OJE  Vol.4 No.8 , May 2014
Abundance and Diversity of the Phototrophic Microbial Mat Communities of Sulphur Mountain Banff Springs and Their Significance to the Endangered Snail, Physella johnsoni
Abstract: Seasonal population fluctuations and diversity of anoxygenic phototrophs and cyanobacteria at the Sulphur Mountain thermal springs, Banff, Canada were investigated and compared to drastic population changes of the endangered snail Physella johnsoni. The microbial community revealed new species of anoxygenic phototrophic bacteria with novel spectral and morphological characteristics. Major mat-forming organisms included densely growing Thiothrix-like species, oxygenic phototrophs of the genera Spirulina, Oscillatoria, and Phormidium and purple nonsulfur bacteria Rhodobacter, Rhodopseudomonas and Rhodomicrobium. Aerobic anoxygenic phototrophs comprised a significant portion, upwards of 9.6 × 104 CFU/cm2 of mat or 18.9% of total aerobic heterotrophic isolates, while PNSB and purple sulfur bacteria were quantified at maximum abundance of 3.2 × 105 and 2.0 × 106 CFU/cm2 of mat, respectively. Photosynthetic activity revealed incredibly productive carbon fixation rates, averaging 40.5 mg C/cm2/day at one studied spring system. A temporal mismatch was observed for mat area and available organics to the fluctuation of P. johnsoni population in a tracking inertia manner. Mat chlorophyll a content appeared directly proportional to snail numbers making it an appropriate indicator of population. This survey of the Sulphur springs microbial communities suggests that phototrophic species are among the main determinants to the proliferation of P. johnsoni.
Cite this paper: Bilyj, M. , Lepitzki, D. , Hughes, E. , Swiderski, J. , Stackebrandt, E. , Pacas, C. and Yurkov, V. (2014) Abundance and Diversity of the Phototrophic Microbial Mat Communities of Sulphur Mountain Banff Springs and Their Significance to the Endangered Snail, Physella johnsoni. Open Journal of Ecology, 4, 488-516. doi: 10.4236/oje.2014.48041.

[1]   Grasby, S.E. and Lepitzki, D.A.W. (2002) Physical and Chemical Properties of the Sulphur Mountain Thermal Springs, Banff National Park and Implications for Endangered Snails. Canadian Journal of Earth Sciences, 39, 1349-1361.

[2]   Grasby, S.E., Hutcheon, I. and Krouse, H.R. (2000) The Influence of Water-Rock Interaction on the Chemistry of Thermal Springs in Western Canada. Applied Geochemistry, 15, 439-454.

[3]   Lepitzki, D.A.W. (2007) Ten-Plus-Year Data Summary for the Banff Springs Snail. A Report in Partial Fulfillment of the Requirements of Contract 07-0055. Wildlife Status Report, Wildlife Systems Research, Banff, 134.

[4]   Clench, W.J. (1926) Three New Species of Physa. Occasional Papers of the Museum of Zoology, University of Michigan, Ann Arbor, 168, 1-8.

[5]   Lepitzki, D.A.W. (2002) Status of the Banff Springs Snail (Physella johnsoni) in Alberta. Wildlife Status Report, Alberta Sustainable Resource Development, Fish and Wildlife Division and Alberta Conservation Association, Edmonton, 29.

[6]   Danger, M., Lacroix, G., Oumarou, C., Benest, D. and Meriguet, J. (2008) Effects of Food-Web Structure on Periphyton Stoichiometry in Eutrophic Lakes: A Mesocosm Study. Freshwater Biology, 53, 2089-2100.

[7]   Overmann, J., Beatty, J.T. and Hall, K.J. (1996) Purple Sulfur Bacteria Control the Growth of Aerobic Heterotrophic Bacterioplankton in a Meromictic Salt Lake. Applied and Environmental Microbiology, 62, 3251-3258.

[8]   Ludwig, R., Pringault, O., De Wit, R., De Beer, D. and Jonkers, H.M. (2006) Limitation of Oxygenic Photosynthesis and Oxygen Consumption by Phosphate and Organic Nitrogen in a Hypersaline Mat: A Microsensor Study. FEMS Microbiology Ecology, 57, 9-17.

