeasts in the order Saccharomycetales with emerg-
ing applications in biotechnology with prospective commercial
benets (Fitzpatrick et al. 2010;Santoset al. 2011; Krassowski
et al. 2018). The most important non-pathogenic species are indi-
cated in Table 3and are briey reviewed below. It must be noted
that, usually, at least one genome sequence is present in Gen-
Bank for industrially relevant species.
The biocatalytic and biotransformation properties and
biomass of non-pathogenic Candida yeasts are applicable in food
and feed, food additives and supplements, beverages, phar-
maceuticals and cosmetic production. Papon, Courdavault and
Clastre (2014) underlined the biotechnological potential of the
Candida species that belong to CTG clade in the era of syn-
thetic biology, thanks to an enhanced protein diversity and
expanded capacity of adaptation of these yeasts to environ-
mental conditions. Also, they may metabolize inexpensive sub-
strates and tolerate extreme stresses. The Candida species that
belong to CTG clade, like C. tropicalis,C. tenuis,C. maltosa or
Candida oleophila have an important potential in production
of different industrially valuable metabolites, such as micro-
bial protein, citric acid, xylitol or xylose reductase (Jiang et al.
2016; Golaghaiee, Ardestani and Ghorbani 2017; Hossain et al.
2018; Uthayakumar et al. 2021). The application of ‘omics’ tech-
niques and metabolic engineering may help to maximize the
biotechnological potential of these yeasts; more recently, several
approaches to genetically modify Candida yeasts using CRISPR-
mediated systems were also developed (Uthayakumar et al.
2021).
Majority of today’s food ingredients, including avor food
additives, need to be so-called natural ingredients to meet
consumers demands. Production of natural avor compounds
from agro-wastes by yeasts is current a promising aspect in
biotechnology of avors. The genus Candida includes some
strains/species with the ability to synthesize desirable avor
compounds during food fermentation processes. For example,
Candida parapsilosis CS2.53 was used among excellent aroma-
producing yeasts to enhance the avor of soy sauce during fer-
mentation of high-salt liquid-state moromi (Jiang et al. 2021). Can-
dida tropicalis was able to produce popular avorings in food
like d-limonene and methyl-butanoate growing on olive mill
waste (G ¨
unes¸er et al. 2017). However, in the last years C. trop-
icalis and C. parapsilosis were frequently recognized as impor-
tant non-Candida albicans opportunistic human pathogens that
primarily infects the immunocompromised patients (Silva et al.
2012).
Some Candida species can produce alternative, natural and
low-calorie sugar substitutes used in the food industry as sweet-
eners. Biotransformation of L-arabinose by C. parapsilosis DSM
70125 results in arabitol production, a ve-carbon sugar alcohol
sweetener. The quoted Candida strain was improved by genome
shufing technology for the efcient production of arabitol.
Obtained fusants (GSII-3 and GSII-16 strains) were more ef-
cient than the wild-type strain in arabitol synthesis (Kordowska-
Wiater, Lisiecka and Kostro 2018). Yeast bioconversion of differ-
ent fat-rich wastes, like animal fat treatment wastewaters, olive
oil mill wastewaters, soap stock of soybean oil rening, soap
stock of olive oil pomace rening, waste cooking oil, soap stock
wash-water and other, may result in microbial oils synthesis.
Some yeast species belonging to the genus Candida are known
to be oleaginous microorganisms, including C. tropicalis and C.
viswanathii. They were reported as single cell oil producers with
the fatty acid composition and degree of unsaturation varied
with the growth substrates with possible use in food and feed as
nutritional supplement (Ayadi et al. 2016; Bettencourt et al. 2020).
Waste substrates rich in VFAs may be utilized as carbon sources
during cultivation of oleaginous yeast. Cultivation of Candida sp.
on acetic acid, propionic acid and a combination of either acid
with glucose as carbon or energy sources resulted in high lipid
to biomass ratio (Kolouchov´
aet al. 2015).
Several studies are currently focused on developing novel
and effective control methods against pre- and post-harvest
decay in different agricultural commodities to avoid the use
of large amounts of fungicides. A number of microorganisms,
including Candida, showed a bioprotective effect. It was observed
that Candida sake may act against major postharvest pathogens
of apple including Botrytis cinerea and Rhizopus nigricans (Kas
et al. 2018). Thanks to the activity of proteinaceous compounds,
Candida ethanolica was recently proposed as promising biological
control against fungal growth like Aspergillus and Penicillium gen-
era during cocoa fermentation processes (Ruggirello et al. 2019).
The inhibitory effect of C. parapsilosis IP1698 on growth of dif-
ferent aatoxigenic strains of Aspergillus species and aatoxin
production was observed (Niknejad et al. 2012). The species C.
oleophila was used to control post-harvest diseases of fruits and
vegetables in the rst-generation yeast-based commercial bio-
control product (Sui et. al. 2020). The whole genome of C. oleophila
was recently sequenced, assembled and annotated by Sui et. al.
(2020) to get information about biocontrol-related genes of the
species and to understand the molecular mechanism responsi-
ble for the activity. Identication of such molecular markers may
help to select new effective biocontrol agents.
Candida intermedia and C. tropicalis are extracellular producers
of citric acid with important application in food technology (Max
et al. 2010).
Pectin-rich agro-industrial wastes, generated in high
amounts from the industrial processing of fruits and vegeta-
bles, are also sustainable for bioreneries. The main sugars
present in pectin-rich agro-industrial hydrolysates, like D-
galacturonic acid and L-arabinose, are not commonly used by
most yeasts. However, Candida succiphila or Candida sp. (YB-2248)
metabolize arabinose to ethanol (Martins et al. 2020). These
authors point out that hydrolysates of pectin-rich residues
contain acetic acid at higher concentration which may limit the
growth of many yeasts. Acetic acid is also the product of acetyl
groups hydrolysis present in hemicelluloses (Kolouchov´
aet al.
2015). Utilization of carboxylic acids, like acetate and lactate,
is known for opportunistic pathogens belonging to Candida
species. This metabolism is used to survive and successfully
thrive in unfavorable environmental conditions and nutrient-
limited conditions. The Candida glabrata drug:H+antiporter
(DHA) CgDtr1 is the only acetate exporter known in Candida
species. It is reported as involved in weak acid stress resistance
and export of acetate (Alves et al. 2020). Another toxic com-
pound present in pectin-rich hydrolysates is methanol, which
toxicity mechanisms are poorly studied. There are several NCY
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Binati et al. 5
Tab le 2. Examples of changes in the taxonomy of yeasts previously classied as Candida (Mycobank, https://www.mycobank.org/,checkedon
21st July 2021).
