[en] The role of culture conditions on the production of exopolymeric substances (EPS) by Synechococcus strain PCC7942 was investigated. Carbonate mineral precipitation in these EPS was assessed in forced precipitation experiments. Cultures were grown in HEPES-buffered medium and non-buffered medium. The pH of buffered medium remained constant at 7.5, but in non-buffered medium it increased to 9.5 within a day and leveled off at 10.5. The cell yield at harvest was twice as high in non-buffered medium than in buffered medium. High molecular weight (>10 kDa) and low molecular weight (3–10 kDa) fractions of EPS were obtained from both cultures. The cell-specific EPS production in buffered medium was twice as high as in non-buffered medium. EPS from non-buffered cultures contained more negatively charged macromolecules and more proteins than EPS from buffered cultures. The higher protein content at elevated pH may be due to the induction of carbon-concentrating mechanisms, necessary to perform photosynthetic carbon fixation in these conditions. Forced precipitation showed smaller calcite carbonate crystals in EPS from non-buffered medium and larger minerals in polymers from buffered medium. Vaterite formed only at low EPS concentrations. Experimental results are used to conceptually model the impact of pH on the potential of cyanobacterial blooms to produce minerals. We hypothesize that in freshwater systems, small crystal production may benefit the picoplankton by minimizing the mineral ballast, and thus prolonging the residence time in the photic zone, which might result in slow sinking rates.
Raven, J. The Twelfth Tansley Lecture. Small Is Beautiful: The Picophytoplankton. Funct. Ecol. 1998, 12, 503–513. [CrossRef]
Ridgwell, A.; Zeebe, R.E. The Role of the Global Carbonate Cycle in the Regulation and Evolution of the Earth System. Earth Planet. Sci. Lett. 2005, 234, 299–315. [CrossRef]
Ivanikova, N.V.; Popels, L.C.; McKay, R.M.L.; Bullerjahn, G.S. Lake Superior Supports Novel Clusters of Cyanobacterial Picoplankton. Appl. Environ. Microbiol. 2007, 73, 4055–4065. [CrossRef] [PubMed]
Falkowski, P.G. The Role of Phytoplankton Photosynthesis in Global Biogeochemical Cycles. Photosynth. Res. 1994, 39, 235–258. [CrossRef] [PubMed]
Falkowski, P.G.; Barber, R.T.; Smetacek, V. Biogeochemical Controls and Feedbacks on Ocean Primary Production. Science 1998, 281, 200–206. [CrossRef] [PubMed]
Agawin, N.S.; Duarte, C.M.; Agustí, S. Nutrient and Temperature Control of the Contribution of Picoplankton to Phytoplankton Biomass and Production. Limnol. Oceanogr. 2000, 45, 591–600. [CrossRef]
Coello-Camba, A.; Agustí, S. Picophytoplankton Niche Partitioning in the Warmest Oligotrophic Sea. Front. Mar. Sci. 2021, 8, 429. [CrossRef]
Pomar, L.; Hallock, P. Carbonate Factories: A Conundrum in Sedimentary Geology. Earth-Sci. Rev. 2008, 87, 134–169. [CrossRef]
Kranz, S.A.; Gladrow, D.W.-; Nehrke, G.; Langer, G.; Rosta, B. Calcium Carbonate Precipitation Induced by the Growth of the Marine Cyanobacteria Trichodesmium. Limnol. Oceanogr. 2010, 55, 2563–2569. [CrossRef]
Buick, R. When Did Oxygenic Photosynthesis Evolve? Philos. Trans. R. Soc. B Biol. Sci. 2008, 363, 2731–2743. [CrossRef]
Blankenship, R.E.; Hartman, H. The Origin and Evolution of Oxygenic Photosynthesis. Trends Biochem. Sci. 1998, 23, 94–97. [CrossRef]
Berman-Frank, I.; Lundgren, P.; Falkowski, P. Nitrogen Fixation and Photosynthetic Oxygen Evolution in Cyanobacteria. Res. Microbiol. 2003, 154, 157–164. [CrossRef]
Knoll, A.H. Cyanobacteria and Earth History. Cyanobacteria Mol. Biol. Genom. Evol. 2008, 484, 1–19.
