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The Dynamics of Bacterial Populations Associated with Corals and the Possible Role of Bacterial Pathogens in Coral Bleaching

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The Dynamics of Bacterial Populations Associated with Corals and the Possible Role of Bacterial Pathogens in Coral Bleaching ResearchOnline@JCU This file is part of the following reference: Littman, Raechel (2011) The dynamics of bacterial populations associated with corals and the possible role of bacterial pathogens in coral bleaching. PhD thesis, James Cook University. Access to this file is available from: http://researchonline.jcu.edu.au/32219/ The author has certified to JCU that they have made a reasonable effort to gain permission and acknowledge the owner of any third party copyright material included in this document. If you believe that this is not the case, please contact [email protected] and quote http://researchonline.jcu.edu.au/32219/ The dynamics of bacterial populations associated with corals and the possible role of bacterial pathogens in coral bleaching Thesis submitted by Raechel Littman M. Public Policy February 2011 For the degree of Doctor of Philosophy In the School of Marine and Tropical Biology James Cook University STATEMENT ON SOURCES Declaration I declare that this thesis is my own work and has not been submitted in any form for another degree or diploma at any university or other institution of tertiary education. Information derived from the published or unpublished work of others has been acknowledged in the text and a list of references is given. …………………………. ……………………. (Signature) (Date) ii STATEMENT ON THE CONTRIBUTION OF OTHERS Funding for the research within this thesis was obtained from the Australian Institute of Marine Science, AIMS@JCU and the ARC Centre of Excellence. Stipend support was given by James Cook University Postgraduate Research Scholarship. Intellectual and editorial support was provided by the supervisory team consisting of Professor Bette Willis (James Cook University) and Dr. David Bourne (Australian Institute of Marine Science). Dr. Line Bay designed the translocation experiment in Chapter 3 and participated in the translocation of corals and sample collection. Dr. David Abrego provided intellectual support in the set-up and design of the heat stress experiment in Chapter 5. Dr. Sylvain Floret provided bioinformatics advice for the metagenomics study in Chapter 6. Dr. Carolyn Smith-Kuene collected samples and bleaching data used in Chapter 6. Emily Howells and Nick Larsen were responsible for the juvenile corals used in Chapter 4 and 5. iii Acknowledgements I would first like to acknowledge my supervisory team that has been there for me throughout health problems, nervous breakdowns and many other trying times. Thank you Bette Willis for your kindness, inspiring enthusiasm for science and your amazing writing skills. Thank you David Bourne for your enduring patience, brilliance, and limitless support. I have become your biggest admirer. I can‟t fully express how much help you two have been to me and how much you have aided in my growth through these years. Several people have given me intellectual support and have worked so very hard in the field to provide me with invaluable samples. I can‟t thank enough David Abrego, Line Bay, Sylvain Floret, Yui Sato, Eneour Puill-Stephan, Emily Howells, Nick Larsen, Allison Palley, Madeleine van Oppen, Ray Berkelmans and Carolyn Smith- Kuene. And finally, thank you to my friends and family that have been my emotional support. Special thanks to James Newton for being my partner through trials and tribulations and making my PhD a fun experience. iv Publications resulting from research in this thesis Littman, R., Bourne, D., Pfeffer, C. and Willis, B. 2009 Diversities of coral-associated bacteria differ with location, but not species, for three acroporid corals on the Great Barrier Reef. FEMS Microbiology, 68, 152-163. Littman, R., Bourne, D. and Willis,B. 2009 Bacterial communities of juvenile corals infected with different Symbiodinium (dinoflagellate) clades. Marine Ecology Progress Series, 389, 45-59. Littman, R., Bourne, D. and Willis, B. 2010 Responses of coral-associated bacterial communities to heat stress differ with Symbiodinium type on the same coral host. Molecular Ecology, 19, 1978-1990. Littman, R., Bourne, D. and Willis, B. 2011 Metagenomic analysis of the coral holobiont during a natural bleaching event on the Great Barrier Reef. Environmental Microbiology (in press) v ABSTRACT The coral holobiont is known to comprise a diverse array of microbial partners, including the dinoflagellate endosymbiont, Symbiodinium, and bacteria living both on and within coral tissues, but little is known about the contributions that bacterial communities make to the overall partnership or how they interact with other microbial partners. Research described in this thesis aimed to understand