[9]   Freeman, C. and Lock, M.A. (1995) The Biofilm Polysaccharide Matrix: A Buffer against Changing Organic Substrate Supply. Limnology and Oceanography, 40, 273-278.

[10]   Lawrence, J.R., Scharf, B., Packroff, G. and Neu, T.R. (2002) Microscale Evaluation of the Effects of Grazing by Invertebrates with Contrasting Feeding Modes on River Biofilm Architecture and Composition. Microbial Ecology, 44, 199-207.

[11]   Roeselers, G., Loosdrecht, M.C. and Muyzer, G. (2008) Phototrophic Biofilms and Their Potential Applications. Journal of Applied Phycology, 20, 227-235.

[12]   McGregor, G.B. and Rasmussen, J.P. (2008) Cyanobacterial Composition of Microbial Mats from an Australian Thermal Spring: A Polyphasic Evaluation. FEMS Microbiology Ecology, 63, 23-35.

[13]   Mishra, A. and Jha, B. (2009) Isolation and Characterization of Extracellular Polymeric Substances from Micro-Algae Dunaliella salina under Salt Stress. Bioresource Technology, 100, 3382-3386.

[14]   Parikh, A. and Madamwar, D. (2006) Partial Characterization of Extracellular Polysaccharides from Cyanobacteria. Bioresource Technology, 97, 1822-1827.

[15]   Stal, L.J. (1995) Physiological Ecology of Cyanobacteria in Microbial Mats and Other Communities. New Phytologist, 131, 1-32.

[16]   Stewart, P.S. and Franklin, M.J. (2008) Physiological Heterogeneity in Biofilms. Nature Reviews Microbiology, 6, 199-210.

[17]   Bender, J. and Phillips, P. (2004) Microbial Mats for Multiple Applications in Aquaculture and Bioremediation. Bioresource Technology, 94, 229-238.

[18]   Freeman, C., Chapman, P.J., Gilman, K., Lock, M.A., Reynolds, B. and Wheater, H.S. (1995) Ion-Exchange Mechanisms and the Entrapment of Nutrients by River Biofilms. Hydrobiologia, 297, 61-65.

[19]   van Gemerden, H. (1993) Microbial Mats: A Joint Venture. Marine Geology, 113, 3-25.

[20]   Yurkov, V. and van Gemerden, H. (1993) Abundance and Salt Tolerance of Obligately Aerobic, Phototrophic Bacteria in a Marine Microbial Mat. Netherlands Journal of Sea Research, 31, 57-62.

[21]   Drews, G., Peters, J. and Dierstein, R. (1983) Molecular Organization and Biosynthesis of Pigment-Protein Complexes of Rhodopseudomonas capsulata. Annales de l’Institut Pasteur/Microbiologie, 134, 151-158.

[22]   Yurkov, V.V., Krieger, S., Stackebrandt, E. and Beatty, J.T. (1999) Citromicrobium bathyomarinum, a Novel Aerobic Bacterium Isolated from Deep-Sea Hydrothermal Vent Plume Waters that Contains Photosynthetic Pigment-Protein Complexes. Journal of Bacteriology, 181, 4517-4525.

[23]   SCOR-UNESCO (1966) Determination of Photosynthetic Pigments. Monographs on Oceanographic Methodology 1, 11-18.

[24]   Waterbury, J. (1992) The Cyanobacteria—Isolation, Purification and Identification. In: Dworkin, M. and Falkow, S., Eds., The Prokaryotes. A Handbook on the Biology of Bacteria: Ecophysiology, Isolation, Identification, Applications, Springer, New York, 2058-2104.

[25]   Hanada, S., Hiraishi, A., Shimada, K. and Matsuura, K. (1995) Isolation of Chloroflexus aurantiacus and Related Thermophilic Phototrophic Bacteria from Japanese Hot Springs Using an Improved Isolation Procedure. Journal of General and Applied Microbiology, 41, 119-130.

[26]   Steemann Nielsen, E. (1952) Use of Radioactive Carbon (C14) for Measuring Organic Production in the Sea. Journal of the International Council for the Exploration of the Sea, 43, 117-140.

