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Physiological and Phylogenetic Studies of Thermophilic, Hydrogen and Sulfur Oxidizing Bacteria Isolated from Icelandic Geothermal Areas

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Physiological and Phylogenetic Studies of Thermophilic, Hydrogen and Sulfur Oxidizing Bacteria Isolated from Icelandic Geothermal Areas University of Akureyri Department of Buisness and Science Faculty of Natural Resource Science Natural Resource Science Physiological and phylogenetic studies of thermophilic, hydrogen and sulfur oxidizing bacteria isolated from Icelandic geothermal areas Hildur Vésteinsdóttir Supervisor: Dr. Jóhann Örlygsson University of Akureyri Submitted as in partial fulfillment for the degree of Master of Science in Natural Resource Science – Biotechnology May 2008 “I am among those who think that science has great beauty. A scientist in his laboratory is not only a technician: he is also a child placed before natural phenomena which impress him like a fairy tale.” Marie Curie ii University of Akureyri Department of Natural Resource Science Faculty of Business and Science 2008 Physiological and phylogenetic studies of thermophilic, hydrogen and sulfur oxidizing bacteria isolated from Icelandic geothermal areas Hildur Vésteinsdóttir Masters thesis for 45 credit M.Sc. in Biotechnology Printed copies: 15 Number of pages: 106 Appendices: 0 iii Declarations I here by declare that I am the only author of this thesis and it is the product of my own research. _____________________________ Hildur Vésteinsdóttir It is here by confirmed that this master thesis is satisfactory to M.Sc.- degree from the Faculty of Business and Science, department of Natural Resource Science. ______________________________ Dr. Jóhann Örlygsson iv Abstract Four thermophilic hydrogen oxidizing bacteria were isolated from various hot-springs in Grensdalur, Hveragerði, SW-Iceland. The strains were investigated with respect to phylogenetics, physiology, hydrogen uptake rates, biomass yield and sulfur metabolism. Phylogenetic studies of the isolates were done with both partial and full 16S rRNA analysis. Two true thermophilic strains were isolated, strain 16A and D10 growing optimally at 70 - 75°C, closely related to Hydrogenobacter species, showing 96% and 95% homology with Hydrogenobacter hydrogenophilus, respectively. The strains were cultivated under hydrogen oxidizing- (HOX), sulfur oxidizing- (SOX) and both hydrogen and sulfur oxidizing- (HOX+SOX) conditions. Kinetics of hydrogen oxidation, sulfate formation and generation times were investigated under all growth conditions. Both of the true thermophilic strains could grow under HOX conditions and are potential candidates for single cell protein production. In addition both strains were sulfur oxidizers and produced sulfate as end product which resulted in a low pH at the end of the experimental times. During both HOX and SOX conditions, a simultaneous oxidation of both hydrogen and thiosulfate occurred, although at lower rate compared to pure HOX and SOX conditions. The other strains isolated were moderate thermophiles. Strain 16C was identified as new species within the genus Hydrogenophilus, most closely related to H. thermoluteolus (95.6%) and strain 6C was identified as new species within the genus Thiomonas closely related to Tm. thermosulfata, Tm. perometabolis and Tm. intermedia (94.7 – 97.3% homology). Detailed results on various growth parameters were investigated for both moderate thermophilic strains, under various growth conditions (chemolithotrophic, heterotrophic, mixotrophic), concerning hydrogen uptake rate, biomass formation, sulfate production and utilization rates of organic compounds as well as growth rates. 16C was a very effective hydrogen oxidizer but could not utilize any of the sulfur compounds investigated. The strain could grow mixotrophically on hydrogen and several organic compounds. Strain 6C showed very versatile physiology. It could oxidize hydrogen and thiosulfate and grew also mixotrophically on hydrogen and/or thiosulfate with several organic compounds. This strain is a potential bacterium has a potential of being useful in bioremediation, i.e. removal of hydrogen sulfide. Key words: hot-spring, thermophilic, hydrogen oxidizing, sulfur oxidizing, single cell protein, bioremediation v Útdráttur Fjórar hitakærar vetnisoxandi bakteríur voru einangraðar úr heitum hverum úr Grensdal við Hveragerði. Stofnarnir voru rannsakaðir m.t.t. erfðafræðilegs skyldleika, lífeðlisfræði, vetnisupptökuhraða, lífmassamyndunar og brennisteinsefnaskipta. Skyldleikarannsóknir á stofnunum voru gerðar með bæði hlut- og fullraðgreiningu á 16S rRNA. Tveir hitakærir stofnar voru einangraðir, 16C og D10 sem vaxa best við 70 – 75°C. Þeir sýndu mestu sampörun við Hydrogenobacter hydrogenophilus (96 og 95%). Vöxtur var athugaður við mismunandi frumbjarga aðstæður; vetnisoxandi (HOX), brennisteinsoxandi (SOX) og bæði vetnis- og brennisteinsoxandi (HOX + SOX). Vaxtarhraði, vetnisoxunarhraði