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Analysis of the Hybrid Genomes of Brewing Yeasts AN INVITATION A LYSIS OF THE HYBRID GENOMESLYSIS OF BREWING YE ANALYSIS OF THE To attend the defence of my PhD thesis: HYBRID GENOMES OF Analysis of the hybrid genomes of brewing yeasts on Wednesday, January 6th, 2015 at 15:00 in the Senaatzaal BREWING YEASTS of the Aula at TU Delft, Mekelweg 6, Delft Prior to the defence (14:30) there will be a presentation of the thesis for non-experts You are also invited to the reception which follows, starting 17:00, in ‘t Keldertje, A Department of Biotechnology, STS Julianalaan 67, Delft Irina Bolat [email protected] Paranymphs: Barbara Kozak [email protected] Daniel Solís Escalante [email protected] Irina Bolat Irina Bolat Irina Bolat Analysis of the hybrid genomes of brewing yeasts Proefschrift ter verkrijging van de graad van doctor aan de Technische Universiteit Delft, op gezag van de Rector Magnificus prof. ir. K.Ch.A.M. Luyben, voorzitter van het College voor Promoties, in het openbaar te verdedigen op woensdag, 6 januari 2016 om 15:00 door Irina BOLAT Dipl-Ing in Food Science and Engineering, “Dunărea de Jos” University, Galaţi, geboren te Galaţi, Romania The dissertation has been approved by the: Promotor: Prof. dr. J.T. Pronk Copromotor: Dr. ir. J-M. Daran Composition of the doctoral committee: Rector Magnificus Chairperson Prof. dr. J.T. Pronk Delft University of Technology, promotor Dr. ir. J-M. Daran Delft University of Technology, copromotor Independent members: Prof. dr. E.J. Smid Wageningen University Prof. dr. G. Walker University of Abertay Dundee Prof. dr. W.R. Hagen Delft University of Technology Dr. B. Gibson VTT Technical Research Centre, Espoo, Finland Dr. ir. J-M. Geertman Heineken Supply Chain, Zoeterwoude The research described in this thesis was performed at the Industrial Microbiology Section, Department of Biotechnology, Delft University of Technology, the Netherlands and financed by Heineken Supply Chain via the R&I platform. Cover design & layout by Alex Wesselink, Persoonlijkproefschrift.nl TABLE OF CONTENTS Samenvatting/Summary 9 Chapter 1 General introduction 19 Chapter 2 Chromosomal copy number variation in Saccharomyces 53 pastorianus is evidence for extensive genome dynamics in industrial lager brewing strains Chapter 3 amdSYM, a new dominant recyclable marker cassette for 89 Saccharomyces cerevisiae Chapter 4 Functional analysis and transcriptional regulation of 115 two orthologs of ARO10, encoding broad-substrate- specificity 2-oxo-acid decarboxylases, in the brewing yeast Saccharomyces pastorianus CBS1483 Chapter 5 Saccharomyces cerevisiae x Saccharomyces eubayanus 141 interspecific hybrid, the best of both worlds and beyond Curriculum vitae 172 List of Publications 173 Acknowledgments 175 HYMN TO NINKASI Born of the flowing water, Tenderly cared for by the Ninhursag,(…) You are the one who handles the dough [and] with a big shovel, Mixing in a pit, the bappir with sweet aromatics, Ninkasi, you are the one who handles the dough [and] with a big shovel, Mixing in a pit, the bappir with [date] - honey, You are the one who bakes the bappir in the big oven, Puts in order the piles of hulled grains, Ninkasi, you are the one who bakes the bappir in the big oven, Puts in order the piles of hulled grains, You are the one who waters the malt set on the ground, The noble dogs keep away even the potentates, Ninkasi, you are the one who waters the malt set on the ground, The noble dogs keep away even the potentates, You are the one who soaks the malt in a jar, The waves rise, the waves fall. Ninkasi, you are the one who soaks the malt in a jar, The waves rise, the waves fall. You are the one who spreads the cooked mash on large reed mats, Coolness overcomes, Ninkasi, you are the one who spreads the cooked mash on large reed mats, Coolness overcomes, You are the one who holds with both hands the great sweet wort, Brewing [it] with honey [and] wine Ninkasi, (...)(You the sweet wort to the vessel) The fermenting vat, which makes a pleasant sound, You place appropriately on a large collector vat. Ninkasi, the fermenting vat, which makes a pleasant sound, You place appropriately on a large collector vat. When you pour out the filtered beer of the collector vat, It is [like] the onrush of Tigris and Euphrates. Ninkasi, you are the one who pours out the filtered beer of the collector vat, It is [like] the onrush of Tigris and Euphrates. The oldest recipe for brewing written by Sumerians as a poem dedicated to their beer goddess Ninkasi. Written down in 1800 BC, the hymn is in fact much older. Translation by Miguel Civil. (Joshua J. Mark, 2011. The hymn to Ninkasi, goddess of beer, Ancient Encyclopedia History) SAMENVATTING SUMMARY of the PhD thesis “Analysis of the hybrid genomes of brewing yeasts” Samenvatting