[27]   Franson, M.A.H. (1998) Standard Methods for the Examination of Water and Wastewater. 20th Edition, American Public Health Association, Washington DC.

[28]   Rathgeber, C., Yurkova, N., Stackebrandt, E., Schumann, P., Beatty, J.T. and Yurkov, V. (2005) Roseicyclus mahoneyensis gen. nov., sp nov., an Aerobic Phototrophic Bacterium Isolated from a Meromictic Lake. International Journal of Systematic and Evolutionary Microbiology, 55, 1597-1603.

[29]   Rainey, F.A., Ward-Rainey, N., Kroppenstedt, R.M. and Stackebrandt, E. (1996) The Genus Nocardiopsis Represents a Phylogenetically Coherent Taxon and a Distinct Actinomycete Lineage: Proposal of Nocardiopsaceae fam. nov. International Journal of Systematic and Evolutionary Microbiology, 46, 1088-1092.

[30]   Lepitzki, D.A.W. and Pacas, C. (2007) Recovery Strategy and Action Plan for the Banff Springs Snail (Physella johnsoni), in Canada. Species at Risk Act Recovery Strategy Series. Parks Canada Agency, Ottawa, 61.

[31]   Cohen, Y. and Gurevitz, M. (2006) The Cyanobacteria—Ecology, Physiology and Molecular Genetics. In: Dworkin, M. and Falkow, S., Eds., The Prokaryotes, Vol. 1, Symbiotic Associations, Biotechnology, Applied Microbiology a Handbook on the Biology of Bacteria, Springer-Verlag, New York, 1074-1098.

[32]   Geider, R.J. (1987) Light and Temperature Dependence of the Carbon to Chlorophyll a Ratio in Microalgae and Cyanobacteria: Implications for Physiology and Growth of Phytoplankton. New Phytologist, 106, 1-34.

[33]   Post, A.F., Dewit, R. and Mur, L.R. (1985) Interactions between Temperature and Light Intensity on Growth and Photosynthesis of the Cyanobacterium Oscillatoria agardhii. Journal of Plankton Research, 7, 487-495.

[34]   Pierson, B.K., Sands, V.M. and Frederick, J.L. (1990) Spectral Irradiance and Distribution of Pigments in a Highly Layered Marine Microbial Mat. Applied and Environmental Microbiology, 56, 2327-2340.

[35]   Stal, L., van Gemerden, H. and Krumbein, W.E. (1985) Structure and Development of a Benthic Marine Microbial Mat. FEMS Microbiology Letters, 31, 111-125.

[36]   Yurkov, V. and Beatty, J.T. (1998) Aerobic Anoxygenic Phototrophic Bacteria. Microbiology and Molecular Biology Reviews, 62, 695-724.

[37]   Hanada, S., Kawase, Y., Hiraishi, A., Takaichi, S., Matsuura, K., Shimada, K. and Nagashima, K.V. (1997) Porphyrobacter tepidarius sp. nov., a Moderately Thermophilic Aerobic Photosynthetic Bacterium Isolated from a Hot Spring. International Journal of Systematic and Evolutionary Microbiology, 47, 408-413.

[38]   Yurkov, V., Stackebrandt, E., Holmes, A., Fuerst, J.A., Hugenholtz, P., Golecki, J., Gad’on, N., Gorlenko, V.M., Kompantseva, E.I. and Drews, G. (1994) Phylogenetic Positions of Novel Aerobic, Bacteriochlorophyll α-Containing Bacteria and Description of Roseococcus thiosulfatophilus gen. nov., sp. nov., Erythromicrobium ramosum gen. nov., sp. nov., and Erythrobacter litoralis sp. nov. International Journal of Systematic and Evolutionary Microbiology, 44, 427-434.

[39]   Saitoh, S., Suzuki, T. and Nishimura, Y. (1998) Proposal of Craurococcus roseus gen. nov., sp. nov. and Paracraurococcus ruber gen. nov., sp. nov., Novel Aerobic Bacteriochlorophyll α-Containing Bacteria from Soil. International Journal of Systematic and Evolutionary Microbiology, 48, 1043-1047.

