Evaluating Accessibility, Usability and Interoperability of Genome-Scale Metabolic Models for Diverse Yeasts Species

Total Page:16

File Type:pdf, Size:1020Kb

Evaluating Accessibility, Usability and Interoperability of Genome-Scale Metabolic Models for Diverse Yeasts Species Evaluating accessibility, usability and interoperability of genome-scale metabolic models for diverse yeasts species Downloaded from: https://research.chalmers.se, 2021-09-30 12:00 UTC Citation for the original published paper (version of record): Domenzain Del Castillo Cerecer, I., Li, F., Kerkhoven, E. et al (2021) Evaluating accessibility, usability and interoperability of genome-scale metabolic models for diverse yeasts species FEMS Yeast Research, 21(1) http://dx.doi.org/10.1093/femsyr/foab002 N.B. When citing this work, cite the original published paper. research.chalmers.se offers the possibility of retrieving research publications produced at Chalmers University of Technology. It covers all kind of research output: articles, dissertations, conference papers, reports etc. since 2004. research.chalmers.se is administrated and maintained by Chalmers Library (article starts on next page) FEMS Yeast Research, 21, 2021, foab002 doi: 10.1093/femsyr/foab002 Advance Access Publication Date: 11 January 2021 Minireview MINIREVIEW Evaluating accessibility, usability and interoperability of genome-scale metabolic models for diverse yeasts species Ivan´ Domenzain1,2,†,‡,FeiranLi1,2,†,§, Eduard J. Kerkhoven1,2 and Verena Siewers1,2,* 1Department of Biology and Biological Engineering, Chalmers University of Technology, Kemivagen¨ 10, SE-412 96, Gothenburg, Sweden and 2Novo Nordisk Foundation Center for Biosustainability, Chalmers University of Technology, Kemivagen¨ 10, SE-412 96, Gothenburg, Sweden ∗Corresponding author: Department of Biology and Biological Engineering, Chalmers University of Technology, Kemivagen¨ 10, SE-412 96 Gothenburg, Sweden. E-mail: [email protected] One sentence summary: Review on computational models of metabolism for diverse yeast species, their development history, applications and critical assessment of their accessibility, usability and interoperability. †Both authors contributed equally to this work. Editor: Jean-Marc Daran ‡Ivan´ Domenzain, http://orcid.org/0000-0002-5322-2040 §Feiran Li, http://orcid.org/0000-0001-9155-5260 ABSTRACT Metabolic network reconstructions have become an important tool for probing cellular metabolism in the field of systems biology. They are used as tools for quantitative prediction but also as scaffolds for further knowledge contextualization. The yeast Saccharomyces cerevisiae was one of the first organisms for which a genome-scale metabolic model (GEM)was reconstructed, in 2003, and since then 45 metabolic models have been developed for a wide variety of relevant yeasts species. A systematic evaluation of these models revealed that—despite this long modeling history—the sequential process of tracing model files, setting them up for basic simulation purposes and comparing them across species and even different versions, is still not a generalizable task. These findings call the yeast modeling community to comply to standard practices on model development and sharing in order to make GEMs accessible and useful for a wider public. Keywords: genome-scale metabolic models; yeast species; systems biology; accessibility; usability; interoperability INTRODUCTION capabilities of a living organism to reconstruct a complete metabolic map (Nielsen 2017). Another widely used approach Genome-scale metabolic model reconstruction has been estab- for model reconstruction consists of the use of one or multiple lished as one of the major modeling approaches for systems- well-curated networks as scaffolds, due to the high degree of level metabolic studies (Gu et al. 2019). These models are mainly conservation of metabolism for phylogenetically close species. built in a bottom-up approach, in which genome information is Metabolic models have been proven to be useful as knowledge combined with the accumulated knowledge about the metabolic databases (Herrgard˚ et al. 2008), tools for contextualization of Received: 14 September 2020; Accepted: 8 January 2021 C The Author(s) 2021. Published by Oxford University Press on behalf of FEMS. This is an Open Access article distributed under the terms of the Creative Commons Attribution-NonCommercial License (http://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact [email protected] 1 2 FEMS Yeast Research, 2021, Vol. 21, No. 1 omics data (Kerkhoven et al. 2016) and for guiding metabolic connectivity and the number of included metabolites, mak- engineering projects (Meadows et al. 2016), enabling systematic ing it a suitable model for simulation purposes (Dobson et al. explorations of the relationship between genotypes and pheno- 2010). Further updates to the consensus metabolic network have types. shown to improve predictions on gene essentiality, induced aux- The metabolic model iFF708 (Forster¨ et al. 2003)ofSaccha- otroph phenotypes and cellular growth on diverse environments romyces cerevisiae, the genome of which was the first eukaryotic (Yeast5 (Heavner et al. 2012), Yeast6 (Heavner et al. 2013)and one to be sequenced (Goffeau et al. 1996), was the first published Yeast7 (Aung, Henry and Walker 2013)). In 2019, a new ver- GEM for its entire domain in 2003. This model has been used as a sion of the consensus metabolic network, Yeast8, was published scaffold for further network refinements (Duarte, Herrgard˚ and (Lu et al. 2019), its reconstruction process combined informa- Palsson 2004; Kuepfer, Sauer and Blank 2005; Herrgard˚ et al. 2006; tion from previous GEMs, different curated databases such as Nookaew et al. 2008), which has facilitated the development of KEGG (Kanehisa et al. 2016), SGD (Hellerstedt et al. 2017), Bio- metabolic models for several other budding yeast species over Cyc (Karp et al. 2019), Reactome (Fabregat et al. 2018 )andUniProt the years, due to their well evolutionarily-conserved metabolic (The UniProt Consortium 2017) and experimental data on sub- capabilities (Shen et al. 2018). strate usage. Furthermore, Yeast8 provides an ecosystem of mul- Multiple model reconstructions exist, not just for S. cerevisiae, tilayer models suited for different kinds of phenotype predic- but for several other yeast species. These reconstructions have tions, ranging from 1011 strain-specific models to incorpora- usually been carried out by different research groups, resulting tion of enzyme constraints (ecYeast8) and protein 3D structures in specific network improvements according to their scientific (proYeast; Lu et al. 2019). interests, but at the same time yielding incompatible identifiers In parallel with the development of the consensus net- for reactions and metabolites hampering any systematic com- work, iSce926 (Chowdhury, Chowdhury and Maranas 2015)was parison and evaluation across models (Herrgard˚ et al. 2008). derived from Yeast7 (Aung, Henry and Walker 2013) in 2015, As GEMs are valuable tools for a wide variety of applications, incorporating gene essentiality and synthetic lethality informa- their end users vary from academic researchers with different tion to curate gene-reaction rules. The model iSc-AMRS-1 (Wich- backgrounds and levels of computational skills, to professionals mann et al. 2016) was developed from iLL672 (Kuepfer, Sauer and in the biotechnology and pharmaceutical industries. Therefore, Blank 2005) in 2016, mainly by curation of proton balancing for there is a strong need for computational metabolic models to be mitochondrial ATP production and reaction reversibility, aiming accessible and published in a ready-to-use format, which facili- to improve flux distribution predictions in order to investigate tates their utilization by non-expert users. Additionally, the use production of isopropenoids. of consistent and standardized identifiers for their components The model SpoMBEL1693 for Schizosaccharomyces pombe,a enables comparisons across models, thus simplifying the pro- model organism for eukaryotic cell cycle studies, was devel- cess of finding the best model for a given application. oped in 2012 using annotated genes and reactions from the KEGG database as a draft network (Sohn et al. 2012). iNX804, Latest developments on yeasts GEMs a metabolic model for Candida glabrata, known as a platform organism for pyruvate production, was reconstructed in 2013 The development, interconnections and applications of and used for identification of gene targets for enhanced pro- metabolic models for different yeast species have been reviewed duction of pyruvate-derived fine chemicals (Xu et al. 2013). The extensively (Sanchez´ and Nielsen 2015; Lopes and Rocha 2017; metabolism of Candida tropicalis, known as a promising host for Castillo, Patil and Jouhten 2019; Chen, Li and Nielsen 