Hoehler, T.M.; Bebout, B.M.; Des Marais, D.J. The Role of Microbial Mats in the Production of Reduced Gases on the Early Earth. Nature 2001, 412, 324–327. [CrossRef]
Uyeda, J.C.; Harmon, L.J.; Blank, C.E. A Comprehensive Study of Cyanobacterial Morphological and Ecological Evolutionary Dynamics through Deep Geologic Time. PLoS ONE 2016, 11, e0162539. [CrossRef]
Arrigo, K.R. Marine Microorganisms and Global Nutrient Cycles. Nature 2005, 437, 349–355. [CrossRef]
Litchman, E.; de Tezanos Pinto, P.; Edwards, K.F.; Klausmeier, C.A.; Kremer, C.T.; Thomas, M.K. Global Biogeochemical Impacts of Phytoplankton: A Trait-based Perspective. J. Ecol. 2015, 103, 1384–1396. [CrossRef]
Buitenhuis, E.T.; Li, W.K.; Vaulot, D.; Lomas, M.; Landry, M.; Partensky, F.; Karl, D.; Ulloa, O.; Campbell, L.; Jacquet, S. Picophytoplankton Biomass Distribution in the Global Ocean. Earth Syst. Sci. Data 2012, 4, 37–46. [CrossRef]
Robbins, L.; Tao, Y.; Evans, C. Temporal and Spatial Distribution of Whitings on Great Bahama Bank and a New Lime Mud Budget. Geology 1997, 25, 947–950. [CrossRef]
Schultze-Lam, S.; Schultze-Lam, S.; Beveridge, T.J.; Des Marais, D.J. Whiting Events: Biogenic Origin Due to the Photosynthetic Activity of Cyanobacterial Picoplankton. Limnol. Oceanogr. 1997, 42, 133–141. [CrossRef]
Thompson, J.B.; Ferris, F.G. Cyanobacterial Precipitation of Gypsum, Calcite, and Magnesite from Natural Alkaline Lake Water. Geology 1990, 18, 995. [CrossRef]
Danckwerts, P.; Melkersson, K.-A. Kinetics of the Conversion of Bicarbonate to Carbon Dioxide. Trans. Faraday Soc. 1962, 58, 1832–1838. [CrossRef]
Heywood, B.R.; Mann, S. Template-directed Nucleation and Growth of Inorganic Materials. Adv. Mater. 1994, 6, 9–20. [CrossRef]
Heywood, B.R.; Mann, S. Molecular Construction of Oriented Inorganic Materials: Controlled Nucleation of Calcite and Aragonite under Compressed Langmuir Monolayers. Chem. Mater. 1994, 6, 311–318. [CrossRef]
Mitchell, A.C.; Ferris, F.G. The Influence of Bacillus Pasteurii on the Nucleation and Growth of Calcium Carbonate. Geomicrobiol. J. 2006, 23, 213–226. [CrossRef]
Dupraz, C.; Reid, R.P.; Braissant, O.; Decho, A.W.; Norman, R.S.; Visscher, P.T. Processes of Carbonate Precipitation in Modern Microbial Mats. Earth-Sci. Rev. 2009, 96, 141–162. [CrossRef]
Kamennaya, N.; Ajo-Franklin, C.; Northen, T.; Jansson, C. Cyanobacteria as Biocatalysts for Carbonate Mineralization. Minerals 2012, 2, 338–364. [CrossRef]
Braissant, O.; Cailleau, G.; Dupraz, C.; Verrecchia, E.P. Bacterially Induced Mineralization of Calcium Carbonate in Terrestrial Environments: The Role of Exopolysaccharides and Amino Acids. J. Sediment. Res. 2003, 73, 485–490. [CrossRef]
Marvasi, M.; Visscher, P.T.; Casillas Martinez, L. Exopolymeric Substances (EPS) from Bacillus Subtilis: Polymers and Genes Encoding Their Synthesis. FEMS Microbiol. Lett. 2010, 313, 1–9. [CrossRef]
Dittrich, M.; Sibler, S. Calcium Carbonate Precipitation by Cyanobacterial Polysaccharides. Geol. Soc. Lond. Spec. Publ. 2010, 336, 51–63. [CrossRef]
Dupraz, C.; Visscher, P.T. Microbial Lithification in Marine Stromatolites and Hypersaline Mats. Trends Microbiol. 2005, 13, 429–438. [CrossRef] [PubMed]
Trichet, J.; Defarge, C. Non-Biologically Supported Organomineralization, Bulletin de l’Institut Océanographique (Monaco) Numéro Spécial 14; de l’Institut Oceanographique (Monaco): Monaco City, Monaco, 1995; 203–236.
Decho, A.W. Microbial Exopolymer Secretions in Ocean Environments: Their Role (s) in Food Webs and Marine Processes. Oceanogr. Mar. Biol. Annu. Rev. 1990, 28, 73–153.