[40]   Segers, P., Vancanneyt, M., Pot, B., Torck, U., Hoste, B., Dewettinck, D., Falsen, E., Kersters, K. and De Vos, P. (1994) Classification of Pseudomonas diminuta Leifson and Hugh 1954 and Pseudomonas vesicularis Busing, Doll and Freytag 1953 in Brevundimonas gen. nov. as Brevundimonas diminuta comb. nov. and Brevundimonas vesicularis comb. nov., Respectively. International Journal of Systematic and Evolutionary Microbiology, 44, 499-510.

[41]   Britton, G., Brown, D.J., Goodwin, T.W., Leuenberger, F.J. and Schocher, A.J. (1977) The Carotenoids of Flavobacterium Strain R1560. Archives of Microbiology, 113, 33-37.

[42]   Ouchane, S., Steunou, A.S., Picaud, M. and Astier, C. (2004) Aerobic and Anaerobic Mg-Protoporphyrin Monomethyl ester Cyclases in Purple Bacteria: A Strategy Adopted to Bypass the Repressive Oxygen Control System. Journal of Biological Chemistry, 279, 6385-6394.

[43]   Imhoff, J.F. (2005) Genus I. Rhodobacter. In: Brenner, D.J., Krieg, N.R. and Staley, J.T., Eds., Bergey’s Manual of Systematic and Determinative Bacteriology, Springer, New York, 161-167.

[44]   Imhoff, J.F. (2005) Genus XVI. Rhodomicrobium. In: Brenner, D.J., Krieg, N.R. and Staley, J.T., Eds., Bergey’s Manual of Systematic and Determinative Bacteriology, Springer, New York, 543-454.

[45]   Evans, K., Fordham-Skelton, A.P., Mistry, H., Reynolds, C.D., Lawless, A.M. and Papiz, M.Z. (2005) A Bacteriophytochrome Regulates the Synthesis of LH4 Complexes in Rhodopseudomonas palustris. Photosynthesis Research, 85, 169-180.

[46]   Pfennig, N. (1989) Green Sulfur Bacteria. In: Staley, J.T., Bryant, M.P., Pfennig, N. and Holt, J.G., Eds., Bergey’s Manual of Systematic Bacteriology, Williams and Wilkins, Baltimore, 1682-1697.

[47]   Imhoff, J.F. (2003) Phylogenetic Taxonomy of the Family Chlorobiaceae on the Basis of 16S rRNA and fmo (FennaMatthews-Olson Protein) Gene Sequences. International Journal of Systematic and Evolutionary Microbiology, 53, 941-951.

[48]   Asao, M., Takaichi, S. and Madigan, M.T. (2007) Thiocapsa imhoffii, sp. nov., an Alkaliphilic Purple Sulfur Bacterium of the Family Chromatiaceae from Soap Lake, Washington (USA). Archives of Microbiology, 188, 665-675.

[49]   Puchkova, N.N., Imhoff, J.F. and Gorlenko, V.M. (2000) Thiocapsa litoralis sp. nov., a New Purple Sulfur Bacterium from Microbial Mats from the White Sea. International Journal of Systematic and Evolutionary Microbiology, 50, 1441-1447.

[50]   Ananyev, G., Carrieri, D. and Dismukes, G.C. (2008) Optimization of Metabolic Capacity and Flux through Environmental Cues to Maximize Hydrogen Production by the Cyanobacterium Arthrospira (Spirulina) maxima. Applied and Environmental Microbiology, 74, 6102-6113.

[51]   Cohen, Z., Vonshak, A. and Richmond, A. (1987) Fatty Acid Composition of Spirulina Strains Grown under Various Environmental Conditions. Phytochemistry, 26, 2255-2258.

[52]   Lu, C. and Vonshak, A. (2002) Effects of Salinity Stress on Photosystem II Function in Cyanobacterial Spirulina platensis Cells. Physiologia Plantarum, 114, 405-413.

[53]   Gitelson, A., Qiuang, H. and Richmond, A. (1996) Photic Volume in Photobioreactors Supporting Ultrahigh Population Densities of the Photoautotroph Spirulina platensis. Applied and Environmental Microbiology, 62, 1570-1573.