Species (year of effective publication) Current name (year of new taxonomy publication)
Candida auringiensis (1978) Groenewaldozyma auringiensis (2016)
Candida batistae (1999) Starmerella batistae (2018)
Candida cellulosicola (2011) Spencermartinsiella cellulosicola (2016)
Candida chrysomelidarum (2006) Metschnikowia chrysomelidarum (2018)
Candida curvata (1952) Cutaneotrichosporon curvatum (2015)
Candida etchellsii (1978) Starmerella etchellsii (2018)
Candida fructus (1978) Clavispora fructus (2018)
Candida galli (2004) Yarrowia galli (2017)
Candida gelsemii (2007) Metschnikowia gelsemii (2018)
Candida guilliermondii (Candida guilliermondii var.
guilliermondii) (1938)
Meyerozyma guilliermondii (2010)
Candida ishiwadae (1969) Nakazawaea ishiwadae (2014)
Candida kofuensis (1999) Metschnikowia kofuensis (2018)
Candida picachoensis (2004) Metschnikowia picachoensis (2018)
Candida pimensis (2004) Metschnikowia pimensis (2018)
Candida rancensis (1984) Metschnikowia rancensis (2018)
Candida shehatae (1967) Scheffersomyces shehatae (2012)
Candida stellata (1978) Starmerella stellata (2018)
Candida utilis (1952) Cyberlindnera jadinii (2009)
Candida zemplinina (2003) Starmerella bacillaris (2012)
that can efciently use methanol as the sole carbon and energy
source. The most well-known methylotrophic yeasts important
for biotechnological applications (production of single cell pro-
teins, pectinase or ethanol) are Candida boidinii,C. parapsilosis
and C. glabrata (Martins et al. 2020). The sophorolipids isolated
from C. albicans and C. glabrata cultures were suggested as pos-
sible food emulsions stabilizers with antibacterial properties
against pathogenic bacteria (Kumar Gaura et al. 2019).
Candida yeasts have great advantage in bioprocesses and
bioreneries due to robustness with a wide range of physio-
chemical tolerance and efcient growth on different inexpen-
sive carbon and nitrogen sources. They are able to utilize organic
acids, alcohols, pentose sugars, urea, ammonium salts, various
amino acids or pyrimidine and are scarcely affected by extremes
in pH. Some Candida strains may adapt to high osmotic stress
related with elevated concentrations of sugars or salt in culture
medium, which are common stresses in biotechnology. Candida
species that can grow on 60% glucose and 16% sodium chloride
have been described, including C. andamanensis,C. boleticola or C.
suratensis (Kurtzman et al. 2015). For those, no genome sequence
is available to date. Furfural is one of the typical inhibitors gener-
ated in hydrothermal treatment of lignocellulosic biomass. The
mechanism of furfural detoxication and metabolic response in
C. tropicalis, which shows intrinsic tolerance to inhibitor furfural,
was studied by Wang et al. (2016).
Remarkably, considering that the most accessible and abun-
dant renewable raw material on the world is lignocellulosic
biomass, mainly consisting of cellulose and hemicelluloses with
β(1,4)-xylan as the main component of hemicellulose, the abil-
ity of different yeasts to utilize xylose and other pentoses
released during hemicellulose hydrolysis is rather a unique fea-
ture. There already have been identied strains of the genus Can-
dida being capable of using xylose as a carbon source. They have
been mainly found in xylose-rich material and habitats, espe-
cially in wood-ingesting insects, insect frass, rotting wood, peat
collected from tropical peat swamp forest and moss, but also
water environments (Kaewwichian et al. 2019). The discussed
yeasts strains can become biocatalysts of different processes
based on xylose utilization on industrial scale or may support
genetic engineering strategies to modify other microorganisms.
The strain Candida akabanensis UFVJM-R131 ferments the hemi-
cellulosic hydrolyzate obtained by acid treatment of the sun-
ower seed cake and converts xylose into ethanol. The strain
is also capable to co-fermenting xylose and glucose, which is
a unique yeast ability. New global cellular metabolic engineer-
ing tools may allow to develop yeasts co-fermenting hexoses
and pentoses (Young, Lee and Alper 2010; Valinhas et al. 2018).
The strain C. intermedia PYCC 4715 was the rst yeast identied
with high xylose-transport capacity via glucose/xylose–H+sym-
porter. Its glucose/xylose transporter gene was used for S. cere-
visiae transformation (Leandro, Gonc¸alves and Spencer-Martins
2006). Another Candida D-xylose-fermenting yeast is Candida
kantuleensis (Nitiyon et al. 2018).
As for the genus, in Mycobank there are currently 754 legit-
imate species names ascribed to the genus Candida,butthey
include synonyms and species already reclassied. Also, many
interesting isolates are unclassied Candida. Thus, the metabolic
potential of the genus is still largely undiscovered, and its bio-
diversity maybe associated with unregistered biotechnological
advantages, but the not completely resolved taxonomy makes it
difcult to systematically access this biodiversity.
Genus Starmerella
As for Starmerella, among the biotechnologically relevant species
(Table 4), the best studied for industrial application is Starmerella
bombicola, originally isolated from bumblebee honey in Canada
and in concentrated grape juice in South Africa. The interest
toward S. bombicola is related to the industrial production of
sophorolipids, a class of biosurfactants with antimicrobial activ-
ity that are principally used in the cleaning and cosmetic indus-
tries in place of traditional agents (i.e. triclosans) which raise
environmental and medical concerns. Further, sophorolipids
can be employed for the bioremediation of soil pollution by
hydrocarbons, as anticancer agents in biomedicine, as antimi-
crobial additives in lubricants and as taste-modulating agents
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6FEMS Yeast Research, 2021, Vol. 21, No. 7
Tab le 3. List of industrially relevant Candida species, in alphabetical order (checked on July 27th, 2021); taxonomic information related to former names and type strains were retrieved from
Mycobank, https://www.mycobank.org/.
