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A Study on the Phototrophic Microbial Mat Communities of Sulphur Mountain Thermal Springs and Their Association with the Endangered, Endemic Snail Physella Johnsoni

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A Study on the Phototrophic Microbial Mat Communities of Sulphur Mountain Thermal Springs and Their Association with the Endangered, Endemic Snail Physella Johnsoni A Study on the Phototrophic Microbial Mat Communities of Sulphur Mountain Thermal Springs and their Association with the Endangered, Endemic Snail Physella johnsoni By Michael Bilyj A thesis submitted to the Faculty of Graduate Studies in partial fulfillment of the requirements for the degree of Master of Science Department of Microbiology Faculty of Science University of Manitoba Winnipeg, Manitoba October 2011 © Copyright 2011, Michael A. Bilyj 1 Abstract The seasonal population fluctuation of anoxygenic phototrophs and the diversity of cyanobacteria at the Sulphur Mountain thermal springs of Banff, Canada were investigated and compared to the drastic population changes of the endangered snail Physella johnsoni. A new species and two strains of Rhodomicrobium were taxonomically characterized in addition to new species of Rhodobacter and Erythromicrobium. Major mat-forming organisms included Thiothrix-like species, oxygenic phototrophs of genera Spirulina, Oscillatoria, and Phormidium and purple nonsulfur bacteria Rhodobacter, Rhodopseudomonas and Rhodomicrobium. Aerobic anoxygenic phototrophs comprised upwards of 9.6 x 104 CFU/cm2 of mat or 18.9% of total aerobic heterotrophic bacterial isolates at certain sites, while maximal purple nonsulfur and purple sulfur bacteria were quantified at 3.2 x 105 and 2.0 x 106 CFU/cm2 of mat, respectively. Photosynthetic activity measurements revealed incredibly productive carbon fixation rates averaging 40.5 mg C/cm2/24 h. A temporal mismatch was observed for mat area and prokaryote-based organics to P. johnsoni population flux in a ―tracking inertia‖ manner. 2 Acknowledgements It is difficult to express sufficient gratitude to my supervisor Dr. Vladimir Yurkov for his unfaltering patience, generosity and motivation throughout this entire degree. Dedication to his students‘ progress and betterment was never a question. Thanks also to my committee members Michele Piercey-Normore and Brian Mark for their guidance, understanding and all of their time spent following the project. To Charlie Pacas and Dwayne Lepitzki, thank you for all the coordination and information you both provided and for the opportunity to work in a unique environment on such an exceptional project. To my lab comrade Julius Csotonyi, I can‘t think of anyone better to have shared the space, the science and endless humor with. Thanks go to him for always having time to be a good teacher and great friend. I would like to thank everyone else that has been a part of the Yurkov lab including Chris Rathgeber, Sarah-Taylor Mullineaux, Max Popov, Elizabeth Hughes and Chris Maltman. I learned something from all of you. 3 Table of Contents Abstract……………………………………………………………………………...2 Acknowledgements………………………………………………………………….3 Table of Contents……………………………………………………………………4 List of Tables………………………………………………………………………..7 List of Figures……………………………………………………………………….8 1 Introduction 1.1 Sulphur Mountain Thermal Springs, Banff, Alberta 1.1.1 Sulphur Mountain and Thermal Springs…………………………......11 1.1.2 Human Activity and Historic Spring Sites………...............................13 1.1.3 Climate and Spring Water Characteristics…………………………...15 1.1.4 Scientific Interest…………………………………………………….17 1.2 Physella johnsoni, the Banff Springs Snail 1.2.1 Species Description ………………………………………………….18 1.2.2 Distribution, Population Trends and Limiting Factors………………21 1.2.3 Significance and Recovery Management…………………………….24 1.3 Cyanobacterial Mats and Spring Ecology 1.3.1 General Description………………………………………………….28 1.3.2 Vertical Structure and Chemical Gradients………….………………31 1.4 Oxygenic and Anoxygenic Phototrophs in Microbial Mats 1.4.1 Cyanobacteria and Algae……………………….................................34 1.4.2 Exopolymeric Substances……………………..……..………………41 1.4.3 Purple and Green Sulfur and Nonsulfur Bacteria................................43 1.4.4 Aerobic Anoxygenic Phototrophic Bacteria……………….………...48 1.4.5 Thiothrix……………………………………………………………...50 1.4.6 Advantages of Communal Living……………………………………51 4 1.5 Prokaryotes and Mollusc Nutrition 1.5.1 Nutrition in Physids………………………………………………….52 1.5.2 Grazer Interactions with Periphyton…………………………………56 1.6 Project Goals…………………………………………………………………57 2 Materials and Methods 2.1 Collection of Samples………………………………………………………60 2.2 Isolation, Enumeration and Enrichment of Bacteria……………………….60 2.3 Spectral Analysis……………………………………………………………62 2.4 Light Microscopy...…………………………………………………………63 2.5 Photosynthetic Activity and Carbonates Measurement……………………..63 2.6 Physiological and Biochemical Tests……………….……………….……...63 2.7 Genomic Analysis……………………………………………….