2019)how- α, ω-dicarboxylic acids production, has been studied with the ever, the list of yeast GEM models is continuously increasing model iCT646, reconstructed through the collection of multiple both in number of GEMs and encompassed species. Here we database information in 2016 (Mishra et al. 2016). The model briefly summarize the development history of all models for iOD907, a metabolic network for Kluyveromyces lactis, a yeast diverse yeast species that are currently available in the scientific commonly used in the dairy industry, was published in 2014 literature. The validation strategies and main applications of (Dias et al. 2014). Its reconstruction process used iMM904, for these models, as described in their original publications, are S. cerevisiae, as a scaffold
Recommended publications
  • (Vles) in the Yeast Debaryomyces Hansenii
    toxins Article New Cytoplasmic Virus-Like Elements (VLEs) in the Yeast Debaryomyces hansenii Xymena Połomska 1,* ,Cécile Neuvéglise 2, Joanna Zyzak 3, Barbara Zarowska˙ 1, Serge Casaregola 4 and Zbigniew Lazar 1 1 Department of Biotechnology and Food Microbiology, Faculty of Biotechnology and Food Science, Wrocław University of Environmental and Life Sciences (WUELS), 50-375 Wroclaw, Poland; [email protected] (B.Z.);˙ [email protected] (Z.L.) 2 SPO, INRAE, Montpellier SupAgro, Université de Montpellier, 34060 Montpellier, France; [email protected] 3 Department of Microbiology, Laboratory of Microbiome Immunobiology, Ludwik Hirszfeld Institute of Immunology and Experimental Therapy, Polish Academy of Sciences, 53-114 Wroclaw, Poland; [email protected] 4 INRAE, AgroParisTech, Micalis Institute, CIRM-Levures, Université Paris-Saclay, 78350 Jouy-en-Josas, France; [email protected] * Correspondence: [email protected]; Tel.: +48-71-3207-791 Abstract: Yeasts can have additional genetic information in the form of cytoplasmic linear dsDNA molecules called virus-like elements (VLEs). Some of them encode killer toxins. The aim of this work was to investigate the prevalence of such elements in D. hansenii killer yeast deposited in culture collections as well as in strains freshly isolated from blue cheeses. Possible benefits to the host from harboring such VLEs were analyzed. VLEs occurred frequently among fresh D. hansenii isolates (15/60 strains), as opposed to strains obtained from culture collections (0/75 strains). Eight new different systems were identified: four composed of two elements and four of three elements. Full sequences of three new VLE systems obtained by NGS revealed extremely high conservation Citation: Połomska, X.; Neuvéglise, among the largest molecules in these systems except for one ORF, probably encoding a protein C.; Zyzak, J.; Zarowska,˙ B.; resembling immunity determinant to killer toxins of VLE origin in other yeast species.
    [Show full text]
  • The Classification of Orphans Is Improved by Combining Searches in Both Proteomes and Genomes
    bioRxiv preprint doi: https://doi.org/10.1101/185983; this version posted May 19, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY 4.0 International license. The classification of orphans is improved by combining searches in both proteomes and genomes. Walter Basile1,2, Marco Salvatore1,2, Arne Elofsson1,2,3,*, 1 Science for Life Laboratory, Stockholm University SE-171 21 Solna, Sweden 2 Department of Biochemistry and Biophysics, Stockholm University, SE-106 91 Stockholm, Sweden 3 Swedish e-Science Research Center (SeRC) * Corresponding author: [email protected] Abstract The identification of de novo created genes is important as it provides a glimpse on the evolutionary processes of gene creation. Potential de novo created genes are identified by selecting genes that have no homologs outside a particular species, but for an accurate detection this identification needs to be correct. Genes without any homologs are often referred to as orphans; in addition to de novo created ones, fast evolving genes or genes lost in all related genomes might also be classified as orphans. The identification of orphans is dependent on: (i) a method to detect homologs and (ii) a database including genes from related genomes. Here, we set out to investigate how the detection of orphans is influenced by these two factors. Using Saccharomyces cerevisiae we identify that best strategy is to use a combination of searching annotated proteins and a six-frame translation of all ORFs from closely related genomes.