Species Former name Sequenced strain
Genome accession
numbers
Candida boidinii Candida alcomigas, Candida koshuensis,Candida methanolica,Candida methylica,Candida
olivaria,Candida ooitensis,Candida queretana, Koleckera boidini,Torulopsis enoki,Candida
silvicola var. melibiosica
JCM 9604T
NRRL Y-2332T
UNISS-Cb60
NDK27A1
Cb18
GF002
DBVPG6799
DBVPG8035
TOMC-Y47
DBVPG7578
TOMC-Y13
Y01308
BCGP00000000
NHAQ00000000
MSRY00000000
MSSE00000000
MSRX00000000
LMZO00000000
MSSB00000000
MSSD00000000
MSSA00000000
MSSC00000000
MSRZ00000000
PKKY00000000
Candida ethanolica Torulopsis ethanolitolerans var. ethanolitoleran, Torulopsis ethanolitolerans var. minor M2 ANNA00000000
Candida glabrata Cryprococcus glabratus, Torulopsis glabrata, Terulopsis stercoralis CBS 138
BG2
ATCC 2001
DSY562
DSY565
044
040
UAB047-W10D4
OL152
2B
1A
1B
3B
3A
FFUL887
FFUL887
2A
CCTCC M202019
CR380947-59
CP048230-42
CP048118-30
MVOE00000000
MVOF00000000
SKBJ00000000
SKBK00000000
NETP00000000
SKBI00000000
LLZY00000000
LLWO00000000
LMAA00000000
LMAB00000000
LMAY00000000
FMSJ00000000
FWDN00000000
LLZZ00000000
AYJS00000000
Candida intermedia Candida intermedia var. intermedia, Candida intermedia var. ethanophila, Blastodendrion
intermedius, Cryptococcus intermedius, Mycotorula intermedia
CBS 141 442
PYCC 4715
JCM 1607T
LT635756-63
LT635764-71
BCGD00000000
Candida maltosa Candida cloacae, Candida novellus, Candida subtropicallis Xu316 AOGT00000000
Candida oleophila Candida rignihuensis //
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Binati et al. 7
Tab le 3. Continued
Species Former name Sequenced strain
Genome accession
numbers
Candida parapsilosis Monilia parapsilosis, Mycocandida parapsilosis, Candida parapsilosis var. parapsilosis,
Mycotorula parapsilosis, Blastodendrion globosum, Schizoblastosporion globosum,
Blastodendrion gracile, Schizoblastosporion gracile, Brettanomyces petrophilum, Candida
osornensis, Candida montrocheri, Monilia onychophila, Mycocandida onychophila, Mycotorula
onychophila, Mycotorula vesica, Pseudomycoderma vesicum, Pseudomycoderma vesica,
Blastodendrion intestinale var. epidermicum, Castellania epidermica, Mycotorula parapsilopsis
ATCC 22019T
FDAARGOS 653
FDAARGOS 652
FDAARGOS 650
FDAARGOS 651
90–137
CBS6318
CBS1954
GA1
DE0235
USM039K
USM026
N3 182 000G1
S2 005 002R2a
JADLIH000000000
JABWAC00000000
JABWAB00000000
JABVZZ000000000
JABWAA00000000
VUYR00000000
CBZQ000000000
CBZP000000000
CBZX000000000
VTQU00000000
JADCQT000000000
JADCQS000000000
SCGV00000000
SCGQ00000000
Candida sake Eutorulopsis sake, Torulopsis sake, Candida australis, Candida salmonicola, Candida vanrijiae,
Torula lambica, Hansenula lambica, Mycotorula lambica, Candida tropicalis var. lambica,
Torulopsis austromarina, Candida austromarina, Candida vanriji
CBA6005
H14 14C
QELA00000000
JADPYB000000000
Candida succiphila Candida methanolphaga JCM 9445TBCGL00000000
Candida tenuis Yamadazyma tenuis, Mastigomyces philippovii ATCC 10573TAEIM00000000
Candida tropicalis
(type species)
Oidium tropicale, Monilia tropicalis, Atelosaccharomyces tropicalis, Castellania tropicalis,
Endomyces tropicalis, Myceloblastanon tropicale, Procandida tropicalis, Candida albicans var.
Tropicalis, Candida tropicalis var. Tropicalis, Mycotorula tropicalis, Blastodendrion irritans,
Parasaccharomyces irritans, Candida benhamii, Candida insolita, Candida paratropicalis,
Candida vulgaris, Geotrichoides vulgaris, Cryptococcus interdigitalis, Mycotorula interdigitalis,
Syringospora interdigitalis, Torulopsis interdigitalis, Cryptococcus mattletii, Endomyces
bronchialis, Candida bronchialis, Castellania bronchialis, Monilia bronchialis, Myceloblastanon
bronchiale, Endomyces burgesii, Endomyces cruzii, Zymonema cruzii, Endomyces enterica,
Endomyces insolitus, Candida insolita, Castellania insolita, Monilia insolita, Myceloblastanon
insolitum, Endomyces niveus, Candida nivea, Castellania nivea, Monilia nivea, Myceloblastanon
niveum, Endomyces paratropicalis, Atelosaccharomyces paratropicalis, Candida paratropicalis,
Castellania paratropicalis, Monilia paratropicalis, Myceloblastanon paratropicale, Mycocandida
paratropicalis, Endomyces perryi, Monilia perryi, Parendomyces perryi, Parendomyces perryii,
Monilia aegyptiaca, Castellania aegyptiaca, Monilia argentina, Mycotoruloides argentina,
Castellania burgesii, Monilia burgesii, Monilia candida, Monilia bonordenii, Myceloblastanon
candidum, Monilia candida, Monilia kefyr, Monilia metatropicalis, Castellania metatropicalis,
Monilia murmanica, Monilia pseudobronchialis, Candida pseudobronchialis, Mycotorula
dimorpha, Syringospora dimorpha, Mycotorula japonica, Mycotorula trimorpha, Mycotoruloides
trimorpha, Parasaccharomyces candidus, Parasaccharomyces taticei, Pseudomonilia miso-alpha,
Saccharomyces linguae-pilosae, Castellania linguae-pilosae, Cryptococcus linguae-pilosae,
Myceloblastanon linguae-pilosae, Torulopsis linguae-pilosae, Saccharomyces pleomorphus,
Torulopsis tonsillae, Cryptococcus tonsillae, Candida bimundalis var. Chlamydospora, Torulopsis
candida var. Nitratophila, Endomyces entericus, Candida enterica, Castellania enterica, Monilia
enterica, Myceloblastanon entericum, Mycoderma issavi, Monilia issavi, Syringospora issavi,
Geotrichum issavi, Monilia burgessi, Geotrichum vulgaris, Endomyces burgessii, Monilia
burgessii, Castellania burgessii, Candida benhamiae, Parasaccharomyces talicei
IBUN-090–03 567
MYA-3404
121
Y6604
MYA-3404
MYA-3404
MYA-3404
JAHFZN000000000
JAFIQD000000000
JGYC00000000
PKKZ00000000
CP047869-75
AAFN00000000
PQTP00000000
Candida viswanathii Procandida viswanathii, Candida citrica, Trichosporon lodderae, Candida lodderae,
Fermentotrichon lodderae, Candida viswanathii, Fermentotrichon lodderi, Trichosporon lodderi
ATCC 20 962 QLNQ00000000
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8FEMS Yeast Research, 2021, Vol. 21, No. 7
Tab le 4. List of industrially relevant Starmerella species, in alphabetical order (checked on June 18th, 2021); taxonomic information related to
former names and type strains were retrieved from Mycobank, https://www.mycobank.org/.
Species Former name Sequenced strain Genome accession numbers
Starmerella apicola Torulopsis apicola, Candida apicola NRRL Y-50 540
NRRL Y-2481
LBNK00000000
NRDU00000000
Starmerella bacillaris Candida zemplinina NPS
CBS 9494T
PYCC 3044
PAS 13
FRI751
NQLE00000000
QLKO00000000
PEOB00000000
MWPI00000000
MWSF00000000
Starmerella batistae Candida batistae //
Starmerella bombicola
(type species)
Candida bombicola JCM 9596
NRRL Y-17069T
NBRC 10 243
PYCC 5882
BCGO00000000
NRDR00000000
BBSW00000000
PEOC00000000
Starmerella oricola Candida oricola //
Starmerella kuoi Candida kuoi NRRL Y-27208TNRDS00000000
Starmerella riodocensis Candida riodocensis NRRL Y-27 859 NRDT00000000
Starmerella stellata Saccharomyces stellatus, Torulopsis
stellata, Cryptococcus stellatus,
Candida stellata
//
and emulsiers in food (van Bogaert et al. 2013; Roelants et al.
