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By Christopher Rathgeber Doctor of Philosophy Depar Diversity of the Aerobic Phototrophic and Heavy Metalloid Reducing Bacteria: Perspectives Gained from the Study of Novel Isolates. By Christopher Rathgeber A Thesis Submitted to the Faculty of Graduate Studies in Partial Fulfillment of the Requirements for the Degree of Doctor of Philosophy Department of Microbiology University of Manitoba Winnipeg, Manitoba Canada December,2006 @ Christopher Rathgeber, 2006 TI{E T]NIVERSITY OF MANITOBA FACT]LTY OF GRADUATE STUDIBS ***** COPYRIGHT PERMISSION Diversity of the Aerobic Phototrophic and Heavy Metalloid Reducing Bacteria: Perspectives Gained from the Study of Novel Isolates BY Christopher Rathgeber A Thesis/Practicum submitted to the Faculty of Graduate Studies of The University of Manitoba in partial fulfillment of the requirement of the degree Doctor of Philosophy Christopher Rathgeber @ 2007 Permission has been granted to the Library of the University of Manitoba to lend or sell copies of this thesis/practicum, to the National Library of Canada to microfïlm this thesis and to lend or sell copies of the film, and to University Microfîlms Inc. to publish an abstract of this thesis/practicum. This reproduction or copy of this thesis has been made available by authority of the copyright owner solely for the purpose of private study and research, and may only be reproduced and copied as permitted by copyright laws or with express written authorization from the copyright owner. Abstract. The research presented focused on the isolation of bacteria from extreme environments and their characterization in terms of phenotype, phylogeny, photosynthetic function and ability to reduce heavy metalloids. Isolates from the meromictic Mahoney Lake and deep ocean hydrothermal vents were examined using classical techniques and several were described taxonomically. The Mahoney Lake strains represented diverse new members of the aerobic phototrophic and the purple non-sulfur bacteria, produced unusual pigment protein complexes and were adapted to the fluctuating levels of pH and salinity in a meromictic lake. The metalloid resistant isolates also tolerated fluctuating conditions, and reduced TeO32- or SeO32- accumulating elemental Te or Se. Roseicyclus mahoneyensis gen. nov., sp. nov was proposed for ten vibrioid strains of aerobic phototrophic bacteria with an unusual monomodal light harvesting II complex (805-806 nm), and tolerance to high salinity. Four appendaged and budding bacteria were closely related to the genera Erythrobacter and Porphyrobacter. Although 165 rRNA phylogeny could not resolve the relationship between these two genera, the new isolates shared several phenotypic traits with the genus Porphyrobacter arld thus were proposed as a new species, P. meromictius. Phylogenetic analysis of metalloid-reducing strains identified them as relatives of Pseudoalteromonas. However they had important differences from previously described species and thus were proposed as P. telluritireducens sp. nov. and P. spiralis sp. nov. In order to determine the distribution of aerobic anoxygenic phototrophs in the ocean around black smokers the cultivable population rvas investigated, revealing that C. bathyomarinum can be found at depths of 500 m and below, but not at the surface. The T pigment protein complexes of this species were capable of light induced ¿- transfer and thus C. bathyomarinumis photosynthetically competent and should be able to supplement its energy needs when light is available. Photosynthetic e- transfer was investigated in P. meromictius, ML31 and R. mahoneyençls, ML6r. Photochemical activity in ML31 was observed aerobically, and the photosynthetic apparatus was not functional under anaerobic conditions. In ML6r low levels of photochemistry were measured anaerobically, however, electron transfer occurred optimally under low oxygen conditions, an interesting and unique case. m Acknowledgements. I would like to thank my supervisor, Dr. Vladimir Yurkov, for his guidance, and for his tremendous patience, for giving me the chance to pursue a graduate degree and for believing in my ability to tackle this project. I would also like to give special thanks to my collaborators for their important contributions. Dr. Jean Alric for providing invaluable assistance with all of the biophysical experiments. Dr. André Verméglio for advising on much of the biophysics portion of my research and for giving the opportunity to work in his lab in France. Dr. Natalia Yurkova for starting the Mahoney Lake and metalloid reduction projects, and leaving a wealth of data for my research Dr. J. Thomas Beatty who helped with preparations for my first research cruise, and for invaluable assistance in the preparation of articles. Dr. Erko Stackebrandt for phylogenetic analysis of most of the strains, and for supplying me with numerous phylogenetic trees. Michael T. Lince for phylogenetic analysis of the deep ocean