    [Show full text]
  • Comparative Genomics of Protoploid Saccharomycetaceae
    Downloaded from genome.cshlp.org on October 5, 2021 - Published by Cold Spring Harbor Laboratory Press Evolution of protoploid yeast genomes ___________________________________________________________________________ Comparative genomics of protoploid Saccharomycetaceae. The Génolevures Consortium (1) Running title: Evolution of protoploid yeast genomes Key words: protein families, synteny, tandems, annotation, SONS, ancestor genome Corresponding author: Jean Luc Souciet Université de Strasbourg, CNRS, UMR 7156 Institut de Botanique, 28 rue Goethe, F-67000 Strasbourg, France Tel: 33 3 90 24 18 17 FAX: 33 3 90 24 20 28 e-mail: [email protected] (1) List of participants and affiliations appear at the end of the paper 1 Downloaded from genome.cshlp.org on October 5, 2021 - Published by Cold Spring Harbor Laboratory Press Evolution of protoploid yeast genomes ___________________________________________________________________________ Abstract Our knowledge on yeast genomes remains largely dominated by the extensive studies on Saccharomyces cerevisiae and the consequences of its ancestral duplication, leaving the evolution of the entire class of hemiascomycetes only partly explored. We concentrate here on five species of Saccharomycetaceae, a large subdivision of hemiascomycetes, that we call “protoploid” because they diverged from the S. cerevisiae lineage prior to its genome duplication. We determined the complete genome sequences of three of these species, Kluyveromyces (Lachancea) thermotolerans and Saccharomyces (Lachancea) kluyveri (two members of the newly described Lachancea clade) and Zygosaccharomyces rouxii. We included in our comparisons the previously available sequences of Klyveromyces lactis and Ashbya (Eremothecium) gossypii. Despite their broad evolutionary range and significant individual variations in each lineage, the five protoploid Saccharomycetaceae share a core repertoire of ca.
    [Show full text]
  • Global Expression Analysis of the Yeast Lachancea
    Washington University School of Medicine Digital Commons@Becker Open Access Publications 11-2013 Global expression analysis of the yeast Lachancea (saccharomyces) kluyveri reveals new URC genes involved in pyrimidine catabolism Anna Andersson Rasmussen Lund University Dineshkumar Kandasamy Lund University Halfdan Beck Lund University Seth D. Crosby Washington University School of Medicine in St. Louis Olof Bjornberg Lund University See next page for additional authors Follow this and additional works at: https://digitalcommons.wustl.edu/open_access_pubs Recommended Citation Rasmussen, Anna Andersson; Kandasamy, Dineshkumar; Beck, Halfdan; Crosby, Seth D.; Bjornberg, Olof; Schnackerz, Klaus D.; and Piskur, Jure, ,"Global expression analysis of the yeast Lachancea (saccharomyces) kluyveri reveals new URC genes involved in pyrimidine catabolism." Eukaryotic Cell.13,1. 31-42. (2013). https://digitalcommons.wustl.edu/open_access_pubs/2116 This Open Access Publication is brought to you for free and open access by Digital Commons@Becker. It has been accepted for inclusion in Open Access Publications by an authorized administrator of Digital Commons@Becker. For more information, please contact [email protected]. Authors Anna Andersson Rasmussen, Dineshkumar Kandasamy, Halfdan Beck, Seth D. Crosby, Olof Bjornberg, Klaus D. Schnackerz, and Jure Piskur This open access publication is available at Digital Commons@Becker: https://digitalcommons.wustl.edu/open_access_pubs/2116 Global Expression Analysis of the Yeast Lachancea (Saccharomyces) kluyveri Reveals New URC Genes Involved in Pyrimidine Catabolism Anna Andersson Rasmussen, Dineshkumar Kandasamy, Downloaded from Halfdan Beck, Seth D. Crosby, Olof Björnberg, Klaus D. Schnackerz and Jure Piskur Eukaryotic Cell 2014, 13(1):31. DOI: 10.1128/EC.00202-13. Published Ahead of Print 1 November 2013. http://ec.asm.org/ Updated information and services can be found at: http://ec.asm.org/content/13/1/31 These include: SUPPLEMENTAL MATERIAL Supplemental material on January 28, 2014 by Washington University in St.
    [Show full text]
  • Conservation of Mrna Quality Control Factor Ski7 and Its Diversification Through Changes in Alternative Splicing and Gene Duplication
    Conservation of mRNA quality control factor Ski7 and its diversification through changes in alternative splicing and gene duplication Alexandra N. Marshalla, Jaeil Hana, Minseon Kima, and Ambro van Hoofa,1 aDepartment of Microbiology and Molecular Genetics, University of Texas Health Science Center at Houston and University of Texas Graduate School of Biomedical Sciences, Houston, TX 77030 Edited by Lynne E. Maquat, University of Rochester School of Medicine and Dentistry, Rochester, NY, and approved May 7, 2018 (received for review February 2, 2018) Eukaryotes maintain fidelity of gene expression by preferential Ski7 function was initially thought to have arisen after the du- degradation of aberrant mRNAs that arise by errors in RNA plication, we have previously shown that the single Lachancea processing reactions. In Saccharomyces cerevisiae, Ski7 plays an kluyveri ortholog can carry out both Ski7 and Hbs1 functions and important role in this mRNA quality control by mediating mRNA thus, that Ski7 function was already present before whole ge- degradation by the RNA exosome. Ski7 was initially thought to be nome duplication (8, 10, 11). In addition, we have shown that the restricted to Saccharomyces cerevisiae and close relatives because L. kluyveri gene encodes two different proteins through alter- the SKI7 gene and its paralog HBS1 arose by whole genome du- native splicing with a shorter splice isoform performing the plication (WGD) in a recent ancestor. We have recently shown that function of HBS1 and a longer splice isoform performing the the preduplication gene was alternatively spliced and that Ski7 function of SKI7 (10). Furthermore, based on sequence analysis of function predates WGD.
