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Ir. David Laureys

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Ir. David Laureys VRIJE UNIVERSITEIT BRUSSEL Faculteit Wetenschappen en Bio-ingenieurswetenschappen Onderzoeksgroep Industriële Microbiologie en Voedingsbiotechnologie UNIVERSITEIT GENT Faculteit Wetenschappen Laboratorium voor Microbiologie MICROBIAL SPECIES DIVERSITY, COMMUNITY DYNAMICS, SUBSTRATE CONSUMPTION, AND METABOLITE PRODUCTION DURING WATER KEFIR FERMENTATION ir. David Laureys _______________________________________________________ Proefschrift voorgedragen tot het bekomen van de graad van Doctor in de Bio-ingenieurswetenschappen en Doctor in de Wetenschappen: Biochemie en Biotechnologie. Academiejaar 2016-2017. Thesis submitted in fulfilment of the requirements for the degree of Doctor of Bioengineering Sciences and Doctor of Science: Biochemistry and Biotechnology. Academic year 2016-2017. Promotors: Prof. Dr. ir. Luc De Vuyst Prof. Dr. Peter Vandamme Published by the Research Group of Industrial Microbiology and Food Biotechnology. IMDO, Vrije Universiteit Brussel, Pleinlaan 2, B-1050 Brussels, Belgium. Apart from any fair dealing for the purposes of research or private study or criticism or review, this publication may not be reproduced, stored in a retrieval system, or transmitted, in any form or by any means, electronic, mechanical, photocopying, recording, scanning, or otherwise, without the prior permission in writing of the publisher. D. Laureys – Microbial species diversity, community dynamics, substrate consumption, and metabolite produciton during water kefir fermentation – 2017 Ph.D. thesis Vrije Universiteit Brussel, Brussels, Belgium – With summary in Dutch – 212 p. ISBN: 9789078810179 WOORD VOORAF Dit doctoraat is tot stand gekomen dankzij de hulp en steun van vele mensen die ik bij deze wil bedanken. Vooreerst wil ik mijn promotor Prof. Dr. ir. Luc De Vuyst bedanken om mij de mogelijkheid te bieden diepgaand wetenschappelijk onderzoek uit te voeren over waterkefir, een gefermenteerde drank waar ik een bijzondere interesse voor had. Ik wil hem ook bedanken voor de nauwkeurige verbetering van manuscripten, rapporten en presentaties, wat reeds resulteerde in verscheidene publicaties in gerenommeerde wetenschappelijke tijdschriften en de successvolle afwerking van dit doctoraat. Daarnaast kreeg ik ook de kans om mijn werk te presenteren op verschillende nationale en internationale congressen. Ik wil ook graag mijn copromotor Prof. Dr. Peter Vandamme bedanken om mij de mogelijkheid te bieden een nieuw Bifidobacterium species te karakteriseren en grote hoeveelheden isolaten te derepliceren via MALDI-TOF-MS. Ik wil hem ook bedanken voor zijn steun bij het afwerken van dit doctoraat. Verder wil ik Prof. Dr. ir. Frédéric Leroy bedanken om mij te helpen met de vele vragen over talloze problemen die ik ondervond tijdens mijn onderzoek. I want to thank all members of my Ph.D. jury, Prof. Dr. ir. Gert Desmet, Prof. Dr. Aurélien Carlier, Prof. Dr. Tom Coenye, Prof. Dr. Juergen Wendland, Prof. Dr. ir. Sarah Lebeer, and Prof. Dr. Matthias Ehrmann, for the critical reading of my manuscript and their questions and suggestions. Graag wil ik ir. Tom Balzarini en ing. Wim Borremans bedanken voor hun technische bijstand in het labo en voor de vele interessante discussies. Prof. Dr. Stefan Weckx wil ik bedanken voor zijn hulp met de genetische technieken en zijn hulp bij het indienen van manuscripten. Margo Cnockaert wil ik graag bedanken voor de begeleiding bij het karakteriseren van het nieuwe Bifidobacterium species en Dr. Maarten Aerts wil ik bedanken voor de begeleiding bij het derepliceren van de isolaten via MALDI-TOF-MS. Dries Reynders wil ik graag bedanken voor zijn deskundige hulp met de statistische verwerking van bepaalde experimentele resultaten. Prof. Dr. Ir. Isabelle Vandendael en Marc Raes hielpen mij bij het bestuderen van de microbiële kolonisatie van de waterkefirkorrels en Christina Makarona hielp mij bij de analyse van de waterkefirkorrelhydrolysaten via micro-X-straal fluorescentie. Ik wil eveneens Jean Dumont van het bedrijf Kaskade bedanken voor het aanleveren van de samples van het industriële waterkefirproductieproces, alsook de KMO-portefeuille die de samenwerking met Kaskade mogelijk maakte. Ook Rita en Annick wil ik van harte bedanken om allerlei administratieve zaken in goede banen te leiden, alsook voor hun morele steun. I also want to thank my thesis students Amandine Van Jean en Ana Matos for their help with my research. Last but not least, I would like to thank all collegues and ex collegues at IMDO, namely Andrea, Angeliki, Audrey, David Lantin, Deborah, Dorrit, Emiel, Florac, Gorik, Henning, Jonas, Kevin, Koen, Louise, Maria, Marija, Marko, Moens, Natalia, Rudy, Sander, Simon, Sophia, Tom G., Tom R., Vasileios, and Wim G. for the many pleasant