Moreno, J.; Vargas, M.A.; Olivares, H.; Rivas, J.; Guerrero, M.G. Exopolysaccharide Production by the Cyanobacterium Anabaena sp. ATCC 33047 in Batch and Continuous Culture. J. Biotechnol. 1998, 60, 175–182. [CrossRef]
Simon, M.; Grossart, H.-P.; Schweitzer, B.; Ploug, H. Microbial Ecology of Organic Aggregates in Aquatic Ecosystems. Aquat. Microb. Ecol. 2002, 28, 175–211. [CrossRef]
Decho, A.W.; Gutierrez, T. Microbial Extracellular Polymeric Substances (EPSs) in Ocean Systems. Front. Microbiol. 2017, 8, 922. [CrossRef] [PubMed]
Tsuneda, S.; Aikawa, H.; Hayashi, H.; Yuasa, A.; Hirata, A. Extracellular Polymeric Substances Responsible for Bacterial Adhesion onto Solid Surface. FEMS Microbiol. Lett. 2003, 223, 287–292. [CrossRef]
Wang, L.-L.; Wang, L.-F.; Ren, X.-M.; Ye, X.-D.; Li, W.-W.; Yuan, S.-J.; Sun, M.; Sheng, G.-P.; Yu, H.-Q.; Wang, X.-K. PH Dependence of Structure and Surface Properties of Microbial EPS. Environ. Sci. Technol. 2012, 46, 737–744. [CrossRef]
Santschi, P.H.; Chin, W.-C.; Quigg, A.; Xu, C.; Kamalanathan, M.; Lin, P.; Shiu, R.-F. Marine Gel Interactions with Hydrophilic and Hydrophobic Pollutants. Gels 2021, 7, 83. [CrossRef]
Moore, K.R.; Gong, J.; Pajusalu, M.; Skoog, E.J.; Xu, M.; Feliz Soto, T.; Sojo, V.; Matreux, T.; Baldes, M.J.; Braun, D. A New Model for Silicification of Cyanobacteria in Proterozoic Tidal Flats. Geobiology 2021, 19, 438–449. [CrossRef]
Rossi, F.; De Philippis, R. Role of Cyanobacterial Exopolysaccharides in Phototrophic Biofilms and in Complex Microbial Mats. Life 2015, 5, 1218–1238. [CrossRef]
Bertilsson, S.; Jones Jr, J.B. Supply of Dissolved Organic Matter to Aquatic Ecosystems: Autochthonous Sources. In Aquatic Ecosystems; Elsevier: Amsterdam, The Netherlands, 2003; pp. 3–24.
Fisher, M.L.; Allen, R.; Luo, Y.; Curtiss III, R. Export of Extracellular Polysaccharides Modulates Adherence of the Cyanobacterium Synechocystis. PLoS ONE 2013, 8, e74514. [CrossRef] [PubMed]
Hoiczyk, E. A Molecular Motor for Gliding Motility in Cyanobacteria. J. Phycol. 2000, 36, 30–31. [CrossRef]
Billi, D.; Potts, M. Life and Death of Dried Prokaryotes. Res. Microbiol. 2002, 153, 7–12. [CrossRef]
Ehling-Schulz, M.; Scherer, S. UV Protection in Cyanobacteria. Eur. J. Phycol. 1999, 34, 329–338. [CrossRef]
De Philippis, R.; Vincenzini, M. Exocellular Polysaccharides from Cyanobacteria and Their Possible Applications. FEMS Microbiol. Rev. 1998, 22, 151–175. [CrossRef]
Deng, W.; Cruz, B.N.; Neuer, S. Effects of Nutrient Limitation on Cell Growth, TEP Production and Aggregate Formation of Marine Synechococcus. Aquat. Microb. Ecol. 2016, 78, 39–49. [CrossRef]
Pannard, A.; Pedrono, J.; Bormans, M.; Briand, E.; Claquin, P.; Lagadeuc, Y. Production of Exopolymers (EPS) by Cyanobacteria: Impact on the Carbon-to-Nutrient Ratio of the Particulate Organic Matter. Aquat. Ecol. 2016, 50, 29–44. [CrossRef]
Bemal, S.; Anil, A.C. Effects of Salinity on Cellular Growth and Exopolysaccharide Production of Freshwater Synechococcus Strain CCAP1405. J. Plankton Res. 2018, 40, 46–58. [CrossRef]
Li, D.; Wu, N.; Tang, S.; Su, G.; Li, X.; Zhang, Y.; Wang, G.; Zhang, J.; Liu, H.; Hecker, M. Factors Associated with Blooms of Cyanobacteria in a Large Shallow Lake, China. Environ. Sci. Eur. 2018, 30, 27. [CrossRef]