    [Show full text]
  • Searching for Telomerase Rnas in Saccharomycetes
    bioRxiv preprint doi: https://doi.org/10.1101/323675; this version posted May 16, 2018. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. Article TERribly Difficult: Searching for Telomerase RNAs in Saccharomycetes Maria Waldl 1,†, Bernhard C. Thiel 1,†, Roman Ochsenreiter 1, Alexander Holzenleiter 2,3, João Victor de Araujo Oliveira 4, Maria Emília M. T. Walter 4, Michael T. Wolfinger 1,5* ID , Peter F. Stadler 6,7,1,8* ID 1 Institute for Theoretical Chemistry, University of Vienna, Währingerstraße 17, A-1090 Wien, Austria; {maria,thiel,romanoch}@tbi.univie.ac.at, michael.wolfi[email protected] 2 BioInformatics Group, Fakultät CB Hochschule Mittweida, Technikumplatz 17, D-09648 Mittweida, Germany; [email protected] 3 Bioinformatics Group, Department of Computer Science, and Interdisciplinary Center for Bioinformatics, University of Leipzig, Härtelstraße 16-18, D-04107 Leipzig, Germany 4 Departamento de Ciência da Computação, Instituto de Ciências Exatas, Universidade de Brasília; [email protected], [email protected] 5 Center for Anatomy and Cell Biology, Medical University of Vienna, Währingerstraße 13, 1090 Vienna, Austria 6 German Centre for Integrative Biodiversity Research (iDiv) Halle-Jena-Leipzig, Competence Center for Scalable Data Services and Solutions, and Leipzig Research Center for Civilization Diseases, University Leipzig, Germany 7 Max Planck Institute for Mathematics in the Sciences, Inselstraße 22, D-04103 Leipzig, Germany 8 Santa Fe Institute, 1399 Hyde Park Rd., Santa Fe, NM 87501 * Correspondence: MTW michael.wolfi[email protected]; PFS [email protected] † These authors contributed equally to this work.
    [Show full text]
  • The Genetics of Non-Conventional Wine Yeasts: Current Knowledge and Future Challenges
    MINI REVIEW published: 11 January 2016 doi: 10.3389/fmicb.2015.01563 The Genetics of Non-conventional Wine Yeasts: Current Knowledge and Future Challenges Isabelle Masneuf-Pomarede 1, 2, Marina Bely 1, Philippe Marullo 1, 3 and Warren Albertin 1, 4* 1 ISVV, Unité de Recherche Œnologie EA 4577, USC 1366 Institut National de la Recherche Agronomique, Bordeaux INP, University Bordeaux, Villenave d’Ornon, France, 2 Bordeaux Sciences Agro, Gradignan, France, 3 Biolaffort, Bordeaux, France, 4 ENSCBP, Bordeaux INP, Pessac, France Saccharomyces cerevisiae is by far the most widely used yeast in oenology. However, during the last decade, several other yeasts species has been purposed for winemaking as they could positively impact wine quality. Some of these non-conventional yeasts (Torulaspora delbrueckii, Metschnikowia pulcherrima, Pichia kluyveri, Lachancea thermotolerans, etc.) are now proposed as starters culture for winemakers in mixed fermentation with S. cerevisiae, and several others are the subject of various studies (Hanseniaspora uvarum, Starmerella bacillaris, etc.). Along with their biotechnological use, the knowledge of these non-conventional yeasts greatly increased these last 10 years. The aim of this review is to describe the last updates and the current state-of-art of Edited by: the genetics of non-conventional yeasts (including S. uvarum, T. delbrueckii, S. bacillaris, Gemma Beltran, Universitat Rovira i Virgili, Spain etc.). We describe how genomics and genetics tools provide new data into the population Reviewed by: structure and biodiversity of non-conventional yeasts in winemaking environments. Aspasia Nisiotou, Future challenges will lie on the development of selection programs and/or genetic Technological Educational Institute of improvement of these non-conventional species.
