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Corals at the Extreme: Partitioning the Response of Coral Holobionts to Marginal Habitats

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Corals at the extreme: partitioning the response of coral holobionts to marginal habitats Bethan Greenwood A thesis submitted for the degree of Doctor of Philosophy in Marine Biology School of Life Sciences University of Essex October 2020 Abstract While coral reefs worldwide are threatened by unprecedented environmental change, some reef-building corals can already be found living under extreme conditions within marginal habitats. Learning how corals can survive high temperature fluctuations and multiple other stressors experienced in mangroves, relative to typical reefs, is a key step in understanding the adaptive capacity of reef-building corals to future environmental change. The role of the coral host, symbiotic algae, and diverse microbiota, and how these components of the holobiont interact to define the adaptive capacity of reef-building corals requires further exploration. In this thesis, the thermal tolerance limits of conspecific corals from a mangrove versus a reef habitat were tested in a 20-day heat-ramping experiment. Heating corals beyond their regional thermal maxima caused severe decreases in productivity, irrespective of which habitat the coral came from, but corals from the mangrove habitat suffered less thermally induced bleaching. Amplicon sequencing coral holobionts from reef and mangrove habitats in Indonesia and the Seychelles revealed significant habitat-dependent differences in coral microbiome compositions. A potentially novel coral-bacteria symbiosis between a mangrove-dwelling merulinid coral and an unclassified spirochaete, which accounted for 47% of the coral’s bacterial community, was also uncovered, though its role in the holobiont remains unknown. Reciprocal translocations of corals between reef and mangrove habitats resulted in rapid reorganisation of coral-associated bacterial communities. Within four days of translocation, coral-associated bacterial communities had changed. Corals demonstrated local adaptation and exhibited increased survivability when back-transplanted in their native habitat than when cross-transplanted to a new habitat. Experimental manipulation of the coral microbiome by antibiotic treatment demonstrated its sensitivity to disturbance, with rapid shifts in bacterial abundance, diversity, and composition taking place within 36 hours. These findings demonstrate the conservation value of mangrove coral habitats and highlight the rapid habitat-dependent flexibility of the coral microbiome. I Acknowledgements My PhD began in the wake of the world’s third global mass-bleaching event (colloquially termed the Godzilla El Niño), and ended amidst the ongoing Coronavirus pandemic. Though depressing and stressful at times, working on this four-year long project has taught me so much about resilience (and not just in corals!). I’d like to start by thanking all of my supervisors, including those I started this journey with, and those I gained along the way. Dave, Etienne, Boyd, and Michelle, I really appreciate all the advice and support given, and wouldn’t have been able to pull this together without the expertise and encouragement of all of you. You have all helped shape me as a scientist. I would also like to acknowledge the EnvEast Doctoral Training Partnership for support and training provided throughout my PhD, and recognise the scholarship I was awarded from NERC which funded me to conduct this project. Thank you to the University of Essex technicians – Tania, Russ, John, and Farid – who helped me navigate each lab I worked in, graduate administrator – Emma, and graduate directors – Terry and Corinne, for keeping me organised. I am extremely grateful for the amazing opportunities afforded to me by the NGOs Operation Wallacea, and Earthwatch with funding from Mitsubishi. I am privileged to have worked in places some people only ever dream of visiting. I am also thankful for the partnerships made with Hasanuddin University, Makassar, Indonesia and the Seychelles National Parks Authority. I would like to say a whole-hearted thank you to the local staff at both the field sites I worked at. Thank you to the boat captains and crews who always helped with a smile, no matter how awkward my logistical requests. Thank you to the local administrative, house- keeping, and kitchen staff for making me feel so welcome to work in their home countries. And thank you to the enthusiastic international volunteers who I dragged along to the mangroves, and hopefully inspired to continue marine science. II I am grateful for all my colleagues and friends made over the 5 years I have spent living in Essex, and those I lived and worked in close quarters with during field expeditions. The value of teamwork became so clear on these research expeditions. A truly heartfelt thank you goes to my amazing parents who taught me not to shy away from hard work, and inspired my love of the ocean through the summers spent rock-pooling in Cornwall and Brittany, eventually learning to SCUBA dive with my dad and brother. Thank you to my grandparents who would always ask about my many trips to far-flung locations, getting bored to sleep by the digital photo albums, and asking ‘have you discovered anything yet?’. Finally thank you to my partner Phil for believing in me, supporting me through all the stresses of my (and his) PhD, and for answering the phone in the dead of night to Indonesian phone numbers when I needed someone to scan my visa documents! A special mention goes to our wonderful unruly hound, Dylan the dachshund, who kept me on my toes, figuratively and literally, through the write-up during the UK coronavirus lockdown. I dedicate this thesis in loving memory of Jim ‘Papa’ Greenwood. III Table of Contents Abstract .............................................................................................................................. I Acknowledgements ........................................................................................................... II Chapter 1: Literature review: Exploring the survival mechanisms of coral holobionts facing sub-optimal environments ...................................................................................... 1 Abstract ............................................................................................................................. 1 1.1. The coral bleaching crisis ........................................................................................... 2 1.2. The coral holobiont ..................................................................................................... 7 1.3. The coral host ........................................................................................................... 10 1.3.1. Host genotype .................................................................................................... 10 1.3.2. Host acclimatisation ........................................................................................... 13 1.3.3. Gene expression ................................................................................................ 14 1.3.4. Host control over symbionts ............................................................................... 16 1.4. Zooxanthellae ........................................................................................................... 17 1.4.1. What are they? Their symbiotic relationship with coral ....................................... 17 1.4.2. The breakdown of the relationship – bleaching .................................................. 18 1.4.3. Symbiodiniaceae systematics and thermotolerance ........................................... 19 1.4.4. Adaptive bleaching hypothesis ........................................................................... 20 1.4.5. Symbiont switching ............................................................................................ 21 1.4.6. Symbiont shuffling .............................................................................................. 22 1.4.7. Trade offs ........................................................................................................... 23 1.4.8. How can the role of zooxanthellae be disentangled from other factors? ............. 24 IV 1.5. Bacteria .................................................................................................................... 25 1.5.1. Bacterial bleaching hypothesis ........................................................................... 25 1.5.2. Coral probiotic hypothesis .................................................................................. 25 1.5.3. Role of bacteria in conferring heat tolerance ...................................................... 26 1.5.4. Antibiotic treatment ............................................................................................ 27 1.6. Archaea .................................................................................................................... 28 1.7. Fungi ........................................................................................................................ 29 1.9. Viruses ..................................................................................................................... 30 1.10. Natural laboratories ................................................................................................ 31 1.11. Conclusion .............................................................................................................. 32 1.12. Synopsis ................................................................................................................
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