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Identification and Quantification of Bacteria Associated with Cultivated Identification and quantification of bacteria associated with cultivated Spirulina and impact of physiological factors A thesis submitted for the degree of Master of Science in Engineering By Motlalekgomo Mogale In Centre for Bioprocess Engineering Research Department of Chemical Engineering University of Cape Town University of Cape Town The copyright of this thesis vests in the author. No quotation from it or information derived from it is to be published without full acknowledgement of the source. The thesis is to be used for private study or non- commercial research purposes only. Published by the University of Cape Town (UCT) in terms of the non-exclusive license granted to UCT by the author. University of Cape Town Plagiarism declaration I know the meaning of plagiarism and declare that all the work in the document, save for that which is properly acknowledged, is my own. Signature: i Acknowledgement I am grateful for the financial assistance of the South African Research Chairs Initiative (SARChI), of the Department of Science and Technology (DST) and the National Research Foundation (NRF) of South Africa. I thank the University of Cape Town for the space to learn and grow. To my main supervisor, Prof Sue Harrison, thank you for giving me the opportunity to be a part of the Centre for Bioprocess Engineering Research (CeBER) family, for taking me under your wing and nurturing me throughout this MSc. Your encouragement and motivation during our meetings and reviews has kept me sane and helped me not to give up on myself. Thank you for the job as well. My co-supervisors: Drs Melinda Griffiths and Mariette Smart, thank you for your support and advice. Mel, thank you for the many laughs, friendship and for sharing your knowledge with me. A big thank you to the Algae group, students and postdoctoral fellows at CeBER for their academic input. Dr Rob Huddy, thank you for the contribution at the beginning of this study. Emmanuel Nkgoma, Tich Samkange and Sharon Rademayer, thank you for the help with the laboratory work. To Sue Jobson, Candice Mazzolini, Lesley Mostert and Sandra Christian, thank you for all you’ve done for me and continue to do for CeBER. Thank you to the workshop for the help I received along the way. Joe Mackey, thank you for fixing the raceway ponds. Lefa Nkadimeng, thank you for your contribution, love and support. You are an amazing person. Thank you for believing in me and always seeing the best in me. Another big thank you to my family for the love, support and the many prayers you kept sending my way. Mommy, thank you for encouraging me and always being there for me. My late uncles: ramogolo Maachipane and rangwane Serishane, this work is dedicated to you. I dream and aspire for more because of you. God, thank you for my life and health. ii Abstract Research into the use of ‘algal’ biomass for human consumption is receiving increased attention due to their favourable nutritional value, photosynthetic efficiency, and lower requirement of land and fresh water as compared to terrestrial crops. The Spirulina species, also known as Arthrospira, is of particular interest due to its high protein content and nutritional value. Open raceway pond systems are popularly used for commercial industrial scale cultivation of microalgae due to their economic feasibility. These open cultivation systems are, however, susceptible to contamination by other microorganisms. This raises concerns relating to suitability for human ingestion and the need to control bacterial growth to prevent contamination by pathogens and to minimise the overall bacterial load. Further, bacterial contamination in processed (harvested and dried) Spirulina biomass has been reported, suggesting that some of these contaminants may end up in the market ready product where appropriate processing approaches are not used. This study sought to identify the microorganisms that typically contaminate Spirulina cultivation ponds, to understand their interaction with Spirulina biomass during cultivation and to evaluate the vulnerabilities of these contaminants, in order to generate strategies for controlling their populations during open pond cultivation. The main objectives of this study were therefore: To quantify the bacterial load in processed Spirulina powder from a single pilot facility to ascertain the presence of the contaminant in the final product derived from the outdoor pond system used as a case study, and to quantify the bacterial load in the outdoor cultivation cultures. To identify and characterize the bacteria associated with these Spirulina cultures and processed powder from a pilot operation carried out in Franschhoek, South Africa, with a particular focus on evaluating the likelihood for pathogens. To establish the dynamics of the relationship between Spirulina and bacterial growth under different environmental conditions including pH, salinity and temperature. To develop practical methods to control and minimize contamination. iii The bacterial contaminants were isolated from a sample taken from a commercial scale Spirulina cultivation