[54]   Lemasson, C., Tandeaud, N. and Cohenbaz, G. (1973) Role of Allophycocyanin as a Light Harvesting Pigment in Cyanobacteria. Proceedings of the National Academy of Sciences of the United States of America, 70, 3130-3133.

[55]   Graham, M.H. and Mitchell, B.G. (1999) Obtaining Absorption Spectra from Individual Macroalgal Spores Using Microphotometry. Hydrobiologia, 399, 231-239.

[56]   Bauld, J. (1984) Microbial Mats in Marginal Marine Environments: Shark Bay, Western Australia and Spencer Gulf, South Australia. MBL (Marine Biology Laboratory) Lectures in Biology, 3, 39-58.

[57]   Namsaraev, Z.B., Gorlenko, V.M., Namsaraev, B.B., Buryukhaev, S.P. and Yurkov, V.V. (2003) The Structure and Biogeochemical Activity of the Phototrophic Communities from the Bol’sherechenskii Alkaline Hot Spring. Microbiology, 72, 193-202.

[58]   Casamayor, E.O., Garcia-Cantizano, J., Mas, J. and Pedros-Alio, C. (2001) Primary Production in Estuarine Oxic/Anoxic Interfaces: Contribution of Microbial Dark CO2 Fixation in the Ebro River Salt Wedge Estuary. Marine Ecology Progress Series, 215, 49-56.

[59]   Bryanskaya, A.V., Namsaraev, Z.B., Kalashnikova, O.M., Barkhutova, D.D., Namsaraev, B.B. and Gorlenko, V.M. (2006) Biogeochemical Processes in Algal-Bacterial Mats of the Urinskii Alkaline Hot Spring. Microbiology, 75, 611-620.

[60]   Romani, A.M. and Sabater, S. (1999) Effect of Primary Producers on the Heterotrophic Metabolism of a Stream Biofilm. Freshwater Biology, 41, 729-736.

[61]   Espeland, E.M. and Wetzel, R.G. (2001) Effects of Photosynthesis on Bacterial Phosphatase Production in Biofilms. Microbial Ecology, 42, 328-337.

[62]   Kawata, M., Hayashi, M. and Hara, T. (2001) Interactions between Neighboring Algae and Snail Grazing in Structuring Microdistribution Patterns of Periphyton. Oikos, 92, 404-416.

[63]   King-Lotufo, E.C., Brown, K.M. and Carman, K.R. (2002) The Influence of Periphyton Biomass and Density on Grazing in Physella virgata. Hydrobiologia, 482, 23-29.

[64]   Liess, A. and Haglund, A.L. (2007) Periphyton Responds Differentially to Nutrients Recycled in Dissolved or Faecal Pellet form by the Snail Grazer Theodoxus fluviatilis. Freshwater Biology, 52, 1997-2008.

[65]   Feminella, J. (1995) Interactions between Stream Herbivores and Periphyton: A Quantitative Analysis of Past Experiments. Journal of the North American Benthological Society, 14, 465-509.

[66]   Solbreck, C. and Sillen-Tullberg, B. (1986) Seed Production and Seed Predation in a Patchy and Time-Varying Environment. Dynamics of a Milkweed-Tephritid Fly System. Oecologia, 71, 51-58.

[67]   Crowl, T.A. and Covich, A.P. (1990) Predator Induced Life History Shifts in a Freshwater Snail. Science, 247, 949-951.

[68]   Sheldon, F. and Walker, K.F. (1997) Changes in Biofilms Induced by Flow Regulation Could Explain Extinctions of Aquatic Snails in the Lower River Murray, Australia. Hydrobiologia, 347, 97-108.

[69]   McCollum, E.W., Crowder, L.B. and McCollum, S.A. (1998) Complex Interactions of Fish, Snails and Littoral Zone Periphyton. Ecology, 79, 1980-1994.[1980:CIOFSA]2.0.CO;2

[70]   Sharfstein, B. and Steinman, A.D. (2001) Growth and Survival of the Florida Apple Snail (Pomacea paludosa) Fed Three Naturally Occurring Macrophyte Assemblages. Journal of the North American Benthological Society, 20, 84-95.