2019). Comparative genomics of S. bombicola sequences allowed
the identication of sophorolipid biosynthetic cluster genes and
their expression levels in related proteomics experiments, thus
unravelling the optimal conditions for sophorolipid production
(Gonc¸alveset al. 2020).
The rst-generation substrates for sophorolipids production
by S. bombicola mainly include hydrophobic molecules, such
as alkanes, fatty acids and fatty acid esters (Lang et al. 2000;
van Bogaert and Soetaert 2011; van Bogaert et al. 2015; Paulino
et al. 2016). Other unconventional substrates were investigated,
such as petroselinic acid, coconut oil, meadowfoam seed oil,
eicosapentaenoic and docosahexaenoic acids (van Bogaert et al.
2010;Liet al. 2013; Delbeke et al. 2016). Also, S. bombicola sub-
merged fermentations were conducted starting from animal fat,
waste cooking/frying oil, sugarcane and soy molasses, lignocel-
lulosic biomass and exotic oils (tapis, castor or jatropha oil),
while in solid state fermentations mango kernels, sunower
and safower oil cakes and winterization oil cake with sugar
beet molasses were investigated (Parekh, Patravale and Pandit
2012;Rashadet al. 2014;Jim
´
enez-Pe ˜
nalver et al. 2016; Nooman
et al. 2017). Comparable efciencies with traditional substrates
in terms of yield, titer and productivity were not reached so far,
but the selection or design of highly productive strains and their
combined application based on the use of waste or side-product
as substrate represents the most promising strategy towards
the development of a more sustainable, bio-based sophorolipids
production system (Roelants et al. 2019). In this perspective,
other Starmerella native sophorolipid producers (even though
with lower production titers and productivity compared to S.
bombicola) such as S. apicola,S. riodocensis,S. stellata,S. batistae
and S. oricola can be employed in optimized conditions (Kurtz-
mann et al. Konishi et al. 2008,2010; Konishi et al. 2017). Among
these, S. apicola produces not only sophorolipids, but also mem-
brane fatty acids, and enzymes, such as reductases and pro-
teases, which can be interesting features in the food area, par-
ticularly in winemaking (Reid et al. 2012). Further, strains of S.
kuoi, isolated from secondary peat swamp forests in Thailand
exhibited antifungal activity against Rhizoctonia solani,aricefun-
gal pathogen that causes the sheath blight disease, the second
most important rice disease in the world. The potential of this
species to be used as biological control agent needs to be further
investigated (Satianpakiranakorn, Khunnamwong and Limtong,
2020).
Within the fermented food biotechnology, Starmerella bacil-
laris (formerly Candida zemplinina) showed unique biotechno-
logical applicability as co-starter culture in the production of
fermented low-alcohol beverages with higher glycerol content
(Lemos Junior et al. 2021). The use of S.bacillaris in combination
with S. cerevisiae drives the complete fermentation of the major
sugars present in musts and releases valuable compounds, such
as mannoproteins and glutathione which confer stability and
prevent oxidative reactions, besides meeting the increasing con-
sumer demand for alcoholic beverages with reduced levels of
alcohol (Lemos Junior et al. 2021; Raymond Eder and Rosa 2021).
Strains of S. bacillaris were also explored as biocontrol agents on
grapes and apples as alternatives of synthetic fungicides thanks
to their antifungal activity towards Botrytis cinerea,Penicillium
expansum and Alternaria alternata (Lemos Junior et al. 2016; Nadai
et al. 2018; Lemos Junior et al. 2020; Lemos Junior et al. 2021;Ray-
mond Eder and Rosa 2021).
As for safety, S. bacillaris is not included in the QPS list by the
EFSA, but safety aspects related to human health were also phe-
notypically evaluated in 17 strains selected for biocontrol (Lemos
Junior et al. 2020); none of the strains raised safety concerns, con-
sidering growth at 37◦C (the temperature of the human body),
formation of pseudo hyphae (a virulence factor in human fun-
gal pathogens) and hydrolysis of the peptide bond of proteins
(responsible for the cellular lysis).
Starmerella is related to the genus Wickerhamiella and together
they form the Wickerhamiella/Starmerella (W/S) clade, which in
the Saccharomycotina species tree branches close to Y. lipolytica,
another important species for industrial applications (Gonc¸alves
et al. 2020; Raymond Eder and Rosa 2021).The genus was pro-
posed in 1998 to accommodate the teleomorph of Candida bombi-
cola, isolated from bumblebee honey (Rosa and Lachance 1998).
Since then, 43 other species were added to the genus, most of
them isolated from owers and pollinating insects: 26 species as
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Binati et al. 9
a result of reclassication, mainly from the genus Candida (San-
tos et al. 2018), while 18 were newly described. Main characteris-
tics of the species are an unusually small cell size, the absence
of laments, the formation of conjugated asci with single and
rugose ascospores released terminally from the asci and the
fermentative capacity, which could be due to the uptake of an
alcohol dehydrogenase gene of bacterial origin (Gonc¸alves et al.
2020). The strict adaptation to owers and insects is reected
in the limited nutritional versatility of Starmerella species, due
to the loss of several metabolic traits during their evolution-
ary history; however, this specialization has led to horizontal
acquisitions of functional genes encoding fructose transporters,
siderophores and thiamine salvage traits (ˇ
Cadeˇ
zet al. 2020).
Indeed, the horizontal genes acquisition is far more frequent
compared to other yeasts, for unknown reasons (De Graeve et al.
2018; Gonc¸alveset al. 2020).
So far, only 21 Starmerella genomes (size range: 9.275–11.60
Mbp) belonging to 13 species are available, with S.bacillaris
and S.bombicola the most represented with ve and four
genome sequences, respectively (Table 4). Interestingly, genome
sequencing of the four strains of S. bombicola allowed the pre-
diction of approximately 4599–4629 protein-coding genes, but
only 198 of them were described in detail (Gonc¸alves et al. 2020);
while functions related to carbohydrate polymer synthesis and
degradation, such as secretory aspartyl protease (SAP2p), exoin-
ulinases and invertases, detected in the genome of S. apicola
NRRL Y-50540 showed high sequence divergence (35% identity)
with the same proteins in other yeast species, which could be
associated to differences in terms of substrate recognition (Vega-
Alvarado et al. 2015). Further, other current questions waiting
to be answered are related to the independent evolution of dif-
ferent forms of fructophily, which is the preference for fructose
over glucose when they are both available, and the role of the
alcohol dehydrogenase-coding gene of bacterial origin in non-
fermenting species (Gonc¸alveset al. 2020).
Genus Kluyveromyces
The most widely used species of Kluyveromyces are K. lactis and
K. marxianus (Spohner et al. 2016; Karim, Gerliani and A¨
ıder 2020;
Tab le 5, including all the described species). They are often asso-
ciated with fermented dairy products, such as artisanal cheese
and ker, but can also be isolated from plants and other habi-
tats (Lane and Morrissey 2010). These two species can utilize
xylose, xylitol, cellobiose, lactose and arabinose (Nonklang et al.
2008). Kluyveromyces lactis was the rst species after S. cere-
visiae to obtain GRAS status (Bonekamp and Oosterom 1994).