pond during a pilot study, and identified by analysing their genetic finger prints by 16S rRNA sequencing. Various experiments were designed and carried out in the outdoor commercial scale open raceway ponds owned by BioDelta, laboratory scale open raceway ponds and closed airlift reactors. A modification of the cultivation medium recipe designed for commercial Spirulina production was used as a base case for all cultivation experiments. The medium was altered in various ways to assess the susceptibility of the contaminants to changing environmental conditions, thus, informing potential population control strategies. During the experimental campaigns, samples were analysed for Spirulina biomass concentration, bacterial load (counts) and medium composition in order to establish the growth characteristics and requirements of the bacterial contaminants during Spirulina growth cycle. Bacterial load in Spirulina powder produced from the BioDelta raceway ponds was determined by the standard agar plating method. The results indicated bacterial load of up to 1.6 ⨯ 107 cfu.g-1 of dry powder of Spirulina using fresh (nutrient) agar medium. When the same batches of Spirulina powder were analysed simultaneously on salty (salt enriched) agar, the highest bacterial load obtained was 6.2 ⨯ 107 cfu.g-1 which was between 2 and 4 fold higher than on the fresh agar medium used in CeBER laboratory. The results obtained from the fresh agar plates were compared to those obtained by SwiftSilliker food laboratory which used a similar medium. SwiftSilliker food laboratory obtained 1.6 ⨯ 106 cfu.g-1 as their highest bacterial load. The salts added to make up the salty agar are those present in the BioDelta medium recipe. This suggested that, the BioDelta medium salt composition was potentially favourable to the growth of the bacterial contaminants i.e. that these are halophiles and not pathogens. The nutrient agar cultivation supported no general pathogen threat with only one instance of a single opportunistic pathogen being found. The dominant bacterial contaminants were identified through clone libraries of the 16S rRNA gene fragments. The eleven dominant bacterial species included Alkalimonas delamerensis, Cecembia lonaresis, Pseudomonas mendocina, Paenibacillus camelliae, iv members of the genuses Halomonas, Mesorhizobium, Idiomarina and Micrococcus, with three unidentified species. These contaminants were largely halophiles and not the typical pathogens likely to pose danger to consumers. Only one instance of an opportunistic pathogen was found; Pseudomonas mendocina has been found to be pathogenic in immune compromised patients. All bacterial contaminants were associated with natural high salt environments: the soil, lakes and salterns (i.e. high pH and salt concentration). The commercial scale experiment to investigate the association between Spirulina and bacterial contaminants was carried out in a 50 000 L outdoor raceway pond over 67 days. Continuous harvesting of the Spirulina biomass started on day 17 after inoculation. During that initial 17 days of batch cultivation, the Spirulina biomass concentration increase from 0.08 g.L-1 to 1.28 g.L-1, while the bacterial load increased from 3.7 ⨯ 104 cfu.mL-1 after inoculation to 1.26 ⨯ 106 cfu.mL-1. Across the entire experiment, the growth of Spirulina correlated closely with growth in bacterial numbers. Owing to the oscillatory nature of the bacterial counts observed, repeat data was collected to investigate the quality of the results and their trends. A similar experiment to the 50 000 L raceway pond experiment was carried out in 80 L pilot scale open raceway pond in a greenhouse over 71 days with periodic biomass harvesting. Spirulina grew from 0.06 g.L-1 to 1.50 g.L-1 over a period of 41 days. The bacterial load increased from 6.73 ⨯ 104 cfu.mL-1 to 5.56 ⨯ 106 cfu.mL-1. From the comparative analysis between the 50 000L and 80 L pond, it was found that harvesting kept the bacterial load relatively low. Fluctuations were observed as with the 50 000 L pond. The effect of pH control agents (1M HCl and NaHCO3) on the growth of Spirulina culture and associated bacterial load was investigated in airlift reactors in the CeBER laboratories. Spirulina grew relatively the same across all reactors. However, the bacterial load was higher in cultures adjusted with HCl than with NaHCO3. The pH of cultures adjusted with NaHCO3 was better controlled. In order to minimize the bacterial load in open outdoor Spirulina cultivation systems, the effect of temperature, salinity and pH were investigated to provide potential strategies that v could manipulated. Experiments to address this objective were carried out in shake flasks using temperature controlled incubators where necessary. Of the temperatures investigated (25°C, 30°C and 35°C), it was found that 35°C had a negative effect on Spirulina biomass productivity. Spirulina grew best at 30°C. There were no significant effects of temperature on the bacterial load. Increase in salinity of the media by addition of salts did not increase the Spirulina growth or biomass concentration but increased the cost of the production.
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