Zepernick, B.N.; Gann, E.R.; Martin, R.M.; Pound, H.L.; Krausfeldt, L.E.; Chaffin, J.D.; Wilhelm, S.W. Elevated PH Conditions Associated With Microcystis spp. Blooms Decrease Viability of the Cultured Diatom Fragilaria Crotonensis and Natural Diatoms in Lake Erie. Front. Microbiol. 2021, 12, 188. [CrossRef]
Passow, U. Transparent Exopolymer Particles (TEP) in Aquatic Environments. Prog. Oceanogr. 2002, 55, 287–333. [CrossRef]
Iuculano, F.; Mazuecos, I.P.; Reche, I.; Agustí, S. Prochlorococcus as a Possible Source for Transparent Exopolymer Particles (TEP). Front. Microbiol. 2017, 8, 709. [CrossRef] [PubMed]
Engel, A. Distribution of Transparent Exopolymer Particles (TEP) in the Northeast Atlantic Ocean and Their Potential Significance for Aggregation Processes. Deep Sea Res. Part I Oceanogr. Res. Pap. 2004, 51, 83–92. [CrossRef]
Callieri, C. Picophytoplankton in Freshwater Ecosystems: The Importance of Small-Sized Phototrophs. Freshw. Rev. 2008, 1, 1–28. [CrossRef]
Cruz, B.N.; Neuer, S. Heterotrophic Bacteria Enhance the Aggregation of the Marine Picocyanobacteria Prochlorococcus and Synechococcus. Front. Microbiol 2019, 10, 1864. [CrossRef]
Robbins, L.; Blackwelder, P. Biochemical and Ultrastructural Evidence for the Origin of Whitings: A Biologically Induced Calcium Carbonate Precipitation Mechanism. Geology 1992, 20, 464–468. [CrossRef]
Larson, E.B.; Mylroie, J.E. A Review of Whiting Formation in the Bahamas and New Models. Carbonates Evaporites 2014, 29, 337–347. [CrossRef]
Dittrich, M.; Obst, M. Are Picoplankton Responsible for Calcite Precipitation in Lakes? AMBIO 2004, 33, 6. [CrossRef]
Ohlendorf, C.; Sturm, M. Precipitation and Dissolution of Calcite in a Swiss High Alpine Lake. Arct. Antarct. Alp. Res. 2001, 33, 410–417. [CrossRef]
Schultze-Lam, S.; Harauz, G.; Beveridge, T. Participation of a Cyanobacterial S Layer in Fine-Grain Mineral Formation. J. Bacteriol. 1992, 174, 7971–7981. [CrossRef]
Dittrich, M.; Müller, B.; Mavrocordatos, D.; Wehrli, B. Induced Calcite Precipitation by Cyanobacterium Synechococcus. Acta Hydrochim. Hydrobiol. 2003, 31, 162–169. [CrossRef]
Lee, B.D.; Apel, W.A.; Walton, M.R. Screening of Cyanobacterial Species for Calcification. Biotechnol. Prog. 2004, 20, 1345–1351. [CrossRef] [PubMed]
Obst, M.; Dynes, J.J.; Lawrence, J.R.; Swerhone, G.D.W.; Benzerara, K.; Karunakaran, C.; Kaznatcheev, K.; Tyliszczak, T.; Hitchcock, A.P. Precipitation of Amorphous CaCO3 (Aragonite-like) by Cyanobacteria: A STXM Study of the Influence of EPS on the Nucleation Process. Geochim. Cosmochim. Acta 2009, 73, 4180–4198. [CrossRef]
Liang, A.; Paulo, C.; Zhu, Y.; Dittrich, M. CaCO3 Biomineralization on Cyanobacterial Surfaces: Insights from Experiments with Three Synechococcus Strains. Colloids Surf. B Biointerfaces 2013, 111, 600–608. [CrossRef] [PubMed]
Yates, K.K.; Robbins, L.L. Production of Carbonate Sediments by a Unicellular Green Alga. Am. Mineral. 1998, 83, 1503–1509. [CrossRef]
Allen, M.M. SIMPLE CONDITIONS FOR GROWTH OF UNICELLULAR BLUE-GREEN ALGAE ON PLATES 1, 2. J. Phycol. 1968, 4, 1–4. [CrossRef] [PubMed]
Rippka, R.; Deruelles, J.; Waterbury, J.B.; Herdman, M.; Stanier, R.Y. Generic Assignments, Strain Histories and Properties of Pure Cultures of Cyanobacteria. Microbiology 1979, 111, 1–61. [CrossRef]
Coates, J. Interpretation of Infrared Spectra, A Practical Approach. In Encyclopedia of Analytical Chemistry; Meyers, R.A., Ed.; John Wiley & Sons, Ltd.: Chichester, UK, 2006; p. a5606, ISBN 978-0-470-02731-8.