Kluyveromyces marxianus has also achieved QPS status, due to its
long use in dairy products (EFSA 2013).
Kluyveromyces lactis and K. marxianus are the only lactose-
fermenting species frequently found in milk and dairy products;
they also possess weak proteolytic and lipolytic activities. The
ability to metabolize milk constituents (lactose, proteins and fat)
makes them very important in cheese ripening and fermented
milk drink (ker and kumis) production, as they contribute to
maturation and aroma formation.
Kluyveromyces marxianus is very promising to be used as a
probiotic due to the capacity of modications in the cell immu-
nity, adhesion and human gut microbiota with also antiox-
idative, anti-inammatory and hypocholesterolemic properties
(Xie et al. 2015; Cho et al. 2018); it can survive in the digestive
tract, resisting to acid and bile. The latter capacities and a higher
ability to adhere to the Caco-2 cells suggested that it might
have higher antioxidant activities (Cho et al. 2018). Yoshida et al.
(2004) investigated the hypocholesterolemicactivities of 81 yeast
strains from different species, and the highest potentiality in
hypocholesterolemic activity was observed in K. marxianus YIT
8292. Therefore, K. marxianus could be introduced as a potential
probiotic yeast and a novel food supplement with the ability to
prevent hypercholesterolemia.
Kluyveromyces marxianus and K. lactis can metabolize a vari-
ety of low-cost substrates including cheese whey or other dairy
wastes which has economic and ecological benets and makes
them the indispensable candidates for commercial industrial
applications (L ¨
oser et al. 2013; Morrissey et al. 2015). They can
produce high value-added bioingredients, such as oligosaccha-
rides, used as prebiotics to increase the growth of Bidobacterium
spp. in the human and animal intestines; oligonucleotides, usu-
ally used as enhancers of avors in food products; and oligopep-
tides, used as immuno-stimulators (Belem and Lee 1998). When
added to foods, these compounds act as immunopotentiators,
lower the low-density lipoprotein-cholesterol, risk factor for car-
diovascular diseases, promote protection against bacterial infec-
tions, enhance food avors and stabilize food emulsions (Collins
and Reid 2016).
Thermostable inulinases obtained from K. marxianus are
used for the enzymatic hydrolysis of inulin to produce fructo-
oligosaccharides and fructose syrups containing 95% fructose.
Fructo-oligosaccharides are used as prebiotic food ingredients,
whereas fructose could be an alternative sweetener to sucrose
and can increase iron absorption in children. The fructose
production through enzymatic hydrolysis of poly- and oligo-
saccharides of plant extracts by immobilized inulinases of K.
marxianus would be an efcient and advantageous approach for
commercial sugar production (Holyavka, Artyukhov and Koval-
eva 2016). Furthermore, the inulinases produced by K. marxi-
anus using xylose medium could be another promising option
to produce high concentration fructose syrup at industrial level
(Hoshida et al. 2018).
Some of the most important applications of K. lactis include
the industrial production of β-galactosidase and recombinant
chymosin. The β-galactosidase is used to produce lactose-free
dairy products and prebiotic galacto-oligosaccharides (Audic,
Chaufer and Daun 2003; Czermak et al. 2004; Guerrero et al.
2015). Recombinant bovine chymosin from K. lactis is an impor-
tant protein for cheese production and shows a higher spe-
cic activity than traditional rennet (Almeida et al. 2015). Other
commercially relevant proteins produced using K. lactis include
inulinase, phospholipase B, chitinase, xylanase and the sweet-
tasting protein brazzein (Jo, Noh and Kong 2013). Kluyveromyces
lactis is also used for the manufacture of infant nutrition prod-
ucts, single cell proteins (Magalh˜
aes et al. 2011). Several metabo-
lites are produced commercially in K. lactis including lactate, the
D-gluconic acid, which is derived from D-xylose (Toivari et al.
2012), and D-arabitol, produced directly from whey (Toyoda and
Ohtaguchi 2011).
Recently, the interest in K. marxianus and K. lactis has
increased due to their high ability to utilize low-cost substrates
and high biomass production, which could ultimately lead to
high yields of bioemulsier, which can be used as emulsiers,
solubilizers, wetting, foaming, antiadhesive and antimicrobial
agents (Karim, Gerliani and A¨
ıder 2020). It was found that the
emulsication properties of mannoprotein extracted from K.
marxianus FII 510700 cell walls were like mannoprotein obtained
from the cell walls of S. cerevisiae (Lukondeh, Ashbolt and Rogers
2003; Hajhosseini et al. 2020).
Several Kluyveromyces strains are promising candidates for
the synthesis of signicant amounts of aromatic compounds;
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10 FEMS Yeast Research, 2021, Vol. 21, No. 7
Tab le 5. List of all described species in genus Kluyveromyces, in alphabetical order (checked on July 27th, 2021); taxonomic information related to former names and type strains were retrieved from
Mycobank, https://www.mycobank.org/.
Species Former name Sequenced strain
Genome accession
numbers
Kluyveromyces aestuarii Saccharomyces aestuarii, Dekkeromyces aestuarii,Zygofabospora aestuarii NRRL YB-4510T
ATCC 18862T
PPJO00000000
AEAS00000000
Kluyveromyces
dobzhanskii
Saccharomyces dobzhanskii, Dekkeromyces dobzhanskii, Guilliermondella dobzhanskii, Zygofabospora
dobzhanskii, Kluyveromyces marxianus var. dobzhanskii, Dekkeromyces dobzhanskii
NRRL Y-1974T
CBS 2104T
PPJP00000000
CCBQ000000000
Kluyveromyces lactis Torulaspora lactis, Guilliermondella lactis, Zygofabospora lactis, Kluyveromyces lactis, Kluyveromyces
marxianus var. lactis, Dekkeromyces lactis, Saccharomyces lactis, Saccharomyces phaseolospora,
Saccharomyces sociasii, Dekkeromyces vanudenii, Kluyveromyces vanudenii, Kluyveromyces marxianus
var. vanudenii, Zygofabospora lactis var. vanudenii, Torula sphaerica, Candida sphaerica, Cryptococcus
sphaericus, Torulopsis sphaerica, Torulopsis manchurica, Zygofabospora krassilnikovii, Dekkeromyces
krassilnikovii, Zygofabospora lactis var. krassilnikovii, Zygosaccharomyces casei, Zygosaccharomyces
lactis, Zygosaccharomyces mrakii, Zygosaccharomyces versicolor, Saccharomyces drosophilarum,
Dekkeromyces drosophilarum, Guilliermondella drosophilarum, Kluyveromyces drosophilarum,
Zygofabospora drosophilarum, Kluyveromyces lactis var. drosophilarum, Kluyveromyces marxianus
var. drosophilarum, Kluyveromyces drosophilarum, Dekkeromyces drosophilarum, Zygofabospora lactis
var. drosophilarum, Saccharomyces drosophilarum var. drosophilarum, Saccharomyces drosophilarum
var. acellobiosus, Saccharomyces sociasi, Saccharomyces phaseolosporus, Kluyveromyces
phaseolosporus, Dekkeromyces phaseolosporus, Zygofabospora lactis var. phaseolospora, Cryptococcus
spaericus, Candida spherica
NRRL Y-1140
CBS 2105
GG799
NC 006037–42
CP042455-60
CP021239-44
Kluyveromyces marxianus
(type species)
Saccharomyces marxianus, Dekkeromyces marxianus, Guilliermondella marxiana, Zygofabospora
marxiana, Zygorenospora marxiana, Zygosaccharomyces marxianus, Kluyveromyces marxianus var.
