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Bacterial Biological Control of Toxic Cyanobacteria and the Resulting Eco-Toxicity

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Bacterial Biological Control of Toxic Cyanobacteria and the Resulting Eco-Toxicity Bacterial biological control of toxic cyanobacteria and the resulting eco-toxicity Luyanda Ndlela Dissertation presented for the degree of Doctor of Philosophy in the Faculty of Sciences at Stellenbosch University Supervisor: Professor Paul Johannes Oberholster Co-supervisor: Professor Johannes Hendrik van Wyk December 2019 Stellenbosch University https://scholar.sun.ac.za Declaration By submitting this thesis electronically, I declare that the entirety of the work contained therein is my own original work, that I am the authorship owner thereof (unless to the extent explicitly otherwise stated) and that I have not previously in its entirety or in part submitted it for obtaining any qualification. Date: December 2019 Copyright © 2019 Stellenbosch University All rights reserved i Stellenbosch University https://scholar.sun.ac.za Abstract The increased frequency and toxicity of freshwater cyanobacterial blooms is a cause for concern globally. Not only do these blooms result in reduced levels of oxygen in the water column and unpleasant odour, they also produce cyanotoxins as secondary metabolites. These toxins have resulted in the death of humans, aquatic organisms and wildlife. Bloom occurrences have been mapped globally and pose a challenge to water quality management due to toxin release, oxygen depletion, unpleasant water taste and odour. Biological control as a mitigation measure of these blooms has been explored using microorganisms and higher order grazers. A need exists for low cost, passive treatments through environmentally favourable control agents. In this dissertation, the biological control of filamentous Oscillatoria and unicellular Microcystis was investigated using predatory bacteria. Bacterial isolates from the phylum Proteobacteria were isolated and found to be effective in the reduction of microcystins released by both cyanobacteria. These were compared to a Lysinibacillus related isolate, which is from the phylum Firmicutes. The research conducted indicated a need for more molecular identification of wild strains of cyanobacteria, especially the less studied filamentous isolates to expand the database of sequences deposited for identification to be more conclusive through 16s rRNA gene sequencing. Microcystis was positively identified through 16srRNA identification and showed similarity to a species collected from another province in the same country. The exposure of cyanobacteria to bacterial numbers at lower ratios (2:1 ratios of cyanobacteria to bacteria) indicated a stress response from cyanobacterial cell morphology and a reduction in toxicity. The research found that Pseudomonas rhodesiae (isolate 3w) and the Lysinibacillus fusiformis related isolate (isolate B) resulted in a greater reduction of toxins (microcystins) in both the filamentous and unicellular isolates. Measurement of toxicity was through the ELISA (enzyme linked immunosorbent assay) and confirmed through HPLC (high performance liquid chromatography), which indicated the presence of two microcystin variants, microcystin -LR and -RR. The bacterial isolates readily reduced the more toxic microcystin -LR as opposed to microcystin R-R, indicating that there may be microcystin degrading capacity in the isolates. Screening of eco-toxicity from the resultant bacterial treatment in the water indicated that reduced toxicity resulted in higher survival from the bio-indicator organisms overall. Thamnocephalus platyurus, a freshwater crustacean, was the most sensitive to changes in toxicity, proving to be a more suitable confirmation method of microcystin reducing treatment interventions. Isolate B was the best isolate from both a toxin reducing and eco-toxicity response perspective. This study also compiled all the findings from cyanobacterial bloom research in the African context as well as gaps in the area of bacterial biological control globally. In summary, the present study confirmed the ii Stellenbosch University https://scholar.sun.ac.za potential to optimize passive bacterial control of cyanobacterial blooms on a larger scale, within a mixed bloom population. iii Stellenbosch University https://scholar.sun.ac.za Acknowledgements I would like to really thank my supervisors Paul Oberholster and Johannes van Wyk for all their support and guidance through this research. Thank you for all the opportunities you have provided me with and more importantly the motivation to complete this work despite challenges. I would also like to thank everyone I have worked with at the CSIR, from my senior colleagues to my peers. I would like to thank Tebogo Madlala, Paul Cheng, Yolanda Tancu, Maronel Steyn and Bettina Genthe for all the support and ear