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Microbial – Deposit Feeder Aquaculture Bioremediation Systems

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Microbial – Deposit Feeder Aquaculture Bioremediation Systems Microbial – deposit feeder aquaculture bioremediation systems A Thesis Submitted By Georgina Robinson For the Degree of Doctor of Philosophy School of Marine Science and Technology Newcastle University February 2017 Abstract Land-based intensive aquaculture produces large volumes of particulate organic waste that can be upcycled into high value secondary biomass. In this research, the application of two key principles underpinning low-cost bioremediation technologies, namely the addition of rate limiting (i) electron acceptors (oxygen), and (ii) donors (carbon) is investigated in a sediment-based aquaculture effluent treatment system integrating the sea cucumber, Holothuria scabra. Growth trials of H. scabra, combined with next generation sequencing (NGS) technologies, were used to examine the response of sea cucumbers and sediment bacterial communities under contrasting redox regimes, describing fully oxic and redox- stratified sediments. The oxic system resulted in high taxonomic and functional diversity of bacteria with a range of dissimilatory metabolisms required for successful bioremediation of aquaculture wastes; however, the final biomass of H. scabra was significantly lower than the redox-stratified sediments (449.22 ± 14.24 g m-2 versus 626.89 ± 35.44 g m-2). Improving the resource quality of aquaculture waste through carbon supplementation was investigated. Increasing the carbon/nitrogen ratio from 5:1 to 20:1 with soluble starch significantly increased the biomass production of H. scabra on redox-stratified sediments compared to controls (1011.46 ± 75.58 g m-2 versus 702.12 ± 35.93 g m-2). A benthic flux incubation study, combined with NGS, demonstrated that carbon supplementation did not change the pathway of nitrogen cycling by mediating a shift from net release of ammonium to net assimilation, as hypothesised. A final study elucidated the critical role of the sea cucumber microbiome during aquaculture waste bioremediation, demonstrating that endogenous bacteria are primed, at ecological and genomic levels, to respond to nitrogen - a key nutrient limiting deposit feeder growth. Deposit feeder–microbial aquaculture bioremediation systems have the potential to rectify current inefficiencies of nitrogen use in the aquaculture production chain by offering a more economically and environmentally sustainable alternative to closing the nitrogen cycle loop. i We’ve got to learn to Reduce, Reuse, Recycle - Jack Johnson, “The 3 R’s” ii Acknowledgements First and foremost, I would like to thank Gavin Johnston for providing the initial impetus for the research at HIK Abalone Farm Pty and Bert, Louise and Roger for supporting the project. Throughout my time at HIK, I received tremendous support from Greg and his technical team, including Raphael, Gustav, Deon, Graham, Shorty, Sidelo, Nevado, and Tembeko, to build and maintain my recirculation system. I still have my melted plastic plaque from the oven and still occasionally enjoy playing underwater music to my sea cucumbers. I owe a great deal of thanks to Matt and Nelly for providing research support, to all the SASC volunteers and Rhodes students, especially Ann and Chris, for their assistance with experiments. My supervisors have been instrumental in my development and I thank them for giving me free reign and occasionally turning a blind eye to my extracurricular activities. Firstly, I would like to thank Selina, for believing me capable of a PhD all those years ago when we sat on bus driving around Zanzibar. You have supported me throughout this journey as a close friend and supervisor – thank you for looking after me, putting me up and feeding me during my time in Newcastle. I would like to thank Matthew Slater for his supervision during the first year of my PhD – having you on the end of skype to answer my questions when starting my first experiment was awesome. Cliff for teaching me statistics…I have come a long way from a girl who didn’t know how to calculate a standard error and fully admit that I am now a bit of a data geek. Also – thanks to you – I am slowly learning to develop a bit of OCD! Finally, to Gary who took me on part way through my PhD. You have been instrumental in helping me to write and publish my research and have always been there for me, thank you. I would like to acknowledge and thank the commercial hatcheries: Indian Ocean Trepang (formerly Madagascar Holothurie S.A.) and RIA 3 in Vietnam that supplied the juvenile sea cucumbers for this research. Thank you to Igor Eeckhaut for your initial guidance and input on my PhD proposal and to Jaco Chan Kit-Waye, Oliver Meraud and Olivier Avalle for assisting with the shipment from Madagascar. I would also like