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2018 Holanda RB Bangor University DOCTOR OF PHILOSOPHY A study of novel acidophilic Firmicutes and their potential applications in biohydrometallurgy Holanda, Roseanne Award date: 2018 Awarding institution: Bangor University Link to publication General rights Copyright and moral rights for the publications made accessible in the public portal are retained by the authors and/or other copyright owners and it is a condition of accessing publications that users recognise and abide by the legal requirements associated with these rights. • Users may download and print one copy of any publication from the public portal for the purpose of private study or research. • You may not further distribute the material or use it for any profit-making activity or commercial gain • You may freely distribute the URL identifying the publication in the public portal ? Take down policy If you believe that this document breaches copyright please contact us providing details, and we will remove access to the work immediately and investigate your claim. Download date: 11. Oct. 2021 A study of novel acidophilic Firmicutes and their potential applications in biohydrometallurgy A thesis submitted to the Bangor University in candidature for the degree of Philosophiae Doctor by Roseanne Barata Holanda B.Eng. School of Natural Sciences Bangor University Gwynedd, LL57 2UW U.K. 2018 Abstract The application of biotechnologies in the mining sector has intensified over the last 30 years, driven by the increasing demand for metals associated with the rise in energy costs and the awareness for environmentally responsible mining practices. Acidophilic prokaryotes play an important role in biohydrometallurgy, facilitating the solubilisation and recovery of base metals from ores and waste materials. The potential of novel acidophiles of the phylum Firmicutes for applications in biohydrometallurgical processes is examined in this thesis. Eight strains of extremely acidophilic bacteria were studied and shown to belong to the proposed novel genus “Acidibacillus”. These had been isolated previously from several distinct global locations and were shown to be obligately heterotrophic bacteria with potential to carry out tasks critical to biomining such as regenerating ferric iron (by catalysing the dissimilatory oxidation of ferrous iron), generating sulfuric acid (by the oxidation of zero-valent sulfur and tetrathionate; two strains only), and removing potentially inhibitory dissolved organic carbon. These isolates also demonstrated the ability to catalyse the dissimilatory reduction of ferric iron in anaerobic conditions. Results obtained during this study provide the basis for future research to assess their potential roles in microbial consortia applied in the bio-processing of metal ores. A novel obligately anaerobic acidophilic Firmicute (strain I2511) isolated from sediment obtained from an abandoned copper mine, was characterised in terms of its phylogeny and physiology. This isolate formed a separated clade within the Firmicutes, and was considered to represent a novel candidate genus. It also displayed a unique set of physiological traits, distinct from currently validated species of acidophilic Firmicutes. The isolate was an obligate anaerobe that grew via zero-valent sulfur (ZVS) respiration, generating H2S over a wide pH range (1.8 - 5.0), and also catalysed the dissimilatory reduction of ferric iron. Strains of acidophilic sulfate- reducing bacteria (aSRB), also Firmicutes, were shown to reduce ZVS at pH as low as 3. These aSRB, together with isolate I2511, populated a novel variant of a low pH sulfidogenic bioreactor. The “hybrid sulfidogenic bioreactor” (HSB) operated using both sulfate and ZVS as electron acceptors, and glycerol as electron donor. The bioreactor successfully remediated and recovered zinc from circum-neutral pH mine-impacted waters with distinct chemical composition collected from two abandoned lead/zinc mines in the U.K. The microbial consortium used in this system proved to be robust, in which the HSB generated H2S consistently under a wide pH range (2 – 7). Experiments demonstrated that H2S could also be generated abiotically in a non-inoculated low pH reactor, by the chemical reaction of ZVS and zero-valent iron to form iron sulfide, and the consequent acid dissolution of the latter. Operational costs and the advantages of biogenic and abiotic generation of H2S for recovery of transition metals from mine waters are discussed. v Acknowledgements I would like to dedicate this Ph.D. thesis to my wonderful family and friends for their unconditional love and encouragement. In special, to my father and my sister Juliana, that enthusiastically have supported me in every decision I have made in life, including the one to come to Bangor to live this incredible