coral- associated bacterial communities on the Great Barrier Reef and the nature of their interactions with Symbiodinium partners. Bacterial diversities documented on three common reef corals, Acropora millepora, A. tenuis and A. valida, confirmed that corals associate with specific microbiota. According to three culture-independent techniques [denaturing gradient gel electrophoresis (DGGE), terminal restriction fragment length polymorphism (t-RFLP) and clone libraries], consistent bacterial profiles were also conserved among all three species of Acropora within each of two study locations (Magnetic Is and Orpheus Is reefs), suggesting that closely related corals of the same genus harbor similar bacterial types. Bacterial community profiles of A. millepora at Orpheus Island were consistent throughout the year, indicating a stable community despite seasonal variation in environmental parameters. However, clone libraries, DGGE and t-RFLP profiles revealed bacterial communities grouped according to location rather than coral species. To further investigate the influence of environmental factors on coral- microbial associations, adult colonies of A. millepora were reciprocally translocated between two nearshore reefs (Magnetic Island and Great Keppel Island reefs) that differed in temperature. Clone libraries and DGGE profiles for corals placed on i galvanized iron racks revealed that bacterial communities differed from those associated with in situ corals at Magnetic Island. Lack of change in bacterial communities of translocated corals through two bleaching events (a cold water bleaching on Great Keppel Island reef and a warm water bleaching at Magnetic Island reef) suggests that the rack environment of translocated corals was more important in shaping bacterial communities associated with Acropora millepora than the reef environment to which they were translocated. Nutrient inputs, such as metal derived Fe2+, may have influenced the bacteria present on translocated corals and should be considered in manipulative studies. A study comparing bacterial communities on 9-month old juvenile corals hosting either type C1 or D Symbiodinium suggested that coral-associated bacteria are not linked to Symbiodinium type in hospite, at least during early ontogeny. However, in contrast to bacterial profiles of adult corals, bacterial communities associated with juvenile corals were highly variable, indicating that bacterial associates are not conserved in these early stages. When 12-month old juveniles were sampled again in summer, bacterial communities associated with A. tenuis hosting clade D Symbiodinium were dominated by sequences affiliating with Vibrio species, indicating that corals harbouring this symbiont may be more susceptible to temperature stress, allowing growth of opportunistic microbial community members, possibly detrimental to coral health. To further investigate the role that temperature may play in the complex interactions of the coral holobiont, a controlled temperature experiment was undertaken with bacterial community shifts assessed in relation to coral Symbiodinium type. Shifts in bacterial associates on juvenile corals harboring ITS 1 type D Symbiodinium were observed when placed in a high (32°C) temperature treatment. In ii particular, there was a marked increase in the number of retrieved Vibrio-affiliated sequences, which coincided with a marked decline in their photochemical efficiency. In contrast, A. tenuis hosting ITS 1 type C1 Symbiodinium did not exhibit major bacterial shifts in the elevated temperature treatment, indicating a more stable bacterial community during thermal stress; concomitantly a decline in photochemical efficiency was minimal for this group. The lower resilience of A. tenuis to thermal stress when harbouring Symbiodinium D highlights the importance of inter-kingdom interactions among the coral host, dinoflagellate endosymbiont and bacterial associates for coral health and resilience. Comparisons of healthy vs. bleached coral metagenomic datasets revealed major shifts in microbial associates during heat stress, including shifts in Bacteria, Archaea, viruses, Fungi and micro-algae. The microbial community shifted from an autotrophic to a heterotrophically-driven metabolism, as evidenced by increases in fatty acid, protein, simple carbohydrate, phosphorus, and sulfur metabolism genes. The proportion of virulence genes was also higher in the bleached sample, indicating that bleaching may contribute to an increase in microorganisms capable of pathogenesis. These results demonstrate that thermal stress can result in shifts in coral-associated microbial communities, which may lead to deteriorating coral health. iii CONTENTS Abstract i Contents iv List of Figures vii List of Tables ix Chapter 1.0 Background and General Introduction 1 1.1 Coral reefs under threat 2 1.2 The coral holobiont 3 1.2.1 Symbiodinium diversity and function
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