SAMENVATTING Eén van de best bewaarde geheimen van brouwers wordt vertegenwoordigd door de gebruikte gist in het brouwproces, vanwege de enorme impact die deze heeft op het specifieke smaakprofiel van het eindproduct. Dit vindt zijn oorsprong in de genetische aanleg van de gebruikte gist. Gebaseerd op het gedrag van de gistcellen aan het einde van de fermentatiestap in het brouwproces, kunnen er twee hoofdgroepen brouwgist worden onderscheiden: hooggistende Saccharomyces cerevisiae stammen (ale gist) en laaggistende Saccharomyces pastorianus stammen (lager gist). Deze laatste hebben een complexe genetische architectuur vanwege hun hybride genoom, bestaande uit de chromosomen van twee verschillende soorten: S. cerevisiae en S. eubayanus. De S. pastorianus giststammen zijn geclassificeerd in twee groepen, afgeleid van twee afzonderlijke hybridisaties tussen S. cerevisiae en S. eubayanus stammen: de Saaz groep is ontstaan uit de samensmelting van een haploïde S. cerevisiae met een haploïde S. eubayanus; de Frohberg groep vindt zijn oorsprong in de fusie van een diploïde S. cerevisiae met een haploïde S. eubayanus. De giststammen binnen de twee groepen hebben zowel verschillende genoomgroottes als duidelijk verschillende fysiologische eigenschappen. In dit proefschrift worden een aantal studies beschreven die uitgevoerd zijn met ondergistende (lager) giststammen, met CBS1483 uit de Frohberg groep als model. De oorsprong van lager giststammen wordt beschreven in Hoofdstuk 1. Hoewel al veel langer bekend was dat lager giststammen een hybride genoom hebben, was tot voor kort alleen het S. cerevisiae sub-genoom duidelijk geïdentificeerd. De non-cerevisiae tegenhanger is pas recent ontdekt en aangeduid als S. eubayanus. De complexiteit van het genoom van lager giststammen wordt verder vormgegeven door de brouwomstandigheden. Deze veroorzaken abnormale chromosoom kopieaantallen (aneuploïditeit), inter-chromosomale translocaties, geheel of gedeeltelijk verlies van chromosomen, chromosomale rearrangements met toenemende kopieaantallen en introgressie. Al deze veranderingen spelen een belangrijke rol in de uniekheid van ondergistende stammen. Dit wordt behandeld in Hoofdstuk 2, waar de totale genoomsequentie van zes ondergistende stammen duidelijk laat zien dat de hybride genomen van biergisten meer zijn dan alleen eenvoudige samenvoegingen van twee sub- genomen. De stam CBS1483, die gedurende dit proefschrift als studieobject werd gebruikt, is gesequenced met Illumina HiSeq2500 en 4 gepaarde libraries met verschillende insert groottes. Met deze methode kon de hoogste coverage van een lagergist genoom behaald worden (~270x) die tot nu toe gepubliceerd is. Tevens is het kopieaantal van de chromosomen in CBS1483 bepaald. Hierdoor werd het mogelijk om een genetische kaart samen te stellen, bestaande uit een totaal van 68 chromosomen en 35 verschillende chromosomale structuren. Chromosoom III vertoonde een zeer intrigerende structuur, als een uitzonderlijk chimeer chromosoom, zonder eenvoudige kopieën van één van de twee sub-genomen. De aneuploïditeit van CBS1483 werd benadrukt door de hoge variatie in kopieaantal van de 35 chromosomale structuren, uiteenlopend van 1 tot wel 5 kopieën. 10 Samenvatting Dergelijke buitengewone kopieaantallen werden bevestigd met qPCR en flow cytometrie. Al met al bleek het genoom van S. pastorianus CBS1483 te bestaan uit 56% van S. cerevisiae, 34% van S. eubayanus en 10% chimeer S. cerevisiae/S. eubayanus chromosomaal DNA, verdeeld over 68 chromosomen. Naast de identificatie van de chromosomale complexiteit werd nog een tweede bijzondere eigenschap vastgesteld in CBS1483 die zich uitte in allel variatie, waarbij kopieën van hetzelfde gen bestonden uit verschillende nucleotide sequenties. Om meer inzicht te krijgen in het genomische landschap van lager giststammen werden nog vijf Frohberg-type gisten gesequenced, resulterend in een complex beeld van de soort S. pastorianus. Niet alleen varieerde het chromosoom kopieaantal significant tussen de verschillende bestudeerde industriële lager stammen (van 49 tot 79), ook werd een duidelijke impact aangetoond op brouweigenschappen als de capaciteit om diacetyl te produceren en de flocculatie capaciteit. Aneuploïditeit in lager gistcellen geeft overlevingsvoordelen, maar het onderhoud en de expressie van complete extra chromosomen zorgt ook voor een toegenomen energiebehoefte. Dit zou een verklaring kunnen zijn voor de hoge gevoeligheid voor antibiotica die aneuploïde stammen vertonen. Gezien het feit dat dergelijke remmers onderdeel uitmaken van de genetische modificatie strategie die gebruikt wordt bij de selectie van bepaalde eigenschappen, beperkt deze gevoeligheid van lager giststammen het aantal heterologe genen dat als selectiemarker gebruikt kan worden. Tegemoetkomend
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