marxianus, Blastodendrion procerum, Candida macedonienas, Candida mortifera, Monilia mortifera,
Mycocandida mortifera, Cryptococcus kartulisii, Castellania kartulisii, Monilia kartulisii,
Myceloblastanon kartulisii, Cryptococcus sulphureus, Monilia sulphurea, Mycoderma sulphureum,
Mycoderma sulfureum, Endomyces pseudotropicalis, Atelosaccharomyces pseudotropicalis, Castellania
pseudotropicalis, Myceloblastanon pseudotropicale, Mycotorula pseudotropicalis, Candida
pseudotropicalis, Monilia pseudotropicalis, Mycocandida pseudotropicalis, Candida pseudotropicalis
var. Pseudotropicalis, Monilia pseudotropicalis var. Pseudotropicalis, Hansenula pozolis, Kluyveromyces
cicerisporus, Dekkeromyces cicerisporus, Kluyveromyces wikenii, Dekkeromyces wikenii, Kluyveromyces
marxianus var. Wikenii, Monilia macedoniensoides, Candida macedoniensis var. macedoniensoides,
Monilia macedoniensis var. macedoniensoides, Castellania macedoniensoides, Mycotorula lactis,
Pseudomycoderma mazzae, Saccharomyces cavernicola, Saccharomyces fragrans, Saccharomyces
macedoniensis, Fabospora macedoniensis, Dekkeromyces macedoniensis, Saccharomyces muciparus,
Dekkeromyces muciparus, Torula cremoris, Torula lactosa, Mycotorula lactosa, Candida
pseudotropicalis var. lactosa, Torulopsis lactica, Zygosaccharomyces ashbyi, Monilia macedoniensis,
Mycotorula macedoniensis, Blastodendrion macedoniensis, Castellania macedoniensis, Myceloblastanon
macedoniense, Mycotoruloides macedoniensis, Candida macedoniensis, Candida macedoniensis var.
macedoniensis, Saccharomyces fragilis, Dekkeromyces fragilis, Fabospora fragilis, Guilliermondella
fragilis, Kluyveromyces fragilis, Zygorenospora fragilis, Dekkeromyces fragilis, Kluyveromyces fragilis,
Saccharomyces kefyr, Candida kefyr, Cryptococcus kefyr, Geotrichoides kefyr, Mycotorula kefyr,
Torulopsis kefyr, Candida kefyr, Monilia macedoniensis var. macedoniensis, Monilia pseudotropicalis
var. metapseudotropicalis, Mycocandida pinoyisimilis var. citelliana, Saccharomyces chevalieri var.
atypicus, Saccharomyces fragilis var. fragilis, Saccharomyces fragilis var. bulgaricus, Dekkeromyces
bulgaricus, Kluyveromyces bulgaricus, Kluyveromyces marxianus var. bulgaricus, Saccharomyces kefyr
var. kefyr, Zygosaccharomyces ashbyii, Cryptococcus sulfureus, Kluyveromyces cicerosporus, Monilia
sulfurea, Mycocandida pinoysimilis var. citelliana
FIM1
NBRC 1777
CBS 6556
NRRL Y-6860
ATCC 8635
B0399
DMB1
L03
LHW-O
IIPE453
UFS-Y2791
Olga-1
Olga-2
100656–19
DMKU3-1042
KCTC 17 555
CP015054-60
AP014599-07/
CP067326-33
CP067318-24
CP023456.1–63
JACVOB01000000
LXZY01000000
BBIL01000000
VOSP01000000
PYUN01000000
LDJA01000000
LYPD01000000
PUHV01000000
PUHT01000000
CABJCX010000000
NC 036025–32
AKFM02000000
Kluyveromyces
nonfermentans
Zygofabospora nonfermentans NRRL Y-27 343 QYLQ00000000
Kluyveromyces starmeri - UFMG-CM-Y3682TWACN00000000
Kluyveromyces
wickerhamii
Saccharomyces wickerhamii, Dekkeromyces wickerhamii, Guilliermondella wickerhamii, Kluyveromyces
wickerhamii, Zygofabospora wickerhamii, Dekkeromyces wickerhamii
UCD 54–210TAEAV00000000
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Binati et al. 11
in particular, K. marxianus possesses high potential to produce
2-phenyethanol, alcohols, furanones, fruit esters, ketones, car-
boxylic acids and aromatic hydrocarbons using, as substrate for
cultivation, different agro-industrial wastes, such as pepper and
tomato pomaces, grape and acid whey (Morrissey et al. 2015;
G¨
unes¸er et al. 2016).
Using lactose fermenting yeast could be an attractive
approach for bread production. Caballero et al. (1995) carried
out an experiment with K. marxianus strains (NRRL-Y-1109 and
NRRL-Y-2415) as baker’s yeast since this yeast shows high
growth in whey without any previous treatment. It was observed
that K. marxianus displayed a higher proong activity in the
doughs prepared with whey or lactose than the commercial
baker’s yeast strains. Furthermore, the use of K. marxianus
together with Lactobacillus delbrueckii ssp. bulgaricus or L. helveti-
cus as starter cultures to make sourdough bread could lead to
longer shelf-life and better sensory quality of the breads (Plessas
et al. 2008).
Whole wheat bread contains relatively high levels of fruc-
tans, which are the main source of oligo-, di- and mono-
saccharides and polyols (FODMAPs) in our diet. It was found that
wheat fructans were more accessible to K. marxianus inulinase
compared to S. cerevisiae invertase; and subsequently, a higher
degradation of fructans might be obtained by K. marxianus inuli-
nase (Struyf et al. 2017), which is a very important result, because
a diet low in FODMAPs could reduce the abdominals symptoms
to about 70% of the patients suffering from irritable bowel syn-
drome (Struyf et al. 2018).
Kluyveromyces marxianus and K. lactis are categorized as
Crabtree-negative and as such, do not undergo aerobic alcoholic
fermentation (Fonseca et al. 2008; Lane et al. 2011). This can be
a benecial phenotype for industrial production of those com-
pounds which are linked to biomass formation (i.e. biomass-
directed applications, protein production) since ethanol forma-
tion as a toxic or unintended by-product under aerobic condi-
tion could be avoided (Wagner and Alper 2016). Being Crabtree-
negative makes them preferable for large-scale fermentation. It
should be mentioned that there are some contradictory reports
in the literature of the ‘Crabtree status’ of K. marxianus and K.
lactis. The results of some experiments show that both species
have the genes required for ethanol production under certain
conditions. The strength of Crabtree effect can be inuenced by
extrinsic factors and varies even within species, which explains
why some, but not all, strains of K. marxianus and K. lactis are
very effective producers of ethanol (Hong et al. 2007;Mericoet al.