to thank Duy Nguyen Dinh Quang, Ty and Minh for their epic effort in successfully shipping live animals from Vietnam to South Africa and Ampie Van Wyk and Michael Falls for your valuable help and assistance with the red tape. I would like to acknowledge several people who assisted with specific components of the research: Margot for teaching me to use a pipette and Gwyneth for teaching me Mothur; Andrew Free for denoising my 454 data in QIIME; Matthew Wade for patiently helping with iii R scripts and Andrew Nelson for advising on Illumina workflows. The experiment in Chapter 5 was performed jointly with Thomas MacTavish with assistance and support from Candida Savage (Otago University, New Zealand), Trevor Probyn (DAFF, South Africa), Iain Alexander and Bradley Eyre at Southern Cross University, Australia. The experiment in Chapter 6 was performed at NAQUA in the Kingdom of Saudi Arabia. I am grateful to all the staff in the sea cucumber department, particularly Peter, Rory, Dylan, Wang, Melvin, Claro, Froilan, Risi and Monir for running the experiment and for their help during sampling. Sincere thanks to Ismail and his staff at CAS for sample analysis and to Shuaib and his team in microbiology, particularly Peter, for helping with the DNA extraction and sample shipment. Finally, I would like to thank Steve Rushton and Will Reid at Newcastle University for their superb assistance with the modelling of the sea cucumber microbiome. I gratefully acknowledge the financial support from the Biotechnology and Biological Research Council (BBSRC) who funded my Industrial CASE studentship (Grant Code BB/J01141X/1), the industrial partner in South Africa, HIK Abalone Farm Pty, and the Technology and Human Resources Program of the National Research Foundation, South Africa (grant number TP2011070800007). Finally, and most heartfelt, to my family, thank you for all your support during the four years that I have lived overseas - I am very fortunate to have a loving home to return to every year. iv Table of contents Abstract ........................................................................................................................................ i Acknowledgements ................................................................................................................... iii Table of contents ........................................................................................................................ v List of figures .......................................................................................................................... xiii List of tables ............................................................................................................................ xvi Chapter 1. General Introduction ................................................................................................. 1 1.1 Aquaculture ...................................................................................................................... 1 1.1.1 Current trends in global aquaculture production ....................................................... 1 1.1.2 Marine land-based aquaculture .................................................................................. 2 1.1.3 Treatment of dissolved inorganic nitrogen ................................................................ 3 1.1.4 Treatment of particulate organic wastes .................................................................... 4 1.1.5 Sustainability issues in land-based intensive aquaculture ......................................... 5 1.1.6 Ecologically-based systems ....................................................................................... 6 1.1.7 Technological developments ..................................................................................... 6 1.1.8 Particulate organic waste – an increasing problem ................................................... 7 1.2 Integration of deposit feeding sea cucumbers into land-based aquaculture systems ....... 8 1.2.1 Use of particulate organic matter for the production of secondary organisms .......... 8 1.2.2 Deposit feeding sea cucumbers as candidate species for aquaculture bioremediation ............................................................................................................................................ 8 1.2.3 Holothuria scabra – a candidate species for aquaculture bioremediation ................. 9 1.3 Marine sediments ............................................................................................................ 12 1.3.1 Biogeochemical cycling of carbon and nitrogen ..................................................... 12 1.3.2 Deposit feeding sea cucumbers as components of the benthic recycling system .... 14 1.3.3 Food resources and limitation of deposit feeder growth ........................................
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