de Moreno, M.R.; Smith, J.F.; Smith, R.V. Silver Staining of Proteins in Polyacrylamide Gels: Increased Sensitivity through a Combined Coomassie Blue-Silver Stain Procedure. Anal. Biochem. 1985, 151, 466–470. [CrossRef]
Dubois, M.; Gilles, K.; Hamilton, J.; Rebers, P.; Smith, F. A Colorimetric Method for the Determination of Sugars. Nature 1951, 168, 167. [CrossRef]
DuBois, M.; Gilles, K.A.; Hamilton, J.K.; Rebers, P.A.; Smith, F. Colorimetric Method for Determination of Sugars and Related Substances. Anal. Chem. 1956, 28, 350–356. [CrossRef]
Masuko, T.; Minami, A.; Iwasaki, N.; Majima, T.; Nishimura, S.-I.; Lee, Y.C. Carbohydrate Analysis by a Phenol–Sulfuric Acid Method in Microplate Format. Anal. Biochem. 2005, 339, 69–72. [CrossRef] [PubMed]
Oudot, M.; Shir, I.B.; Schmidt, A.; Plasseraud, L.; Broussard, C.; Neige, P.; Marin, F. A Nature’s Curiosity: The Argonaut “Shell” and Its Organic Content. Crystals 2020, 10, 839. [CrossRef]
Morrissey, J.H. Silver Stain for Proteins in Polyacrylamide Gels: A Modified Procedure with Enhanced Uniform Sensitivity. Anal. Biochem. 1981, 117, 307–310. [CrossRef]
Wall, R.S.; Gyi, T.J. Alcian Blue Staining of Proteoglycans in Polyacrylamide Gels Using the “Critical Electrolyte Concentration” Approach. Anal. Biochem. 1988, 175, 298–299. [CrossRef]
Blake, D.C.; Russell, R.G. Demonstration of Lipopolysaccharide with O-Polysaccharide Chains among Different Heat-Stable Serotypes of Campylobacter Jejuni by Silver Staining of Polyacrylamide Gels. Infect. Immun 1993, 61, 5384–5387. [CrossRef] [PubMed]
Korenevsky, A.A.; Vinogradov, E.; Gorby, Y.; Beveridge, T.J. Characterization of the Lipopolysaccharides and Capsules of Shewanella spp. Appl. Environ. Microbiol. 2002, 68, 4653–4657. [CrossRef]
Marin, F.; Pereira, L.; Westbroek, P. Large-Scale Fractionation of Molluscan Shell Matrix. Protein Expr. Purif. 2001, 23, 175–179. [CrossRef]
Wheeler, A.; George, J.W.; Evans, C. Control of Calcium Carbonate Nucleation and Crystal Growth by Soluble Matrx of Oyster Shell. Science 1981, 212, 1397–1398. [CrossRef]
Kawaguchi, T.; Decho, A.W. ISOLATION AND BIOCHEMICAL CHARACTERIZATION OF EXTRACELLULAR POLYMERIC SECRETIONS (EPS) FROM MODERN SOFT MARINE STROMATOLITES (BAHAMAS) AND ITS INHIBITORY EFFECT ON CACO3 PRECIPITATION. Prep. Biochem. Biotechnol. 2002, 32, 51–63. [CrossRef]
Marin, F.; Corstjens, P.; de Gaulejac, B.; de Vrind-De Jong, E.; Westbroek, P. Mucins and Molluscan Calcification: Molecular Characterization of Mucoperlin, a Novel Mucin-like Protein from the Nacreous Shell Layer of the Fan Mussel Pinna Nobilis (Bivalvia, Pteriomorphia). J. Biol. Chem. 2000, 275, 20667–20675. [CrossRef]
Albeck, S.; Aizenberg, J.; Addadi, L.; Weiner, S. Interactions of Various Skeletal Intracrystalline Components with Calcite Crystals. J. Am. Chem. Soc. 1993, 115, 11691–11697. [CrossRef]
Barth, A. Infrared Spectroscopy of Proteins. Biochim. Biophys. Acta (BBA)-Bioenerg. 2007, 1767, 1073–1101. [CrossRef]
Kallas, T.; Castenholz, R.W. Rapid Transient Growth at Low PH in the Cyanobacterium Synechococcus sp. J. Bacteriol 1982, 149, 237–246. [CrossRef] [PubMed]
Giraldez-Ruiz, N.; Mateo, P.; Bonilla, I.; Fernandez-Piñas, F. The Relationship between Intracellular PH, Growth Characteristics and Calcium in the Cyanobacterium Anabaena sp. Strain PCC7120 Exposed to Low PH. New Phytol. 1997, 137, 599–605. [CrossRef]
Touloupakis, E.; Cicchi, B.; Benavides, A.M.S.; Torzillo, G. Effect of High PH on Growth of Synechocystis sp. PCC 6803 Cultures and Their Contamination by Golden Algae (Poterioochromonas sp.). Appl. Microbiol. Biotechnol. 2016, 100, 1333–1341. [CrossRef] [PubMed]
Kurian, D.; Phadwal, K.; Mäenpää, P. Proteomic Characterization of Acid Stress Response in Synechocystis sp. PCC 6803. Proteomics 2006, 6, 3614–3624. [CrossRef]