they have given to me throughout the years. You are greatly appreciated. I also thank the CSIR, NRF, Stellenbosch University and TISO foundation for research funding support over the course of this study. James Wesley-Smith from Sefako Makgatho University, staff from the Stellenbosch University Central Analytical Facility and Monique Smit from CSIR Biosciences, I thank you greatly for collaborating with me on this thesis. Thank you for assisting with microscopy and HPLC analysis which has been crucial in this study. Thank you to the Every Nation Zola family and Tina’s many mothers who have always been there to help when I needed to work long hours and could not cope on my own. Thank you especially to the Mdolomba and the Zaku families. I would also like to thank my great friends of many years for the laughs, support and wisdom through this journey. Bongi, Sthe, Nophiwe, Tshephiso, you are awesome. I would like to thank my family and friends for all their love and support through this journey, especially my little Tina, who has been so patient with me while I pursued this study. I also thank my Heavenly Father, the lover of my soul for gracing me to see this work through. You are faithful. Romans 8:28: And we know that all things work together for good to them that love God, to them who have been called according to his purpose. iv Stellenbosch University https://scholar.sun.ac.za This work has been presented at the following conferences: 19th International Water Association Symposium on Health-related water microbiology conference (North Carolina, USA May 2017): Luyanda Ndlela, Paul Oberholster, Johannes van Wyk & Po-Hsun Cheng. Bacteria as control agents of cyanobacteria (Poster presentation) 18th International Water Association Diffuse Pollutants and Eutrophication Conference (Los Angeles, USA August 2017): Luyanda Ndlela, Paul Oberholster & Johannes van Wyk. Bacterial control of toxic cyanobacteria (Poster presentation) Stellenbosch University Water Institute/WISA Symposium (Stellenbosch, South Africa November 2017): Luyanda Ndlela, Paul Oberholster & Johannes van Wyk. Biological control of toxic cyanobacteria (Oral presentation) 25th Crocodile Specialist Group Working Meeting (Santa Fe, Argentina May 2018): Luyanda Ndlela, Paul Oberholster, Christoff Truter, Monica Munoz de Toro & Johannes van Wyk: Cyanobacterial cell population and colonial form as factors affecting bacterial biological control response (Poster presentation) Water Institute of Southern Africa (WISA) biennial conference (Cape Town, South Africa June 2018) Luyanda Ndlela, Paul Oberholster & Johannes van Wyk. Up-scaling of bacteria as a treatment of wild toxic cyanobacterial isolates. (Oral presentation) This work has been published, accepted or submitted to the following journals Ndlela, L.L., Oberholster, P.J.,Van Wyk, J.H., Cheng, P.H. 2016. An overview of cyanobacterial bloom occurrences and research in Africa over the last decade, Harmful Algae, 60, 11-26. (published-4.138 impact factor) Ndlela, L.L., Oberholster, P.J., Van Wyk, J.H., Cheng, P.H. 2018. Bacteria as biological control agents of freshwater cyanobacteria: is it feasible beyond the laboratory? Applied Microbiology and Biotechnology 102, 9911-9923 (published-3.340 impact factor) Ndlela, L.L., Oberholster, P.J., Van Wyk, J.H., Cheng, P.H. A laboratory based exposure of Microcystis and Oscillatoria cyanobacterial isolates to heterotrophic bacteria (accepted for publication and in press Toxicon- 2.352 impact factor) Ndlela, L.L., Oberholster, P.J., Van Wyk, J.H., Cheng, P.H., Madlala, T.E. Determination of the eco- toxicity changes in biologically treated cyanobacteria Oscillatoria and Microcystis using indicator v Stellenbosch University https://scholar.sun.ac.za organisms (accepted as a book chapter contribution for a Springer book entitled: “Microbiological research methods in Africa”) vi Stellenbosch University https://scholar.sun.ac.za Dedication I dedicate this thesis to my angel in heaven, Minenhle Ndlela and my angel on earth, Tina Zime Silinga. vii Stellenbosch University https://scholar.sun.ac.za Table of Contents Declaration ............................................................................................................................................... i Abstract ................................................................................................................................................... ii Dedication ............................................................................................................................................... vii List of figures ........................................................................................................................................... 1 List of tables ...........................................................................................................................................
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