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Endophytic Bacteria Within the Green Siphonous Seaweed Bryopsis: Exploration of a Partnership

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Endophytic Bacteria Within the Green Siphonous Seaweed Bryopsis: Exploration of a Partnership Endophytic bacteria within the green siphonous seaweed Bryopsis: Exploration of a partnership Joke Hollants Promoters Prof. Dr. Anne Willems Prof. Dr. Olivier De Clerck Dissertation submitted in fulfillment of the requirements for the degree of Doctor (Ph.D.) in Sciences, Biotechnology ______________________________________________________________________________ Joke Hollants - Endophytic bacteria within the green siphonous seaweed Bryopsis: Exploration of a partnership Copyright ©2012 Joke Hollants ISBN-number: 978-94-6197-046-6 No part of this thesis protected by its copyright notice may be reproduced or utilized in any form, or by any means, electronic or mechanical, including photocopying, recording or by any information storage or retrieval system without written permission of the author and promoters. Printed by University Press | www.universitypress.be Ph.D. thesis, Faculty of Sciences, Ghent University, Ghent, Belgium. This Ph.D. work was financially supported by ‘Fonds Wetenschappelijk Onderzoek’ FWO-Flanders. Publicly defended in Ghent, Belgium, June 8th 2012 ______________________________________________________________________________ Examination committee Prof. Dr. Savvas Savvides (Chairman) L-Probe: Laboratory for protein Biochemistry and Biomolecular Engineering, Faculty of Sciences, Ghent University, Ghent, Belgium Prof. Dr. Anne Willems (Promoter) LM-UGent: Laboratory of Microbiology, Faculty of Sciences, Ghent University, Ghent, Belgium Prof. Dr. Olivier De Clerck (Co-promoter) Phycology Research Group, Faculty of Sciences, Ghent University, Ghent, Belgium Dr. Frederik Leliaert Phycology Research Group, Faculty of Sciences, Ghent University, Ghent, Belgium Prof. Dr. Paul De Vos LM-UGent: Laboratory of Microbiology, Faculty of Sciences, Ghent University, Ghent, Belgium Prof. Dr. Wim Bert Nematology Research Group, Faculty of Sciences, Ghent University, Ghent, Belgium Dr. Danny Vereecke Department of Plant production, Faculty of Applied Bioscience Engineering, University College Ghent, Ghent, Belgium Dr. Thomas Wichard Institute for Inorganic and Analytical Chemistry, Friedrich Schiller University Jena, Jena, Germany Preface “Life did not take over the globe by combat, but by networking” Lynn Margulis evolutionary biologist Life itself is contained in this one sentence. Besides Darwin's famous ‘natural selection' theory, symbiosis, the cooperation between different organisms, is necessary for the survival and evolution of species. Looking at a human being, an animal, or a plant. They all tell the same story. Everything works according the same holistic principle of interconnection and cooperation. Our body contains trillions of bacterial cells, 10 times more than human cells. Yes, you are more bacteria than human! Without bacteria you would weigh 1.2 kg less, and yet you don’t want to lose them. Bacteria digest our food and keep us healthy. Also seaweeds undertake close collaborations with external (ectosymbiotic) and internal (endosym- biotic) bacteria. Seaweeds are an unlimited source of oxygen and sugars which bacteria are happy to take advantage of. In exchange for these nutrients, bacteria produce growth promoting minerals and vitamins and they protect their host against environmental threats. As a result, many seaweed- bacterial associations are essential for both symbiotic partners. This thesis focuses on the association between the feathery-like alga Bryopsis and bacteria inside this green seaweed. It has been known for over 40 years that Bryopsis houses bacteria, but nothing was known about their identity and function. The following pages take you on an exploratory trip to the hows and whys of this exciting partnership. I hope that, while reading between the lines, I can tell you a story about the power of collaboration. Not between two, but a lot of partners. Each with their own talents and flaws. Each in their own way. “It takes two to tango, but a whole crowd to stage dive! ” Voorwoord “Life did not take over the globe by combat, but by networking” Lynn Margulis evolutiebiologe Het verhaal van het leven ligt vervat in deze ene zin. Naast Darwins gekende ‘natuurlijke selectie’-theorie, is symbiose, de samenwerking tussen verschillende organismen, nodig voor de overleving van soorten. Het is tevens de motor van hun evolutie. Bekijk een mens, bekijk een dier, bekijk een plant. Ze vertellen allen hetzelfde verhaal. Alles functioneert volgens hetzelfde holistische principe van onderlinge beïnvloeding en samenwerking. In en op ons lichaam zitten biljoenen bacteriële cellen, 10x meer dan menselijke cellen. Ja, je leest het goed, je bent meer bacterie dan mens! Zonder