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Biotechnological Importance of Torulaspora Delbrueckii: from the Obscurity to the Spotlight

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Biotechnological Importance of Torulaspora Delbrueckii: from the Obscurity to the Spotlight Journal of Fungi Review Biotechnological Importance of Torulaspora delbrueckii: From the Obscurity to the Spotlight Ticiana Fernandes 1,2 , Flávia Silva-Sousa 1,2 ,Fábio Pereira 1,2, Teresa Rito 1,2 , Pedro Soares 1,2, Ricardo Franco-Duarte 1,2,* and Maria João Sousa 1,2 1 CBMA (Centre of Molecular and Environmental Biology), Department of Biology, University of Minho, 4710-057 Braga, Portugal; [email protected] (T.F.); sousa.s.fl[email protected] (F.S.-S.); [email protected] (F.P.); [email protected] (T.R.); [email protected] (P.S.); [email protected] (M.J.S.) 2 Institute of Science and Innovation for Bio-Sustainability (IB-S), University of Minho, 4710-057 Braga, Portugal * Correspondence: ricardofi[email protected] or [email protected]; Tel.: +351-253-604-310; Fax: +351-253-678-980 Abstract: Torulaspora delbrueckii has attracted interest in recent years, especially due to its biotech- nological potential, arising from its flavor- and aroma-enhancing properties when used in wine, beer or bread dough fermentation, as well as from its remarkable resistance to osmotic and freez- ing stresses. In the present review, genomic, biochemical, and phenotypic features of T. delbrueckii are described, comparing them with other species, particularly with the biotechnologically well- established yeast, Saccharomyces cerevisiae. We conclude about the aspects that make this yeast a promising biotechnological model to be exploited in a wide range of industries, particularly in wine and bakery. A phylogenetic analysis was also performed, using the core proteome of T. delbrueckii, to compare the number of homologous proteins relative to the most closely related species, under- Citation: Fernandes, T.; Silva-Sousa, standing the phylogenetic placement of this species with robust support. Lastly, the genetic tools F.; Pereira, F.; Rito, T.; Soares, P.; T. delbrueckii Franco-Duarte, R.; Sousa, M.J. available for improvement are discussed, focusing on adaptive laboratorial evolution Biotechnological Importance of and its potential. Torulaspora delbrueckii: From the Obscurity to the Spotlight. J. Fungi Keywords: Torulaspora delbrueckii; non-Saccharomyces; wine; bread; biotechnology; genomics 2021, 7, 712. https://doi.org/ 10.3390/jof7090712 Academic Editor: Jose Ramos 1. Introduction Non-Saccharomyces yeasts were described for many years as sources of spoilage and Received: 9 August 2021 contamination, and are also associated with a negative contribution to the organoleptic Accepted: 25 August 2021 profile of wines. However, in recent decades, wines produced by some non-Saccharomyces Published: 30 August 2021 yeasts revealed distinct and unique characteristics attracting the attention of many research groups [1]. Improved wines are obtained benefiting from their physiological and metabolic Publisher’s Note: MDPI stays neutral features, which have a positive effect on the wine’s sensorial and chemical properties, with regard to jurisdictional claims in namely in terms of sugar and acid consumption, alongside an enhanced aroma complexity published maps and institutional affil- through the release of important metabolites [2–4]. Within this group of yeasts, Torulaspora iations. delbrueckii stands out as one of the most advantageous non-Saccharomyces species due to its potential to introduce diversity and multiplicity to the standard wine’s market, currently established by the use of Saccharomyces cerevisiae [5]. The rising interest in T. delbrueckii is reflected by the number of scientific publications involving this species. According Copyright: © 2021 by the authors. to the Web of Science™ database, between the years 1987 and 2013, an average of eight Licensee MDPI, Basel, Switzerland. publications per year were related to the topic T. delbrueckii (search queries by title, abstracts This article is an open access article and keywords), and this number is continuously growing with a 6-fold increase between distributed under the terms and 2013 and 2021. conditions of the Creative Commons In the present review, we explored available information on the biochemical, genomic Attribution (CC BY) license (https:// creativecommons.org/licenses/by/ and phenotypic features of T. delbrueckii, with special emphasis on the aspects that make 4.0/). this yeast a promising biotechnological model to be exploited in a wide range of industries, J. Fungi 2021, 7, 712. https://doi.org/10.3390/jof7090712 https://www.mdpi.com/journal/jof J. Fungi 2021, 7, x FOR PEER REVIEW 2 of 18 In the present review, we explored available information on the biochemical, ge- nomic and phenotypic features of T. delbrueckii, with special