    [Show full text]
  • Whole-Genome Sequencing and Intraspecific Analysis of the Yeast Species Lachancea Quebecensis
    Whole-genome sequencing and intraspecific analysis of the yeast species Lachancea quebecensis. Kelle C Freel, Anne Friedrich, Véronique Sarilar, Hugo Devillers, Cécile Neuvéglise, Joseph Schacherer To cite this version: Kelle C Freel, Anne Friedrich, Véronique Sarilar, Hugo Devillers, Cécile Neuvéglise, et al.. Whole- genome sequencing and intraspecific analysis of the yeast species Lachancea quebecensis.. Genome Biology and Evolution, Society for Molecular Biology and Evolution, 2016, 8 (3), pp.733-741. 10.1093/gbe/evv262. hal-02635461 HAL Id: hal-02635461 https://hal.inrae.fr/hal-02635461 Submitted on 27 May 2020 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Genome Biology and Evolution Advance Access published January 5, 2016 doi:10.1093/gbe/evv262 Whole-genome sequencing and intraspecific analysis of the yeast species Lachancea quebecensis Downloaded from http://gbe.oxfordjournals.org/ Kelle C. Freel1†, Anne Friedrich1†, Véronique Sarilar2,3, Hugo Devillers2,3, Cécile Neuvéglise2,3 and Joseph Schacherer1* at INRA-VERS-V.G.M.bioinf on February 15, 2016 1. Department of Genetics, Genomics and Microbiology, University of Strasbourg - CNRS, UMR7156, Strasbourg, France 2. INRA, UMR1319 Micalis, Jouy-en-Josas, France 3. AgroParisTech, UMR1319 Micalis, Jouy-en-Josas, France †These authors contributed equally to this work *Author for Correspondence: Joseph Schacherer, Department of Genetics, Genomics and Microbiology, University of Strasbourg, Strasbourg, France, +33 03 68 85 19 61, [email protected] Short title: Population genomics of L.
    [Show full text]
  • D-Fructose Assimilation and Fermentation by Yeasts
    microorganisms Article 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 Rikiya Endoh *, Maiko Horiyama and Moriya Ohkuma Microbe Division/Japan Collection of Microorganisms, RIKEN BioResource Research Center (RIKEN BRC-JCM), 3-1-1 Koyadai, Tsukuba, Ibaraki 305-0074, Japan; [email protected] (M.H.); [email protected] (M.O.) * Correspondence: [email protected] Abstract: The purpose of this study was to investigate the ability of ascomycetous yeasts to as- similate/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 Citation: Endoh, R.; Horiyama, M.; yeast nitrogen base +0.5% (w/v) of D-fructose solution for assimilation and yeast extract-peptone Ohkuma, M. D-Fructose Assimilation +2% (w/v) fructose solution with an inverted Durham tube for fermentation, were used. All strains and Fermentation by Yeasts examined (n = 388, 100%) assimilated D-fructose, whereas 302 (77.8%) of them fermented D-fructose. Belonging to Saccharomycetes: D D Rediscovery of Universal Phenotypes In addition, almost all strains capable of fermenting -glucose could also ferment -fructose. These and Elucidation of Fructophilic results strongly suggest that the ability to assimilate/ferment D-fructose is a universal phenotype Behaviors in Ambrosiozyma platypodis among yeasts in the Saccharomycetes.