og hraði á myndun súlfats voru rannsökuð nákvæmlega við allar aðstæður. Báðir hitakæru stofnarnir gátu vaxið við HOX aðstæður og hugsanlega hægt að nýta sem einfrumuprótein framleiðendur. Einnig oxa báðir stofnarnir þíósúlfat og vetnissúlfíð sem leiddi til lækkunar á sýrustigi í ræktunarvökvum þeirra. Í viðurvist bæði vetnis og þíósúlfats sýndu báðir stofnarnir HOX og SOX efnaskipti á sama tíma þó svo að lægri vetnisupptaka og hægari súlfatmyndun væri en við hreinar HOX og SOX aðstæður. Hinir tveir stofnarnir voru lághitakærir. Stofn 16C var greindur sem ný tegund innan ættkvíslarinnar Hydrogenophilus, næst í skyldleika við H. thermoluteolus (95.6%) og stofn 6C greindist sem ný tegund innan ættkvíslar Thiomonas, skyldastur Tm. thermosulfata, Tm. perometabolis og Tm. intermedia (94.7 – 97.3% skyldleiki). Nákvæm lífeðlisfræðileg gögn eru birt um báða lághitakæru stofnana undir margvíslegum vaxtarskilyrðum (ófrumbjarga, frumbjarga, mixótrópískt); vetnisupptökuhraði, hraði lífmassa myndunar og súlfatmyndunar auk niðurbrotshraða á lífrænum efnum sem voru notuð sem hvarfefni í tilraununum. Stofn 16C var mjög öflugur sem vetnisoxandi en sýndi ekki brennisteinsefnaskipti. Stofninn óx “mixótrópískt” á vetni og nokkrum lífrænum efnasamböndum. Stofn 6C var með mjög fjölbreytt efnaskipti. Hann gat oxað vetni og þíósúlfat og einnig óx hann mikótrópískt á vetni og/eða þíósúlfati með nokkrum lífrænum efnum. Hugsanleg not fyrir slíkan stofn eru í lífhreinsun á brennisteinsefnasamböndum eins og t.d. brennisteinsvetni. Lykilorð: heitir hverir, hitakær, vetnisoxun, brennisteins oxun, einfrumuprótein, lífhreinsun. vi Acknowledgements I would like to thank Dr. Jóhann Örlygsson for giving me the opportunity to be a part of this project, giving me invaluable help and guidance. I would also like to thank Dagný Björk Reynisdóttir and Steinar Rafn Beck Baldursson for the help and support; the staff at Prokaria who gave me helpful information, suggestion and guidance concerning the phylogenetics, Ásgeir Ívarsson, from the engineering company Mannvit, and Jakob K. Kristjánsson for helpful information and suggestion. Furthermore I would like to thank everyone at TUT in Finland for allowing me to do part of my research there and the fellow students on the lab Margrét Auður Sigurbjörnsdóttir and Hilma Eiðsdóttir Bakken. In addition I want to thank my family for supporting me throughout my studies. vii Table of Contents 1. Background and research objective ...........................................................1 2. Introduction................................................................................................3 2.1 Thermophilic prokaryotes and their habitats .............................................4 2.1.1 Geothermal areas ................................................................................7 2.1.2 Microbial flora in Icelandic hot-springs .............................................8 2.1.2.1 Grensdalur.........................................................................................10 2.2 Chemolithotrophy ....................................................................................11 2.3 Energetics of inorganic oxidations...........................................................13 2.4 Hydrogen..................................................................................................15 2.4.1 The "knallgas reaction".....................................................................16 2.5 Hydrogen-oxidizing bacteria (knallgas bacteria).....................................18 2.5.1 Physiology.........................................................................................19 2.5.1.1 Biomass formation ............................................................................20 2.5.2 Distribution .......................................................................................21 2.5.3 Thermophilic hydrogen-oxidizing bacteria.......................................22 2.5.3.1 Hydrogenophilus...............................................................................23 2.6 Inorganic sulfur compounds.....................................................................24 2.6.1 The sulfur cycle.................................................................................24 2.6.2 Oxidation of inorganic reduced sulfur compounds by bacteria ........26 2.7 Sulfur-oxidizing bacteria..........................................................................30 2.7.1 Physiology.........................................................................................30 2.7.2 Distribution .......................................................................................32 2.7.3 Thermophilic sulfur-oxidizing bacteria ............................................32 2.7.3.1 Thiomonas.........................................................................................33 2.7.3.2 Hydrogenobacter ..............................................................................34
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