Zhang, L.-F.; Yang, H.-M.; Cui, S.-X.; Hu, J.; Wang, J.; Kuang, T.-Y.; Norling, B.; Huang, F. Proteomic Analysis of Plasma Membranes of Cyanobacterium Synechocystis sp. Strain PCC 6803 in Response to High PH Stress. J. Proteome Res. 2009, 8, 2892–2902. [CrossRef]
Dogsa, I.; Kriechbaum, M.; Stopar, D.; Laggner, P. Structure of Bacterial Extracellular Polymeric Substances at Different PH Values as Determined by SAXS. Biophys. J. 2005, 89, 2711–2720. [CrossRef]
De Philippis, R.; Sili, C.; Paperi, R.; Vincenzini, M. Exopolysaccharide-Producing Cyanobacteria and Their Possible Exploitation: A Review. J. Appl. Phycol. 2001, 13, 293–299. [CrossRef]
Pereira, S.; Zille, A.; Micheletti, E.; Moradas-Ferreira, P.; De Philippis, R.; Tamagnini, P. Complexity of Cyanobacterial Exopolysac-charides: Composition, Structures, Inducing Factors and Putative Genes Involved in Their Biosynthesis and Assembly. FEMS Microbiol. Rev. 2009, 33, 917–941. [CrossRef]
Pereira, S.B.; Mota, R.; Vieira, C.P.; Vieira, J.; Tamagnini, P. Phylum-Wide Analysis of Genes/Proteins Related to the Last Steps of Assembly and Export of Extracellular Polymeric Substances (EPS) in Cyanobacteria. Sci. Rep. 2015, 5, 14835. [CrossRef] [PubMed]
Phoenix, V.R.; Martinez, R.E.; Konhauser, K.O.; Ferris, F.G. Characterization and Implications of the Cell Surface Reactivity of Calothrix sp. Strain KC97. Appl. Environ. Microbiol. 2002, 68, 4827–4834. [CrossRef] [PubMed]
Fein, J.B.; Boily, J.-F.; Yee, N.; Gorman-Lewis, D.; Turner, B.F. Potentiometric Titrations of Bacillus Subtilis Cells to Low PH and a Comparison of Modeling Approaches. Geochim. Cosmochim. Acta 2005, 69, 1123–1132. [CrossRef]
Braissant, O.; Decho, A.W.; Dupraz, C.; Glunk, C.; Przekop, K.M.; Visscher, P.T. Exopolymeric Substances of Sulfate-Reducing Bacteria: Interactions with Calcium at Alkaline PH and Implication for Formation of Carbonate Minerals. Geobiology 2007, 5, 401–411. [CrossRef]
d’Abzac, P.; Bordas, F.; Joussein, E.; van Hullebusch, E.D.; Lens, P.N.; Guibaud, G. Metal Binding Properties of Extracellular Polymeric Substances Extracted from Anaerobic Granular Sludges. Environ. Sci. Pollut. Res. 2013, 20, 4509–4519. [CrossRef] [PubMed]
Lamelas, C.; Benedetti, M.; Wilkinson, K.J.; Slaveykova, V.I. Characterization of H+ and Cd2+ Binding Properties of the Bacterial Exopolysaccharides. Chemosphere 2006, 65, 1362–1370. [CrossRef] [PubMed]
Liu, H.; Fang, H.H. Characterization of Electrostatic Binding Sites of Extracellular Polymers by Linear Programming Analysis of Titration Data. Biotechnol. Bioeng. 2002, 80, 806–811. [CrossRef] [PubMed]
Silverstein, R.M.; Bassler, G.C. Spectrometric Identification of Organic Compounds. J. Chem. Educ. 1962, 39, 546. [CrossRef]
Stuart, B.H. Infrared Spectroscopy: Fundamentals and Applications; John Wiley & Sons: Hoboken, NJ, USA, 2004; ISBN 0-470-01113-0.
Parikh, A.; Madamwar, D. Partial Characterization of Extracellular Polysaccharides from Cyanobacteria. Bioresour. Technol. 2006, 97, 1822–1827. [CrossRef]
Babele, P.K.; Kumar, J.; Chaturvedi, V. Proteomic De-Regulation in Cyanobacteria in Response to Abiotic Stresses. Front. Microbiol. 2019, 10, 1315. [CrossRef]
Raven, J.A.; Beardall, J.; Sánchez-Baracaldo, P. The Possible Evolution and Future of CO2-Concentrating Mechanisms. J. Exp. Bot. 2017, 68, 3701–3716. [CrossRef] [PubMed]
Price, G.D.; Badger, M.R.; Box, P.O. Expression of Human Carbonic Anhydrase in the Cyanobacterium Synechococcus PCC7942 Creates a High CO2-Requiring Phenotype. Plant Physiol. 1989, 91, 9. [CrossRef] [PubMed]
Price, G.D.; Pengelly, J.J.; Forster, B.; Du, J.; Whitney, S.M.; von Caemmerer, S.; Badger, M.R.; Howitt, S.M.; Evans, J.R. The Cyanobacterial CCM as a Source of Genes for Improving Photosynthetic CO2 Fixation in Crop Species. J. Exp. Bot. 2013, 64, 753–768. [CrossRef] [PubMed]