bacteriën zouden wij maar liefst 1,2 kg minder wegen, geen onaangename gedachte. En toch wil je ze niet kwijt. Bacteriën verteren ons voedsel en houden ons gezond. Ook zeewieren gaan hechte samenwerkingsverbanden aan met uitwendige (ectosymbiontische) en inwendige (endosymbiontische) bacteriën. Zeewieren zijn een onuitputtelijke bron van zuurstof en suikers en daar maken bacteriën maar al te graag gebruik van. In ruil voor deze voedingsstoffen maken bacteriën groeibevorderende mineralen en vitamines aan en beschermen ze hun gastheer tegen bedreigingen van buitenaf. Vele zeewier-bacterie associaties zijn dan ook van levensbelang voor beide symbiose partners. Deze thesis focust op de associatie tussen het vederwier Bryopsis en bacteriën aanwezig binnenin het wier. Het is al meer dan 40 jaar geweten dat het vederwier bacteriën huist, maar er was niets gekend omtrent hun identiteit en functie. De volgende bladzijden nemen je mee op een verkennende tocht naar het hoe en waarom van dit boeiend partnerschap. Ik hoop dat ik jou, tussen de technische hoofdstukken door, een verhaal kan vertellen over de kracht van samenwerking. Niet tussen twee, maar een heleboel partners. Elk met hun eigen talenten en gebreken. Elk op hun eigen manier. “It takes two to tango, but a whole crowd to stage dive! ” Dankwoord Tijdens mijn persoonlijke doctoraats-stage-dive heb ook ik gebruik kunnen maken van gezellige en nuttige symbioses met anderen, daarom gaat mijn dank uit naar Iedereen van het labo microbiologie en algologie, en in het bijzonder naar Mijn promotoren Anne en Olivier voor de opdracht en het vertrouwen Mijn top-begeleider Frederik voor het vele kunst- en vliegwerk en zijn eeuwig optimisme De vele studenten, vooral Helen en Lana voor de praktische hulp Olivier voor het inbed- en snijwerk en de knaagdiermoppen Myriam voor de supersnelle EM-interventies Heroen voor de staalnames, artikel-hulp en opbouwende feedback Lennert voor de staalnames en Bio-ORACLE hulp Ellen en Caroline om mij te leren extraheren en kloneren Frederique om mij te leren duiken en Bryopsis herkennen in Franse wateren Sofie, Tine, Annelien en Pieter om het koude nulde met enkele graden te verwarmen Annemie en Christelle om mij heel wat administratie-frustratie te besparen Jeanine voor de overvloed aan propere potjes en vuile praatjes Margo voor de hulp bij het zoeken naar ongewone dingen Dankwoord Het sympathieke sequentieteam: Liesbeth, Evie en Jindrich voor het kortwieken van de vele sequenties en om zich gewillig te laten omkopen Bjorn voor de hulp bij die ver-draaide excelsheets Wim voor de symbiose tussen leek & PC en hoofd & voeten Gwen en Anne voor de zotheid en om samen het DGGEspook te temmen Renata voor de eerste opvang en de blijvende vriendschap Sofie en Karolien om het drie-muskutier- én symbiose-motto "Eén voor allen, allen voor één!" alle eer aan te doen Vrienden en familie Moeke, vake en meke om mij te laten springen en indien nodig ook op te vangen Dear crowd, It was a pleasure to PhD-dive with you! Joke Table of contents Chapter 1: Literature 1 What to learn from sushi: a review on seaweed-bacterial associations 3 From kitchen secrets to sushi: a historical overview 4 Foundations 4 First cultivation and microscopy studies 6 Emergence of molecular techniques 7 Chemical interactions between seaweeds and bacteria 7 Seaweed partner 9 Bacterial partner 10 Endophytic seaweed-bacterial relationships 13 Bacterial diversity associated with seaweeds 13 Identity of bacteria associated with seaweeds: higher taxonomic ranks 14 Identity of bacteria associated with seaweeds: genus/species level 17 Linking identity to function 19 Conclusion 22 Chapter 2: Objectives 25 Chapter 3: Experimental work 29 Part 1: Optimization of the experimental design 31 3.1.1. Overview 31 Surface sterilization 31 Molecular work: full-cycle 16S rRNA gene approach 32 Cultivation work 33 Functional gene analysis 33 3.1.2. Surface sterilization of Bryopsis samples 35 Table of contents Part 2: Endophytic bacterial communities of Bryopsis cultures 47 3.2.1. Endophytic bacterial diversity within Mexican Bryopsis samples 47 3.2.2. Uniqueness, temporal stability and symbiotic nature of Bryopsis endophytic bacterial communities 67 3.2.3. Disentangling host phylogenetic, environmental and geographic signals in intracellular bacterial communities of Bryopsis 83 3.2.4. Axenic cultivation of the Bryopsis host and in vitro isolation of intracellular bacteria 105 Part 3: Endophytic bacterial communities of natural Bryopsis samples 117 3.3.1. Flavobacteriaceae endosymbionts within natural Bryopsis samples: host specificity and 117 cospeciation 3.3.2. In situ hybridizations of Bryopsis intracellular bacteria with group- and species-specific 137 fluorescent probes Chapter 4: Concluding discussion 143 Summary 155 Samenvatting 158 Bibliography 161 Curriculum vitae 175 Chapter Literature 1 Literature | 3 What to learn
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