    [Show full text]
  • Unlocking a Signal of Introgression from Codons in Lachancea Kluyveri Using a Mutation-Selection Model Cedric Landerer1,2,3* , Brian C
    Landerer et al. BMC Evolutionary Biology (2020) 20:109 https://doi.org/10.1186/s12862-020-01649-w RESEARCH ARTICLE Open Access Unlocking a signal of introgression from codons in Lachancea kluyveri using a mutation-selection model Cedric Landerer1,2,3* , Brian C. O’Meara1,2, Russell Zaretzki2,4 and Michael A. Gilchrist1,2 Abstract Background: For decades, codon usage has been used as a measure of adaptation for translational efficiency and translation accuracy of a gene’s coding sequence. These patterns of codon usage reflect both the selective and mutational environment in which the coding sequences evolved. Over this same period, gene transfer between lineages has become widely recognized as an important biological phenomenon. Nevertheless, most studies of codon usage implicitly assume that all genes within a genome evolved under the same selective and mutational environment, an assumption violated when introgression occurs. In order to better understand the effects of introgression on codon usage patterns and vice versa, we examine the patterns of codon usage in Lachancea kluyveri, a yeast which has experienced a large introgression. We quantify the effects of mutation bias and selection for translation efficiency on the codon usage pattern of the endogenous and introgressed exogenous genes using a Bayesian mixture model, ROC SEMPPR, which is built on mechanistic assumptions about protein synthesis and grounded in population genetics. Results: We find substantial differences in codon usage between the endogenous and exogenous genes, and show that these differences can be largely attributed to differences in mutation bias favoring A/T ending codons in the endogenous genes while favoring C/G ending codons in the exogenous genes.
    [Show full text]
  • Extraordinary Diversity of Telomeres, Telomerase Rnas and Their
    www.nature.com/scientificreports OPEN Extraordinary diversity of telomeres, telomerase RNAs and their template regions in Saccharomycetaceae Vratislav Peska1*, Petr Fajkus1,3, Michal Bubeník1,3, Václav Brázda1, Natália Bohálová1,2, Vojtěch Dvořáček1, Jiří Fajkus1,3 & Sònia Garcia4* Telomerase RNA (TR) carries the template for synthesis of telomere DNA and provides a scafold for telomerase assembly. Fungal TRs are long and have been compared to higher eukaryotes, where they show considerable diversity within phylogenetically close groups. TRs of several Saccharomycetaceae were recently identifed, however, many of these remained uncharacterised in the template region. Here we show that this is mainly due to high variability in telomere sequence. We predicted the telomere sequences using Tandem Repeats Finder and then we identifed corresponding putative template regions in TR candidates. Remarkably long telomere units and the corresponding putative TRs were found in Tetrapisispora species. Notably, variable lengths of the annealing sequence of the template region (1–10 nt) were found. Consequently, species with the same telomere sequence may not harbour identical TR templates. Thus, TR sequence alone can be used to predict a template region and telomere sequence, but not to determine these exactly. A conserved feature of telomere sequences, tracts of adjacent Gs, led us to test the propensity of individual telomere sequences to form G4. The results show highly diverse values of G4-propensity, indicating the lack of ubiquitous conservation of this feature across Saccharomycetaceae. Chromosomes are capped by nucleoprotein structures called telomeres, which are involved in several important functions such as the regulation of gene expression, recombination, mitosis and meiosis1–4.
    [Show full text]
  • Mating-Type Switching by Chromosomal Inversion In
    Mating-type switching by chromosomal inversion PNAS PLUS in methylotrophic yeasts suggests an origin for the three-locus Saccharomyces cerevisiae system Sara J. Hanson, Kevin P. Byrne, and Kenneth H. Wolfe1 UCD Conway Institute, School of Medicine and Medical Science, University College Dublin, Dublin 4, Ireland Edited by Jasper Rine, University of California, Berkeley, CA, and approved October 7, 2014 (received for review August 19, 2014) Saccharomyces cerevisiae has a complex system for switching the S. cerevisiae (subphylum Saccharomycotina) and Schizosaccharomyces mating type of haploid cells, requiring the genome to have three pombe (Taphrinomycotina). A large clade of nonswitching fil- mating-type (MAT)–like loci and a mechanism for silencing two of amentous ascomycetes, the Pezizomycotina, is related more closely them. How this system originated is unknown, because the three- to S. cerevisiae than to S. pombe (Fig. 1). Despite their apparently locus system is present throughout the family Saccharomyceta- independent origins, the switching systems of S. cerevisiae (3) and ceae, whereas species in the sister Candida clade have only one S. pombe (4, 5) have many parallels, including the presence of three locus and do not switch. Here we show that yeasts in a third clade, MAT-like loci (two of which are silenced) with triplicated guide the methylotrophs, have a simpler two-locus switching system sequences, a mechanism for specifically inducing a DNA break at based on reversible inversion of a section of chromosome with MAT, donor bias (27), and cell-lineage tracking. However, the MATa genes at one end and MATalpha genes at the other end. details of switching and silencing are quite different in the two In Hansenula polymorpha the 19-kb invertible region lies beside species (3, 4).
    [Show full text]