Badger, M.R.; Price, G.D. The CO2concentrating Mechanism in Cyanobacteria and Microalgae. Physiol. Plant. 1992, 84, 606–615. [CrossRef]
Kupriyanova, E.V.; Sinetova, M.A.; Bedbenov, V.S.; Pronina, N.A.; Los, D.A. Putative Extracellular α-Class Carbonic Anhydrase, EcaA, of Synechococcus Elongatus PCC 7942 Is an Active Enzyme: A Sequel to an Old Story. Microbiology 2018, 164, 576–586. [CrossRef] [PubMed]
Chrachri, A.; Hopkinson, B.M.; Flynn, K.; Brownlee, C.; Wheeler, G.L. Dynamic Changes in Carbonate Chemistry in the Microenvironment around Single Marine Phytoplankton Cells. Nat. Commun. 2018, 9, 74. [CrossRef] [PubMed]
Badger, M.R.; Price, G.D. The Role of Carbonic Anhydrase in Photosynthesis. Annu. Rev. Plant Biol. 1994, 45, 369–392. [CrossRef]
Badger, M.R.; Price, G.D. Carbonic Anhydrase Activity Associated with the Cyanobacterium Synechococcus PCC7942. Plant Physiol. 1989, 89, 51–60. [CrossRef]
Kim, J.K.; Lee, C.; Lim, S.W.; Adhikari, A.; Andring, J.T.; McKenna, R.; Ghim, C.-M.; Kim, C.U. Elucidating the Role of Metal Ions in Carbonic Anhydrase Catalysis. Nat. Commun. 2020, 11, 4557. [CrossRef]
Jong, E.W.; Bosch, L.; Westbroek, P. Isolation and Characterization of a Cat2+-Binding Polysaccharide Associated with Coccoliths of Emiliania Huxleyi (Lohmann) Kamptner. Eur. J. Biochem. 1976, 70, 611–621. [CrossRef]
Gunthorpe, M.; Sikes, C.; Wheeler, A. Promotion and Inhibition of Calcium Carbonate Crystallization in Vitro by Matrix Protein from Blue Crab Exoskeleton. Biol. Bull. 1990, 179, 191–200. [CrossRef] [PubMed]
Yang, M.; Stipp, S.L.S.; Harding, J. Biological Control on Calcite Crystallization by Polysaccharides. Cryst. Growth Des. 2008, 8, 4066–4074. [CrossRef]
Walker, J.M.; Marzec, B.; Lee, R.B.Y.; Vodrazkova, K.; Day, S.J.; Tang, C.C.; Rickaby, R.E.M.; Nudelman, F. Polymorph Selectivity of Coccolith-Associated Polysaccharides from Gephyrocapsa Oceanica on Calcium Carbonate Formation In Vitro. Adv. Funct. Mater. 2019, 29, 1807168. [CrossRef]
Arp, G.; Reimer, A.; Reitner, J. Photosynthesis-Induced Biofilm Calcification and Calcium Concentrations in Phanerozoic Oceans. Science 2001, 292, 1701–1704. [CrossRef] [PubMed]
Hernández-Hernández, A.; Rodríguez-Navarro, A.B.; Gómez-Morales, J.; Jiménez-Lopez, C.; Nys, Y.; García-Ruiz, J.M. Influence of Model Globular Proteins with Different Isoelectric Points on the Precipitation of Calcium Carbonate. Cryst. Growth Des. 2008, 8, 1495–1502. [CrossRef]
Verrecchia, E.P.; Freytet, P.; Verrecchia, K.E.; Dumont, J.-L. Spherulites in Calcrete Laminar Crusts; Biogenic CaCO3 Precipitation as a Major Contributor to Crust Formation. J. Sediment. Res. 1995, 65, 690–700.
Saraya, M.E.-S.I.; Rokbaa, H.H.A.E.-L. Formation and Stabilization of Vaterite Calcium Carbonate by Using Natural Polysaccha-ride. Adv. Nanopart. 2017, 6, 158.
Costa, O.Y.; Raaijmakers, J.M.; Kuramae, E.E. Microbial Extracellular Polymeric Substances: Ecological Function and Impact on Soil Aggregation. Front. Microbiol. 2018, 9, 1636. [CrossRef]
McEwen, J.T.; Machado, I.M.; Connor, M.R.; Atsumi, S. Engineering Synechococcus Elongatus PCC 7942 for Continuous Growth under Diurnal Conditions. Appl. Environ. Microbiol. 2013, 79, 1668–1675. [CrossRef]
Cruz, D.; Vasconcelos, V.; Pierre, G.; Michaud, P.; Delattre, C. Exopolysaccharides from Cyanobacteria: Strategies for Bioprocess Development. Appl. Sci. 2020, 10, 3763. [CrossRef]
Morales, E.; Rodríguez, M.; García, D.; Loreto, C.; Marco, E. Crecimiento, Producción de Pigmentos y Exopolisacáridos de La Cianobacteria Anabaena sp. PCC 7120 En Función Del PH y CO2. Interciencia 2002, 27, 373–378.