2009). This apparently conicting nding is probably due to the
strain variability, as most of the studies utilized only one repre-
sentative strain of each species. It can be concluded that a high
degree of intra-species disparity exists for this yeast, not only
in terms of its genetics, but also of its physiology (Lane et al.
2011).
Moving to the genus perspective, Kluyveromyces was created
by van der Walt (1956) to accommodate K. polysporus,anunusual
yeast that formed large numbers of ascospores (sometimes 50 or
more). In 1970, the genus comprised 21 species, but the analysis
of genomic sequences in 2003 led to its reorganization to only
six species: K. marxianus, K aestuarii, K. dobzhanskii, K. lactis, K.
wickerhamii and K. nonfermentans (Lachance 2007).
These six Kluyveromyces species vary widely in their ability to
metabolize lactose. Three phenotypic groups were described:
1. lactose positive K. lactis var. lactis and dairy strains of K. marx-
ianus (B haplotype);
2. lactose negative K. dobzhanskii and K. lactis var. drosophilarum,
unable to utilize this sugar at all;
3. Kluyver effect positive for lactose K. aestuarii,K. nonfermen-
tans,K. wickerhamii and non-dairy isolates of K. marxianus
(A and C haplotypes), can respire but not ferment the sugar
(Fukuhara 2006).
Recently, the novel species K. starmeri was described, which is
phylogenetically closer to K. marxianus,K. dobzhanskii and K. lac-
tis. As other cactophilic yeast species, K. starmeri is nutritionally
specialized, able to assimilate only nine of the standard carbon
sources, among which lactose is not included (Freitas et al. 2020).
Lactose positive K. marxianus and K. lactis carry two neigh-
boring genes LAC12 and LAC4 that are accountable for lactose
fermentation (Fukuhara 2006; Rodicio and Heinisch 2013). LAC12
is a membrane permease that imports lactose into the cell, and
LAC4 is an intracellular lactase (β-galactosidase) that hydroly-
ses lactose into glucose and galactose. The uptake of lactose by
LAC12 and its hydrolysis by LAC4 are sufcient to allow fermen-
tative growth of K. lactis and K. marxianus in oxygen-limiting con-
ditions (Ortiz-Merino et al. 2018). The two varieties of K. lactis,
var. lactis (domestic and milk-associated) and var. drosophilarum
(wild, insect-associated), have different LAC4 and LAC12 genetic
make-ups, not functional in the latter (Naumov et al. 2006). Also,
not all strains of K. marxianus consume lactose efciently, due
to polymorphisms in LAC12 gene. Three distinct genomic hap-
lotypes of K. marxianus (A, B and C) are known, of which only
B haplotype is dairy associated and carries a LAC12L, the LAC12
variant with efcient lactose-uptake properties among the four
LAC12 genes present in K. marxianus (Ortiz-Merino et al. 2018;
Var ela et al. 2019).
Kluyveromyces and Saccharomyces are part of the family Sac-
charomycetaceae. Kluyveromyces species are afliated with the
pre-Whole Genome Duplication (WGD) clade, while species of
Saccharomyces belong to the post-WGD. Separation of these
clades based on the presence of the WGD event explains existed
fundamental differences between them (Lane and Morrissey
2010; Lane et al. 2011).
Genus Lachancea
Strains of Lachancea thermotolerans, previously Kluyveromyces ther-
motolerans, are by far the most studied among the Lachancea
species (Table 6), thanks to a signicant technological poten-
tial: they were among the rst non-conventional yeasts to
became commercially available as starter cultures for winemak-
ing (Kurtzman 2003; Porter, Divol and Setati 2019b). The ability
to produce lactic acid (Binati et al. 2020; Gatto et al. 2020), a very
uncommon metabolic activity among yeasts, can be a valuable
source for the biological acidication of wines, and other inter-
esting features from the oenological perspective (e.g. low pro-
duction of volatile acidity, reduction of ethanol content, etc.)
were comprehensively discussed elsewhere (e.g. Benito 2020).
Recent screening efforts on the probiotic properties of NCY
have included representatives from the genus Lachancea,inpar-
ticular L. thermotolerans stood out as one of the most promising
probiotic yeasts (Agarbati et al. 2020;Fern
´
andez-Pacheco et al.
2021).
Strains of L. thermotolerans are also promising candidates for
fermentation of residues from the soybean processing chain.
During the production of soymilk and tofu there are two by-
products generated, liquid soy whey and solid soybean pulp
(okara), which are currently discarded or used as animal feed.
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12 FEMS Yeast Research, 2021, Vol. 21, No. 7
Tab le 6. List of industrially relevant Lachancea species, in alphabetical order (checked on July 27th, 2021); taxonomic information related to
former names and type strains were retrieved from Mycobank, https://www.mycobank.org/
Species Former name Sequenced strain
Genome accession
numbers
Lachancea fermentati Debaryomyces manchuricu, Zymodebaryomyces
manchuricus, Torulaspora manchurica, Saccharomyces
albasitensis, Saccharomyces amurcae, Torulaspora
amurcae, Saccharomyces astigiensis, Saccharomyces
malacitensis, Saccharomyces montanus, Torulaspora
montana, Saccharomyces nilssonii var. malacitensis,
Zymodebaryomyces mandshuricus
CBS 6772 FJUO00000000
Lachancea kluyveri Torulaspora kluyveri, Saccharomyces silvestris,
Saccharomyces smittii
NRRL Y-12651TAACE00000000
Lachancea lanzarotensis - CBS 12615TCDLU00000000
Lachancea thermotolerans
(type species)
Kluyveromyces thermotolerans, Saccharomyces
thermotolerans, Zygofabospora thermotolerans,
Saccharomyces drosophilae, Zygosaccharomyces
drosophilae, Saccharomyces veronae, Kluyveromyces
veronae
SOL13
COLC27
CBS 6340T
WVSD01000000
WVSE01000000
CU928165-71, 80
The fermentation of such substrates by different NCY could pro-
duce an alcoholic beverage or a food ingredient with more pleas-
ant avor characteristics, thanks to the positive yeast biotrans-
formation (Vong and Liu 2017; Chua, Lu and Liu 2018). Interest-
ingly, one L. thermotolerans isolated from honeybee gut in Iran
was suggested to produce sophorolipids (Mousavi, Beheshti-
Maal and Massah 2015).
Recent genotyping analysis of L. thermotolerans strains using
microsatellites showed a clear separation of strains from
anthropic and natural environments, as well as the formation
of clusters based on geographical origin, suggesting that geog-
raphy and adaptation to grape- and wine-related environments
were drivers of genetic evolution. These studies also revealed a
striking intra-specic diversity with distinct phenotypic proles
associated with the genotypic groups formed, mainly related to
important oenological traits (Banilas, Sgouros and Nisiotou 2016;
Hranilovic et al. 2017,2018).