emphasis on the aspects that make this yeast a promising biotechnological model to be exploited in a wide range of industries, but particularly in wine and bakery. Genomic, phenotypic, and metabolic char- acteristics of T. delbrueckii were scrutinized to enrich the understanding of this non-Sac- J. Fungicharomyces2021, 7, 712 yeast, comparing it with the yeast well-established in the market, S. cerevisiae2 of 18. In addition, the importance of applying genetic tools towards T. delbrueckii improvement was highlighted. but particularly in wine and bakery. Genomic, phenotypic, and metabolic characteristics of T. delbrueckii were scrutinized to enrich the understanding of this non-Saccharomyces yeast, 2. Occurrence and Generalcomparing Characteristics it with the yeast well-established in the market, S. cerevisiae. In addition, the importance of applying genetic tools towards T. delbrueckii improvement was highlighted. Yeasts from the genus Torulaspora have been reported in a wide variety of habitats, such as fruits [6], insects2. Occurrence [7,8], soils and [9], General soil invertebrates Characteristics [10], plants [11,12], seawater [13], spoiled food [6] and maltYeasts environments from the genus [6],Torulaspora where yeasthave been from reported other in genera a wide varietylike Saccharo- of habitats, such as fruits [6], insects [7,8], soils [9], soil invertebrates [10], plants [11,12], seawa- myces and Zygosaccharomycester [13], spoiled may foodalso [ 6be] and present malt environments [14,15]. Although [6], where yeastnot considered from other genera a hu- like man pathogen, the speciesSaccharomyces T. delbrueckiiand Zygosaccharomyces can also bemay found also be as present a clinical [14,15]. Althoughisolate [16]. not considered In ad- dition to the diversifieda human isolation pathogen, substrates, the species T.T. delbrueckii delbrueckii can also also bepresents found as a a clinicalworldwide isolate [geo-16]. In addition to the diversified isolation substrates, T. delbrueckii also presents a worldwide graphical distribution,geographical with reports distribution, describing with reports its isolation describing itsin isolation 37 countries in 37 countries from from the the five five continents, as shown continents,in Figure as 1 shown in Figure1 Figure 1. Geographical distribution of Torulaspora delbrueckii. Countries in which T. delbrueckii isolation was reported are Figurehighlighted 1. Geographical in blue. Data were distribution collected from of AlbertinTorulaspora et al. [6 delbrueckii], Drumonde-Neves. Countries et al. [1 in] and which de Vuyst T. etdelbrueckii al. [17]. isola- tion was reported are highlightedSpecies in belonging blue. Data to the we genusre collectedTorulaspora fromcan reproduceAlbertin et asexually al. [6], byDrumonde- cell division Neves et al. [1] and de Vuyst(budding et al. division) [17]. or sexually through asci, containing one to four spherical ascospores, characteristic of ascomycetous yeasts [4,18,19]. Regarding its shape, Torulaspora yeasts are Species belongingmainly to the discerned genus by Torulaspora spherical cells can (hence reproduce the torulu asexually terminology), by but cell also division ovoid and ellipsoidal forms, with dimensions of approximately 2–6×3–7 µm, which are smaller than (budding division) orthose sexually of S. cerevisiae through. The asci, sharing containing of multiple one morphological to four spherical and physiological ascospores, character- characteristic of ascomycetousistics between yeasts some [4,18,19]. species has Regarding led to a misclassification its shape, ofTorulaspora some of them. yeasts Within are the mainly discerned by genussphericalTorulaspora cells, four (hence strains the presumed torulu to beterminology),T. delbrueckii were but later also reclassified ovoid into and the genera Debaryomyces and Saccharomyces. Currently, this group includes at least six species: ellipsoidal forms, withT. dimensions delbrueckii (anamorph of approximatelyCandida colliculosa 2–6×3–7), T. franciscae µm,, T. which pretoriensis are, T.smaller microellipsoides than , those of S. cerevisiae. TheT. globosa sharingand T. of maleeae multiple[20]. Twomorphological other species— andT. indica physiologicaland T. quercuum character-—have also istics between some speciesbeen proposed has led to beto includeda misclassification in this genus, after of some the employment of them. of Within molecular the tools ge- to discriminate them [21]. For many years, T. delbrueckii was described as a haploid yeast, nus Torulaspora, four essentiallystrains presumed because of its to small be T. cell delbrueckii size and due were to the rarelater detection reclassified of tetrads into in sporu- the genera Debaryomyces and Saccharomyces. Currently, this group includes at least six species: T. delbrueckii (anamorph Candida colliculosa), T. franciscae, T. pretoriensis,
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