De Farias Silva, C.E.; Sforza, E.; Bertucco, A. Effects of PH and Carbon Source on Synechococcus PCC 7002 Cultivation: Biomass and Carbohydrate Production with Different Strategies for PH Control. Appl. Biochem. Biotechnol. 2017, 181, 682–698. [CrossRef] [PubMed]
Kurian, N.; Hall, C.J.; Wilkinson, G.F.; Sullivan, M.; Tobin, A.B.; Willars, G.B. Full and Partial Agonists of Muscarinic M3 Receptors Reveal Single and Oscillatory Ca2+ Responses by B2-Adrenoceptors. J. Pharmacol. Exp. Ther. 2009, 330, 502–512. [CrossRef] [PubMed]
Kaplan, A.; Schwarz, R.; Lieman-Hurwitz, J.; Reinhold, L. Physiological and Molecular Aspects of the Inorganic Carbon-Concentrating Mechanism in Cyanobacteria. Plant Physiol. 1991, 97, 851–855. [CrossRef]
Maeda, S.; Price, G.D.; Badger, M.R.; Enomoto, C.; Omata, T. Bicarbonate Binding Activity of the CmpA Protein of the Cyanobac-terium Synechococcus sp. Strain PCC 7942 Involved in Active Transport of Bicarbonate. J. Biol. Chem. 2000, 275, 20551–20555. [CrossRef]
Gallagher, K.; Dupraz, C.; Braissant, O.; Norman, R.; Decho, A.; Visscher, P. Mineralization of Sedimentary Biofilms: Modern Mechanistic Insights. In Biofilm: Formation, Development and Properties.Bailley; Columbus, F., Ed.; Nova Science Publishers: Hauppauge, NY, USA, 2010; pp. 227–258.
Ibelings, B.W.; Maberly, S.C. Photoinhibition and the Availability of Inorganic Carbon Restrict Photosynthesis by Surface Blooms of Cyanobacteria. Limnol. Oceanogr. 1998, 43, 408–419. [CrossRef]
Verspagen, J.M.; Van de Waal, D.B.; Finke, J.F.; Visser, P.M.; Van Donk, E.; Huisman, J. Rising CO2 Levels Will Intensify Phytoplankton Blooms in Eutrophic and Hypertrophic Lakes. PLoS ONE 2014, 9, e104325.
Liao, J.; Zhao, L.; Cao, X.; Sun, J.; Gao, Z.; Wang, J.; Jiang, D.; Fan, H.; Huang, Y. Cyanobacteria in Lakes on Yungui Plateau, China Are Assembled via Niche Processes Driven by Water Physicochemical Property, Lake Morphology and Watershed Land-Use. Sci. Rep. 2016, 6, 36357. [CrossRef]
Hoiczyk, E.; Hansel, A. Cyanobacterial Cell Walls: News from an Unusual Prokaryotic Envelope. J. Bacteriol. 2000, 182, 1191–1199. [CrossRef]
De Philippis, R.; Sili, C.; Vincenzini, M. Response of an Exopolysaccharide-Producing Heterocystous Cyanobacterium to Changes in Metabolic Carbon Flux. J. Appl. Phycol. 1996, 8, 275–281. [CrossRef]
Dam, H.G.; Drapeau, D.T. Coagulation Efficiency, Organic-Matter Glues and the Dynamics of Particles during a Phytoplankton Bloom in a Mesocosm Study. Deep Sea Res. Part II: Top. Stud. Oceanogr. 1995, 42, 111–123. [CrossRef]
Passow, U. Formation of Transparent Exopolymer Particles, TEP, from Dissolved Precursor Material. Mar. Ecol. Prog. Ser. 2000, 192, 1–11. [CrossRef]
Callieri, C. Synechococcus Plasticity under Environmental Changes. FEMS Microbiol. Lett. 2017, 364, fnx229. [CrossRef]
Polowczyk, I.; Bastrzyk, A.; Fiedot, M. Protein-Mediated Precipitation of Calcium Carbonate. Materials 2016, 9, 944. [CrossRef]
Reynolds, C.S.; Oliver, R.L.; Walsby, A.E. Cyanobacterial Dominance: The Role of Buoyancy Regulation in Dynamic Lake Environments. N. Z. J. Mar. Freshw. Res. 1987, 21, 379–390. [CrossRef]
Dean, J.A. Lange’s Handbook of Chemistry; McGraw-Hill: New York, NY, USA, 1999; ISBN 0-07-016384-7.
Azetsu-Scott, K.; Passow, U. Ascending Marine Particles: Significance of Transparent Exopolymer Particles (TEP) in the Upper Ocean. Limnol. Oceanogr. 2004, 49, 741–748. [CrossRef]
Thornton, D.C. Phytoplankton Mucilage Production in Coastal Waters: A Dispersal Mechanism in a Front Dominated System? Ethol. Ecol. Evol. 1999, 11, 179–185. [CrossRef]
Bach, L.T.; Stange, P.; Taucher, J.; Achterberg, E.P.; Algueró-Muñiz, M.; Horn, H.; Esposito, M.; Riebesell, U. The Influence of Plankton Community Structure on Sinking Velocity and Remineralization Rate of Marine Aggregates. Glob. Biogeochem. Cycles 2019, 33, 971–994. [CrossRef]
Schmidt, I.; Wagermaier, W. Tailoring Calcium Carbonate to Serve as Optical Functional Material: Examples from Biology and Materials Science. Adv. Mater. Interfaces 2017, 4, 1600250. [CrossRef]
Grossart, H.; Simon, M. Limnetic Macroscopic Organic Aggregates (Lake Snow): Occurrence, Characteristics, and Microbial Dynamics in Lake Constance. Limnol. Oceanogr. 1993, 38, 532–546. [CrossRef]