Strains of L. thermotolerans and Lachancea fermentati were iso-
lated from traditional fermented foods in the Mediterranean
area, such as a distillate of fermented honey by-products (Gaglio
et al. 2017), and a product from the fermentation of dates
(Abekhti et al. 2021). Indeed, L. fermentati was also frequently
isolated from a wide variety of niches (Porter, Divol and Setati
2019b). The species L. thermotolerans and L. fermentati are the
most promising species in beer brewing too, thanks to the very
efcient alcoholic fermentation of sugars into high lactic acid
and low ethanol concentrations. Their use is of particular inter-
est, especially for the growing market of low-alcohol beer and
sour beer, where the biological acidication and reduced ethanol
yield are interesting features, alongside the enhancement of
aromatic complexity and organoleptic differentiation (Domizio
et al. 2016; Osburn et al. 2018; Bellut et al. 2019; Bellut, Krogerus
and Arendt 2020; Zdaniewicz et al. 2020).
Lachancea kluyveri was proposed as a model species, because
it diverged from S. cerevisiae prior to the ancestral whole-genome
duplication (WGD), and evolved through an introgression event
(Brion et al. 2015; Friedrich et al. 2015). A further advancement on
the studies with L. kluyveri was the recent integration of ‘omics’
data to reconstruct a genome-scale metabolic model, aimed to
understand the metabolism of ethyl acetate and uracil (pyrim-
idine degradation). Besides the value of L. kluyveri as a model
for genomic studies, this interesting yeast is characterized by a
weak Crabtree positive metabolism, therefore it is able to pro-
duce more biomass than other yeasts and potentially produce
valuable biomolecules under industrial conditions (Nanda et al.
2020).
Lachancea lanzarotensis and L. kluyveri are, to a lesser extent
than L. thermotolerans and L. fermentati, isolated from grape
berries/must (Gonz´
alez, Alcoba-Fl ´
orez and Laich 2013;Binati
et al. 2019; Porter, Divol and Setati 2019a). Enzymatic activities,
stress response and monoculture fermentation performance,
although to a much more limited coverage than L. thermotolerans,
were investigated, with L. kluyveri showing pectinase activity,
while L. fermentati and L. lanzarotensis positive for β-glucosidase,
but none of the tested strains have protease or esterase activ-
ity (Binati et al. 2019; Porter, Divol and Setati 2019a,2019b).
In microvinication trials, it has been shown that lactic acid
production is a strain-dependent character in L. thermotolerans,
while single strains of L. kluyveri and L. fermentati showed a com-
pletely different behavior: the former did not produce detectable
amounts of lactic acid, while the latter produced an exception-
ally high quantity (Binati 2019; Gatto et al. 2020). As for acetic
acid, again there is a considerable intraspecic variability, but
L. thermotolerans was consistently reported lower producer com-
pared to the other three Lachancea species.
Whole-genome sequencing was used to investigate differ-
ences at the strain level and link genotypes with phenotypes,
giving important insights especially in the distinctive lactic
acid metabolism associated with some representatives of the
genus Lachancea. One study dealt with L. fermentati kombucha
isolates used in beer brewing (Bellut, Krogerus and Arendt
2020) and another focused on L. thermotolerans grape isolates
promising for multistarter wine fermentations (Gatto et al.
2020).
The above-mentioned species belong to a genus proposed in
2003, after a reorganization of the family Saccharomycetaceae
based on a multigene sequence analysis, comprising former
members of Kluyveromyces,Saccharomyces and Zygosaccharomyces
(Kurtzman 2003). The initial species reclassied to the new
genus were Lachancea cidri,L. fermentati,L. kluyveri,L. thermotoler-
ans and Lachancea waltii;fromwhichL. thermotolerans was chosen
as type species. Following the description of new species in the
last two decades, including Lachancea dasiensis,Lachancea meyer-
sii,Lachancea mirantina,Lachancea nothofagi,Lachancea lanzaroten-
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Binati et al. 13
sis and Lachancea quebecensis, there are currently 11 species
assigned to the ascomycetous genus Lachancea. Most of them
are ubiquitous, including organisms isolated from soil, plants,
insects, but also fermentations of food/beverages and various
substrates in both natural and industrial processes (Friedrich
et al. 2012; Freel et al. 2015; Porter, Divol and Setati 2019b). To date,
the complete genome assemblies of 15 strains from the genus
Lachancea are available in public databases, including all legiti-
mate species, but L. cidri. Most of them show a haploid genome
containing eight chromosomes. A phylogenetic analysis of the
D1/D2 domain of the 26S rRNA gene grouped the 11 species in
four clusters (Porter, Divol and Setati 2019b), while the phyloge-
nomic tree obtained with all the available genomes of Lachancea
in the NCBI database (10 species) revealed two distinct clades,
one containing L. dasiensis,L. nothofagi,L. meyersii and L. lan-
zarotensis, and the other formed by L. mirantina,L. kluyveri,L. fer-
mentati,L. waltii,L. quebecensis and L. thermotolerans (Gatto et al.
2020). As also observed by Freel et al. (2015), the two species L.
thermotolerans and L. quebecensis are very closely related (Gatto
et al. 2020).
CONCLUDING REMARKS
A huge biodiversity exists in yeast genera which include model
species, and expertise built on model species could leverage the
exploration of new strains outside the same species, but within
the same genus, thus unlocking the biotechnological potential
of NCY bioresources.
Reliable molecular (genetic) approaches to provide a mean-
ingful classication, and genome sequencing for pre-screening
are prerequisites for the success of this approach. They
should be complemented by physiological and technologi-
cal testing and will allow effective screening and selection
of novel strains from species different from the models to
successfully exploit NCY as platform organisms to produce
biochemicals.
As a nal remark, not only Ascomycota, dened based on the
formation of asci and ascospores (Kurtzman 2014;Table1), could
be investigated, but also Basidiomycota (dened by the forma-
tion of typical basidia with basidiospores). Many of these yeasts
can utilize refractory substrates (i.e. pentoses, sugar alcohols
and components in lignocellulose); and, due to their ecology,
they produce cold-adapted enzymes and substances, such as
carotenoids and mycosporines. Further, by virtue of their strong
oxidative metabolism, some species play a central role in envi-
ronmental remediation, including radionuclide extraction from
the environment and metal absorption, and in the degrada-
tion of pollutants, aromatic compounds, chemicals, plastics and
polymers (Johnson 2013).
Coherent use of updated microbial names is advocated to
avoid jeopardized information and difcult interpretation of
results in comparison with literature. Also, availability of public
data, such as genome sequences and microbial strains deposited
in culture collections (CCs) and microbial biological resource
centres (mBRCs) could be crucial for NCY exploitation, following
what it is happening for prokaryotes (e.g. Shi et al. 2021). Indeed,
the H2020 funded project IS MIRRI21 (https://ismirri21.mirri.or
g/), focused on the implementation of the pan-European Micro-
bial Resource Infrastructure, could contribute to boost knowl-
edge and exploitation of, among others, NCY. Maintainment of
an updated database openly available for user communities,
including academia, bioindustries, and other stakeholders could
support collaborative research via the MIRRI Collaborative Work
Environment.
Funding
This publication is based upon work from COST Action CA18229
Yeast4Bio (https://yeast4bio.eu/), supported by COST (European
Cooperation in Science and Technology). This work has been
funded by the Horizon 2020 Framework Programme of the Euro-
pean Union.
Conicts of interest. None declared.
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