adventure, and to my mother (in memoriam), the greatest love I have ever experienced. I am immensely grateful for my uncle Lauro and my cousin Germana that have always guided, encouraged and inspired me to pursue a successful career. I am also deeply grateful for Donato, which his love and care motivated me daily to never give up despite all challenges. You will always be in my heart. I would like to express my sincere and deep gratitude to my supervisor Prof. D. Barrie Johnson, for allowing me to be part of his group, his patience and contribution towards my development, for sharing his knowledge and providing me with the best training so, I could have the necessary skills to embrace future professional endeavours with competence and confidence. I want to thank Dr. Barry M. Grail with all my heart and gratitude for his sincere friendship, encouragement, technical support and professional guidance throughout my Ph.D. He has stood by my side at every moment I needed, with endless patience, tranquillity and wisdom, in which I cannot put words to describe how important he has been to my life. I am very grateful for all the wonderful people I have met at Bangor University, in special BART members (Ana, Sarah, Laura Kelly, Eva, Rose Jones and Carmen), Wendy and Shila. I have learnt so much from all of you and I will keep in my heart every moment we spent together. A special thanks to Ivan Ñancucheo and Julio Espirito Santo that were responsible for connecting me with Prof. D. Barrie Johnson and therefore to this Ph.D. I am deeply grateful for the life changing opportunity you offered me and for believing in my potential. I am deeply grateful for having in my life Rita, Marcelo, Lynne, Ian, Verity and all members of Soka Gakkai International (UK) that wholehearted encouragement me during the most challenging times, in particular towards the completion of this thesis. My Buddhist practice has been fundamental to my life, giving me the strength, wisdom, courage and compassion to overcome all hardships, transforming the perception of the dignity and preciousness of my own life and all living beings, and therefore allowing me to create value from each moment I live. Finally, I would like to express my gratitude to the National Council of Technological and Scientific Development (CNPq) in Brazil for providing the scholarship for this Ph.D research. vi Contents Chapter 1 Introduction 1.1 Diversity of acidophilic prokaryotes in low pH environments .......... 1 1.1.1 Acidic ecosystems on planet Earth……………………………………….. 1 1.1.1.1 Natural acidic environments………………………………………………1 1.1.1.2 Extremely acidic mine-impacted environments……………………….. 3 1.1.2 Characteristics of acidophilic prokaryotes………………………… ......... 8 1.1.2.1 Autotrophic acidophilic bacteria……………………………………........ 12 1.1.2.2 Heterotrophic acidophilic bacteria………………………………… ........ 14 1.1.2.2.1 Phylum Firmicutes………………………………………………… ....... 16 1.1.2.2.1.1 Extremely acidophilic Firmicutes…………………………………….17 1.1.2.3 Extremely acidophilic archaea……………………………………………20 1.1.2.4 Zero-valent sulfur-reducing prokaryotes………………………………...22 1.1.2.4.1 Acidophilic and acid-tolerant ZVS-reducing prokaryotes……………25 1.1.2.5 Sulfate-reducing prokaryotes ............................................................. 26 1.1.2.5.1 Acidophilic and acid-tolerant sulfate-reducing prokaryotes…………28 1.2 Application of acidophilic prokaryotes in biohydrometallurgy…….. 30 1.2.1 Bioprocessing of mineral ores………………………………………… ...... 31 1.2.1.1 Oxidative bioprocessing………………………………………………… . 31 1.2.1.2 Reductive mineral bioprocessing…………………………………… ..... 34 1.2.2 Remediation of mine-impacted waters……………………………… ....... 37 1.2.2.1 Passive remediation systems………………………………………… .... 37 1.2.2.2 Active remediation systems…………………………………………… ... 39 1.3 Scope and objectives of the project described in this thesis ............ 44 Chapter 2 Materials and Methods 2.1 Microorganisms .................................................................................... 45 2.2 Microbial cultivation-based techniques............................................... 46 2.2.1 Basal salt solutions .............................................................................. 46 2.2.2 Trace elements (TE) ............................................................................ 46 2.2.3 Zero-valent sulfur (ZVS) suspensions .................................................. 47 2.2.4 Liquid media ......................................................................................... 48 vii 2.2.5 Solid media .......................................................................................... 49 2.2.6 Growth of bacteria under different oxygen concentrations .................... 49 2.3 Analytical Methods ..............................................................................
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