………….64 3 Results and Discussion 3.1 Abundance and Diversity of the Phototrophic Microbial Mat Communities of Sulphur Mountain and their Relationship to the Endangered Banff Springs Snail, Physella johnsoni 3.1.1 Study Site Description……………………………………………….65 3.1.2 Macro- and Microscopic Analysis of Natural Samples……………...67 3.1.3 Seasonal Community Spectrum Analysis……………………………74 3.1.4 Enumeration of Anoxygenic Phototrophs……………………………77 3.1.5 Diversity of Isolated Strains………………………………………….82 3.1.6 Microbial Carbon Fixation Rates ……………………………………90 3.1.7 Microbial Dynamics and Physella johnsoni Trends…………………95 3.1.8 Closing Comments…………………………………………………104 3.2 Rhodomicrobium vangemerdenii sp. nov., an exospore-forming purple nonsulfur bacterium isolated from sulfidic thermal springs in Banff, Alberta, Canada 5 3.2.1 Abstract and Opening Remarks…………………….………………107 3.2.2 Culture Properties…………………………………………………..110 3.2.3 Morphology…………………………………………………………110 3.2.4 Photosynthetic Pigments and Photosynthesis………………………112 3.2.5 Biochemical and Physiological Data……………………………….114 3.2.6 Description of R. vangemerdenii…………………………………...118 3.3 Rhodobacter fonsus sp. nov., a purple nonsulfur Alphaproteobacterium isolated from Sulphur Mountain Thermal Springs in Banff, Alberta, Canada 3.3.1 Abstract and Opening Remarks…………………….………………120 3.3.2 Taxonomic Characterization Test Results………………………….122 3.3.3 Description of R. fonsus…………………………………………….127 3.4 Erythromicrobium magnum sp. nov., an aerobic anoxygenic phototroph isolated from Sulphur Mountain Thermal Springs in Banff, Alberta, Canada 3.4.1 Abstract and Opening Remarks………………………….…………129 3.4.2 Taxonomic Characterization Test Results………………….………129 3.4.3 Description of E. magnum………………………………………….133 4 Conclusions 4.1 Summary of Results……………………………………………………….135 4.2 Future Prospects…………………………………………………………...137 References………………………………………………………………………...140 6 List of Tables Table 1. Summary of seasonal observations showing collection dates, organisms or morphotypes dominant in each sample as viewed by a light microscope, thickness of the mat sample, Site temperature, pH, carbonate and bicarbonate levels, sulfide (HS-) and dissolved oxygen (DO) levels; maximum peaks of whole-community spectral analysis and mat development expressed as a percentage of the maximum development observed in August 2003. HS-, DO from Lepitzki 2007. Blanks indicate not determined (nd).…69 Table 2. Chl a, b and c values in µg Chl/g microbial mat for Banff Springs sampling sites at six collections between October 2005 and November 2007. Proportions were calculated from wet samples and are therefore an underestimate of actual Chl contained per mass of mat. ns indicates not sampled………………………..……………………..74 Table 3. Bchl a values expressed as µg Bchl/g microbial mat for Banff Springs sampling sites in select seasons. Regarding Chl, data were obtained from wet samples and are an underestimate of actual Bchl contained per mass of mat…………………….….……….77 Table 4. Number and proportion of Bchl a-containing isolates of total bacteria enumerated on selective media in all sampling seasons…………………………………80 Table 5. Phenotypic and phylogenetic diversity of select strains isolated from the Sulphur Mountain thermal spring microbial mats……………………………………….83 Table 6. Productivity of different fractions of the microbial mat community and total carbon fixation for sampling locations at the Sulphur Mountain springs in late spring, autumn and winter………………………………………………………………………..91 Table 7. Comparative physiological characteristics of new isolates BF1, BF14 and BF16 and type species R. vannielii…………………………………………………........................117 Table 8. Differential characteristics of strain BF9T and closely related Rhodobacter species ………………………………………………………………………………….124 7 List of Figures Fig. 1. The Banff Springs snail, Physella johnsoni. Bar, 5 mm………………………..20 Fig. 2. Map of the Banff Sulphur Mountain thermal springs area (A) including the Cave and Basin Historic Tourist Site (B) and the Upper Middle springs restricted area (C). Sampling locations Sites are indicated by numbers 1-13. Black dots in (A) indicate individual springs; lined area is Town of Banff; UCB, Upper Cave and Basin spring source; LCB, Lower Cave and Basin spring source…….……………………………….66 Fig. 3. Site photos and phase-contrast micrographs of morphological diversity observed at the Banff springs. Listed genera are morphologically similar or were determined by 16S rRNA sequencing with percent relatedness indicated in brackets. A) purple mat at Site 8, UCB; B) Thiothrix- and Spirulina-dominated development within the UMS stream, C) small portion of unknown Oscillatoria-like filaments, D) Anabaena-like chains, E) Oscillatoria-like filaments; F) Spirulina-like filaments; G) Chlorococcum-like oxygenic phototroph; H) Amphora-like diatoms, I) Dermocarpa-like oxygenic phototroph, J) Thiothrix-like filaments; K) Chloroflexus-like filaments, L) Rhodobacter capsulatus (98.0%),
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