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Molecular- and Culture- Based Approaches to Unraveling the Chemical Cross-Talk Between Delisea Pulchra and Ruegeria Strain R11

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Molecular- and Culture- Based Approaches to Unraveling the Chemical Cross-Talk Between Delisea Pulchra and Ruegeria Strain R11 Molecular- and culture- based approaches to unraveling the chemical cross-talk between Delisea pulchra and Ruegeria strain R11 Rebecca Case A thesis in fulfilment of the requirements for the degree of Doctor of Philosophy School of Biotechnology and Biomolecular Sciences Faculty of Science The University of New South Wales Sydney, Australia June, 2006 Originality Statement ‘I hereby declare that this submission is my own work and to the best of my knowledge it contains no materials previously published or written by another person, or substantial proportions of material which have been accepted for the award of any other degree or diploma at UNSW or any other educational institution, except where due acknowledgement is made in the thesis. Any contribution made to the research by others, with whom I have worked at UNSW or elsewhere, is explicitly acknowledged in the thesis. I also declare that the intellectual content of this thesis is the product of my own work, except to the extent that assistance from others in the project's design and conception or in style, presentation and linguistic expression is acknowledged.’ Signed ……………………………………………........................... 1 The [microbial] world is nature's most astonishing phenomenon. Nothing is impossible to it; the most improbable things commonly occur there. One who penetrates deeply into its mysteries is continually breathless with wonder. [They know] that anything can happen, and that the completely impossible often does. C. J. Briejèr in Rachael Carson's Silent Spring printed on recycled paper 2 Acknowledgements Tack så mycket Staffan. It’s difficult to articulate the influence you've had on my life. Your trust in science, belief in me and the freedom you've allowed me has encouraged me to think creatively and have the courage to take risks in the lab. Luckily, it paid off for us, but more importantly you are my mentor. In finishing my PhD I feel the satisfaction of completion but also the loss of leaving my mentor and friend. Ingela, the day we met has come to be one of those days in life you always remember because nothing was ever the same after that. The conversations we've had, and your hypothesis-driven approach to science, has molded my science. But more than this, you mentored me selflessly and gave me my independence. Carola, your calmness, constancy and help in moments of crisis will forever be remembered with gratitude. Thanks also to Peter for your enthusiasm and helpfulness with the Delisea part of my project. The interdisciplinary environment you and Staffan have created in the CMBB has been fantastic for my PhD. A special thanks to Ford Doolittle and his lab for taking me in. The two major discoveries that changed the focus of my PhD (quorum sensing is laterally transferred and Ruegeria was a potential pathogen) were made during this time. Thanks to Bill O'Sullivan for proof-reading my thesis. Thanks also to Adam and Evi for all the help with submission. I want to thank all the other students that have worked on Delisea pulchra with me: Sharon Longford, Dacre England, Adrian Low, and Vickey Chen. Working with people who readily discuss ideas and pull together has made this project bearable at the worst of times and a lot of fun most of the time. Laurel Crosby for the rpo chats and emails. Knowing there was another PhD student who thought we could use something other than 16S, convinced me to keep going when I thought my project would never take off. 3 Maurice, Flavia and Sacha, you guys have made my PhD. You've been through it all with me, laughter, rowr, tears and a whole lot of science talk. I'm really lucky to have found best friends at work. Thanks to the 304 girls Kirsty, Niina, Megs, Anne, Maria, Ani, Kath, Barbara, Carola, Shaz, Vickey, Sach and Flavs. And the 304 boys who put up with us, Mike, Adrian, Torsten and Brendan. Also thanks to Adam, Mary, Greg, Evi, Nids, Ana-Maria, David, Johnny and Dhana for the comradery and science chats. To my family I owe huge thanks. Especial my mum who’s done my ironing and countless other things for me while I'm writing up. Lucy who always makes us laugh and teaches me about determination. My siblings, especially Tina and Paul for their help in realizing certain goals during university. And Reshma, who listened tirelessly about my project and for making our home so friendly during the first few years of my PhD. Thanks to Ruth and Godfrey for always being interested in my progress. The weekends in the mountains have been some of the most relaxing times over the last few years. Thanks especially for your help in making the decision to do my PhD. Gina thanks for stimulating the other half of my brain and taking me out for a boogie when I needed it. Thanks especially for coming home when I needed you. Yan, you have earned my unending gratitude over the last year. Your patience in teaching me bioinformatics and help throughout the writing process with