moments and the inspiring atmosphere in the lab and the office, as well as the great times after the working hours. Tot slot wil ik mijn familie en vrienden bedanken voor hun geduld en steun tijdens het hele doctoraatsproces. Mijn vriendin Ester ben ik bijzonder dankbaar voor haar geduld en om steeds opnieuw klaar te staan met een luisterend oor en een bordje hinkelspelkaas! CONTENTS INTRODUCTION 1 CHAPTER 1: Exploring the potential of naturally fermented beverages 3 CHAPTER 2: Aims and objectives 31 CHAPTER 3: Microbial species diversity, community dynamics, substrate consumption, 33 and metabolite production during water kefir fermentation: first insights CHAPTER 4: The water kefir grain inoculum influences the water kefir grain growth, the 51 microbial species diversity, the fermentation rate, and the metabolite concentrations during water kefir fermentation CHAPTER 5: Investigation of the instability and low water kefir grain growth during an 69 industrial water kefir production process CHAPTER 6: Bifidobacterium aquikefiri sp. nov., isolated from water kefir 81 CHAPTER 7: The buffer capacity and calcium concentration of the water influence the 91 microbial species diversity, grain growth, and metabolite production during water kefir fermentation CHAPTER 8: The presence of oxygen, nutrient concentration, and nutrient source influence 109 the water kefir fermentation process CHAPTER 9: The type and concentration of the inoculum and substrate influence the grain 127 growth and fermentation rate during water kefir fermentation CHAPTER 10: Backslopping time, rinsing of the grains during backslopping, and 149 incubation temperature influence the water kefir fermentation process GENERAL DISCUSSION 169 REFERENCES 175 SUMMARY 209 SAMENVATTING 211 Introduction INTRODUCTION Many fermented beverages exist since ancient times, but only a few of them are widely available commercially. Originally, all fermented beverages were produced through a spontaneous or backslopped natural fermentation process, but nowadays most of the well- known fermented beverages are produced through a starter culture-initiated fermentation process. The latter is preferred for industrial fermentation processes, as it results in a faster process and safer and more consistent end-products. Nevertheless, many fermented beverages continue to be produced through a natural fermentation process at household level or small industrial scale. A starter culture-initiated fermentation process involves only one (or a few) microorganism(s) that is (are) deliberately added to start the fermentation, whereas spontaneous or backslopped natural fermentation processes usually involve many different microorganisms, some of which may be health-promoting. In Chapter 1, four different naturally fermented beverages, namely Belgian-style acidic ales, kombucha, milk kefir, and water kefir are described, and the metabolic and health potential of the microorganisms occurring in these fermented beverages are dealt with in detail. Natural fermentation processes are often complex and not well understood, and the tools and methods available to study these ecosystems are still evolving, remain time-consuming, and have many limitations. However, to be able to optimize a naturally fermented beverage, a thorough understanding of its fermentation process is indispensible. Water kefir is one of the naturally fermented beverages that might have the potential to be optimized as a tasty and healthy naturally fermented beverage. It is produced by an anaerobic fermentation process, which is started by adding a water kefir grain inoculum to a mixture of water, sugar, and dried figs. In this doctoral thesis, the water kefir fermentation process was investigated in detail. The aims of the experimental work are outlined in Chapter 2. In Chapter 3, the microbial species diversity, community dynamics, water kefir grain wet and dry mass, pH, and substrate consumption and metabolite production kinetics during a water kefir fermentation process were investigated to obtain a better understanding of the water kefir fermentation process. However, different water kefirs harbour different microbial species diversities and the influence of the water kefir grain inoculum on the fermentation process was investigated in Chapter 4 by comparing three fermentation processes started with different water kefir grain inocula. In Chapter 5, an industrial water kefir production process suffering from instability and low water kefir grain growth was characterized to gain more insight into the causes of these two common problems during water kefir fermentation. In several of the previous water kefir fermentation processes, a novel Bifidobacterium species was found. Therefore, in Chapter 6, a strain of this species was isolated from a water kefir fermentation
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