aerobic phototrops. Dr. Peter Schumann for G+C determinations and for ribotyping of strains Se-l-2- redr and Te-2-2r. Dr. Elaine Humphrey for preparation of thin sections and assistance with electron microscopy. Jolantha Swiderski for sequencing of 165 rRNA genes of the Mahoney Lake strains. IV Dr. F. Gerald Plumley for HPLC to determine carotenoid composition of the marine aerobic phototrophs. Dr. Ken Hall for assistance in collecting samples from Mahoney Lake. Dr. Andrew Lang for assistance in collection of the Juan de Fuca Ridge samples. Dr. Robert Blankenship for phylogenetic analysis of the deep ocean aerobic phototrops. Dr. Cindy Van Dover for assisting with the collection of Juan de Fuca Ridge samples. I would also like to express my gratitude to the members of my advisory committee Dr. Elizabeth Worobec and Dr. John Markham for their excellent guidance and suggestions, as well as Dr. Gerhart Drews for agreeing to serve as external examiner for this thesis. V Table of contents. Page Abstract. tr Acknowledgements. IV Table of contents. VI List of tables. XtV List of figures. XVI List of abbreviations. XVm Chapter 1. Introduction. 1 1. 1. Microbial diversity of extreme environments. 2 1.1.1. Towards a definition of "extreme". 2 I.1.2. The meromictic Mahoney Lake. 3 1.1.3. Deep ocean hydrothermal vents of the Juan de Fuca Ridge. 5 1.I.4. Microbial diversity in extreme environments. 8 1.2. Significance of discovering new strains. 8 I.3. The aerobic phototrophic bacteria. 10 1.3.1. Ecological perspectives. 11 L.3.2. The importance of aerobic phototrophs in the ocean. 2I 1.3.3. Issues in taxonomy. 24 1.3.4. Photosynthetic pigments. 25 1.3.5. Photosynthesis in APB. 21 1.4. Heavy metalloid reducing bacteria. 35 VI 1.4.I. Ecological perspectives. 35 1.4.2. Mechanisms of metalloid reduction. 38 1.4.3. Industrial significance. 40 1.5. Aim of the thesis. 43 1.5.1. Chatactefization of new strains isolated from the meromictic Mahoney Lake. 43 1.5.2. Evaluation of the potential to resist and reduce high concentrations of KzTeOg and NazSeOs. 43 1.5.3. Description of new taxa. 44 1,.5.4. Search for APB at deep ocean hydrothermal vents and throughout the water column of the Pacific Ocean 44 1.5.5. Investigation of the photosynthetic apparatus of recently isolated APB. 45 I.6. References. 46 Chapter 2. Diversity, distribution and physiology of the aerobic phototrophic bacterial population in the meromictic Mahoney Lake in British Columbia. 77 2.I. Abstract. t8 2.2. Introduction. 78 2.3. Materials and methods. 80 2.3.1. Collection of samples. 80 2.3.2. Enumeration of bacteria. 80 2.3.3. Spectral analysis. 81 VII 2.3.4. Electron microscopy. 82 2.3.5. Physiology. 82 2.3.6. 165 rDNA-based phylogenetic analysis. 82 2.3.7. Nucleotide sequence accession numbers. 82 2.4. Results and discussion. 83 2.4.1. Enumeration and isolation. 83 2.4.2. Morphology and cytology. 89 2.4.3. Photosynthetic apparatus. 98 2.4.4. Nutritional and other properties. 103 2.4.5. Effect of salinity. 109 2.4.6. Phylogenetic analysis. t12 2.5. Concludingremarks. rt4 2.6. Acknowledgements. TT6 2.7. References. I16 Chapter 3. Isolation of tellurite- and selenite-resistant bacteria from hydrothermal vents of the Juan de Fuca Ridge in the Pacific Ocean. t2L 3.I. Abstract. 122 3.2. Introduction. 722 3.3. Materials and methods. 126 3.3.L Collection of samples. 126 3.3.2. Isolation and enumeration of metalloid-resistant bacteria. 126 3.3.3. Media used for subsequent cultivation. t28 3.3.4. Morphology and cytology. 128 VM 3.3.5. Resistance to and reduction of metalloid oxides. r29 3.3.6. Biochemical and physiological properties. 130 3.3.1. Phylogenetic analysis. 130 3.4. Results and discussion. 73r 3.4.I. Isolation and enumeration. 131 3.4.2. Morphology and cytology. 134 3.4.3. Metalloid oxide resistance and reduction. r40 3.4.4. Diagnostic growth and physiological properties. r44 3.4.5. Phylogenetic analyses. r46 3.5. Concluding remarks. 148 3.6. Acknowledgements. 149 3.7. References. 149 Chapter 4. Roseicyclus møhoneyensß gen. nov., sp. nov., an aerobic Phototrophic bacterium isolated from a meromictic lake. 160 4.I. Abstract. 161 4.2. Introduction. 162 4.3. Materials and methods. r63 4.3.1. Strains and cultivation. t63 4.3.2. Morphological and cytological tests. 164 4.3.3. Physiological and biochemical tests. 164 4.3.4. Pigment analysis. 165 4.3.5. G+C content determination. 165 4.3.6. 165 rDNA sequence analysis. t65 x 4.3.7. Nucleotide accession numbers. r66 4.4. Results and discussion. r66 4.4.I. Isolation. 166 4.4.2. Culture properties. r66 4.4.3. Morphology and cytology. r67 4.4.4. Photosynthetic apparatus. r69 4.4.5. Biochemical and physiological data. 17r 4.4.6. DNA composition and phylogenetic analysis. 173 4.5. Concluding rema¡ks. t75 4.6. Description of Roseicycløs gen. nov. n6 4J . Description of R. mahoneyensis sp. nov. 171 4.8. Acknowledgements. t78 4.9. References. 178 Chapter 5. Porphyrobacter meromictius sp.
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