proof-reading and discussing ideas has been invaluable. bisous 4 Abstract Delisea pulchra is a red macroalga that produces furanones, a class of secondary metabolites that inhibit the growth and colonization of a range of micro- and macro- organisms. In bacteria, furanones specifically inhibit acyl homoserine lactone (AHL)- driven quorum sensing, which is known to regulate a variety of colonization and virulence traits. This thesis aims to unveil multiple aspects of the chemically mediated interactions between an alga and its bacterial flora. It was demonstrated that the quorum sensing genetic machinery of bacteria is laterally transferred, making traditional 16S rRNA gene based-diversity techniques poorly suited to identify quorum sensing species. Previous studies had shown that AHL-producing bacteria belonging to the roseobacter clade can be readily isolated from D. pulchra. Because of this, it was decided to use a roseobacter epiphytic isolate from this alga, Ruegeria strain R11, to conduct a series of colonization experiments on furanone free and furanone producing D. pulchra. Furanones were shown to inhibit Ruegeria strain R11's colonization and infection of D. pulchra. In addition, it was demonstrated that Ruegeria strain R11 has temperature-regulated virulence, similar to what is seen for the coral pathogen Vibrio shiloi. Rising ocean temperatures may explain bleached D. pulchra specimens recently observed at Bare Island, Australia. To assess whether quorum sensing is common within the roseobacter clade, cultured isolates from the Roseobacter, Ruegeria and Roseovarius genera were screened for AHL production. Half of the bacteria screened produced the quorum sensing signal molecules, AHLs. These AHLs were identified using an overlay of an AHL reporter strain in conjunction with thin layer chromatography (TLC). The prevalence of quorum sensing within the roseobacter clade, suggests that these species may occupy marine niches where cellular density is high (such as surface associated communities on substratum and marine eukaryotes). Diversity studies in marine microbial communities require appropriate molecular markers. The 16S rRNA gene is the most commonly used marker for molecular microbial ecology studies. However, it has several limitations and shortcomings, to which attention has been drawn here. The rpoB gene is an alternate ‘housekeeping’ gene used in molecular microbial ecology. Therefore, the phylogenetic properties of these two genes were compared. At most taxonomic levels the 16S rRNA and rpoB 5 genes offer similar phylogenetic resolution. However, the 16S rRNA gene is unable to resolve relationships between strains at the subspecies level. This lack of resolving power is shown here to be a consequence of intragenomic heterogeneity. 6 List of Publications In preparation Case RJ, Chen WC, Holmström C, Dahllöf I, Kjelleberg S, (2006), A comparison of the diversity detected using 16S rDNA-DGGE and rpoB-DGGE using the newly designed 'universal' rpoB primers (in preparation) Submitted Case RJ, Longford S, Crocetti G, Tujula N, Steinberg P, Kjelleberg S, (2006), Pathogens, bleaching and chemical defense in seaweeds, Science, (submitted). Case RJ, Labbate M, Kjelleberg S, (2006), Uncoupled LuxR-type proteins: Hierarchical regulation or simply eavesdropping? Environmental Microbiology, (submitted). Holmström C, Case RJ, Baille H, Thompson L, Kjelleberg S, (2006), Gram-positive bacteria cultured from the surfaces of two red algae and a phylogenetic analysis of the bacteria associated with the red alga, Biofouling, (submitted). In press Case RJ, Boucher Y, Dahllöf I, Holmström C, Doolittle WF, Kjelleberg S. (2006) Comparing the 16S rRNA and rpoB genes as molecular markers for microbial ecology, Applied and Environmental Microbiology (submitted). Published Boucher Y, Douady CJ, Papke T, Walsh DA, Boudreau MER, Nesbø CL, Case RJ, Doolittle WF, (2003), Lateral transfer and the origins of prokaryotic groups. Annual Review in Genetics 37, 283-328. 7 List of Abbreviations aa amino acid(s) AHL N-acyl homoserine lactones bp base pair(s) BLAST Basic Local Alignment Search Tool qC degrees Celsius d day(s) DGGE denaturing gradient gel electrophoresis DNA deoxyribonucleic acid dNTP deoxyribonucleotide triphosphate EDTA ethylene diamine tetraacetic acid, trisodium salt FISH fluorescent in situ hybridization g gram GFP green fluorescent protein GTR general time reversible h hour(s) HCl hydrochloric acid LGT lateral gene transfer l litre m milli (10-3) ȝ micro (10-6) M molar min minute(s) ML maximum likelihood MLSA multilocus sequence analysis NCBI National Centre for Biotechnology Information nm nanometres no. number NSS nine salts solution PCR polymerase chain reaction pmol picomole (10-9) RNA ribonucleic acid rpm revolutions per minute rpoB/RpoB the gene/protein encoding the RNA polymerase ȕ subunit 8 rRNA Ribosomal RNA s second(s) sp. species TBR tree bisection reconnection T-RFLP terminal restriction length polymorphism TLC thin layer chromatography UV ultraviolet VNSS V-medium modified from väätänen w/v weight per volume ratio 9 Table of Contents Originality Statement .....................................................................................................
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