[en] Abstract. Extracellular polymeric substances (EPSs) are an important organic carbon reservoir in many pelagic and benthic environments. The production of EPS
is intimately associated with the growth of phyto- and picoplankton. EPS plays a critical role in carbonate precipitation through the binding of
cations and by acting as a nucleation site for minerals. Large-scale episodes of fine-grained calcium carbonate precipitation in the water column
(whiting events) have been linked to cyanobacterial blooms, including of Synechococcus spp. The mechanisms that trigger these precipitation
events are still debated. We pose that the cyanobacterial EPS, produced during exponential and stationary growth phases, plays a critical role in the
formation of whitings. The aim of this study was to investigate the production of EPS during a 2-month cyanobacterial growth, mimicking a
bloom. The production and characteristics of EPS were examined in different growth stages of Synechococcus spp. using various techniques
such as Fourier transform infrared (FT-IR) spectroscopy as well as colorimetric and sodium dodecyl sulfate–polyacrylamide gel electrophoresis (SDS–PAGE) assays. We further evaluated the potential role of EPS in carbonate precipitation through
in vitro-forced precipitation experiments. EPS produced during the early and late stationary
phase contained a larger amount of negatively charged groups than present in EPS produced during the exponential phase. Consequently, a higher
Ca2+-binding affinity of the stationary-phase EPS led to the formation of a larger amount of smaller carbonate minerals
(< 50 µm) compared to crystals formed in exponential-phase EPS, which were less abundant and larger (> 50 µm). These
findings were used to establish a conceptual model for picoplankton-bloom-mediated CaCO3 precipitation that can explain the role of EPS in
whitings.
Addadi, L. and Weiner, S.: Interactions between acidic proteins and crystals: stereochemical requirements in biomineralization, P. Natl. Acad. Sci. USA, 82, 4110–4114, 1985.
Agawin, N., Duarte, C., and Agustí, S.: Growth and abundance of Synechococcus sp. in a Mediterranean Bay: seasonality and relationship with temperature, Mar. Ecol.-Prog. Ser., 170, 45–53, https://doi.org/10.3354/meps170045, 1998.
Aizawa, K. and Miyachi, S.: Carbonic anhydrase and CO2 concentrating mechanisms in microalgae and cyanobacteria, FEMS Microbiol. Lett., 39, 215–233, https://doi.org/10.1111/j.15746968.1986.tb01860.x, 1986.
Albeck, S., Aizenberg, J., Addadi, L., and Weiner, S.: Interactions of various skeletal intracrystalline components with calcite crystals, J. Am. Chem. Soc., 115, 11691–11697, 1993.
Allgaier, M., Riebesell, U., Vogt, M., Thyrhaug, R., and Grossart, H.-P.: Coupling of heterotrophic bacteria to phytoplankton bloom development at different pCO2 levels: a mesocosm study, Biogeosciences, 5, 1007–1022, https://doi.org/10.5194/bg-5-1007-2008, 2008.
Allen, M. M.: Simple Conditions for Growth of Unicellular Blue-Green Algae on Plates, J. Phycol., 4, 1–4, 1968.
Anderson, D. M., Glibert, P. M., and Burkholder, J. M.: Harmful algal blooms and eutrophication: Nutrient sources, composition, and consequences, Estuaries, 25, 704–726, https://doi.org/10.1007/BF02804901, 2002.
Baba, M., Snoeck, R., Pauwels, R., and De Clercq, E.: Sulfated polysaccharides are potent and selective inhibitors of various enveloped viruses, including herpes simplex virus, cytomegalovirus, vesicular stomatitis virus, and human immunodeficiency virus, Antimicrob Agents Chemother, 32, 1742–1745, 1988.
Babele, P. K., Kumar, J., and Chaturvedi, V.: Proteomic deregulation in cyanobacteria in response to abiotic stresses, Front. Microbiol., 10, 1315, https://doi.org/10.3389/fmicb.2019.01315, 2019.
Badger, M. R. and Andrews, T. J.: Photosynthesis and Inorganic Carbon Usage by the Marine Cyanobacterium, Synechococcus sp, Plant Physiol., 70, 517–523, https://doi.org/10.1104/pp.70.2.517, 1982.
Badger, M. R. and Price, G. D.: The CO2 concentrating mechanism in cyanobactiria and microalgae, Physiol. Plantarum, 84, 606–615, 1992.
Badger, M. R. and Price, G. D.: The role of carbonic anhydrase in photosynthesis, Annu. Rev. Plant Biol., 45, 369–392, 1994.
Badger, M. R., Hanson, D., and Price, G. D.: Evolution and diversity of CO2 concentrating mechanisms in cyanobacteria, Funct. Plant Biol., 29, 161–173, 2002.
Badger, M. R., Price, G. D., Long, B. M., and Woodger, F. J.: The environmental plasticity and ecological genomics of the cyanobacterial CO2 concentrating mechanism, J. Exp. Bot., 57, 249–265, https://doi.org/10.1093/jxb/eri286, 2006.
Bhosle, N. B., Sawant, S. S., Garg, A., and Wagh, A. B.: Isolation and Partial Chemical Analysis of Exopolysaccharides from the Marine Fouling Diatom Navicula subinflata, Bot. Mar., 38, https://doi.org/10.1515/botm.1995.38.1-6.103, 1995.
Borman, A. H., Jong, E. W., Huizinga, M., Kok, D. J., Westbroek, P., and Bosch, L.: The Role in CaCO3 Crystallization of an Acid Ca2+-Binding Polysaccharide Associated with Coccoliths of Emiliania huxleyi, Eur. J. Biochem., 129, 179–183, https://doi.org/10.1111/j.1432-1033.1982.tb07037.x, 1982.
Braissant, O., Decho, A. W., Dupraz, C., Glunk, C., Przekop, K. M., and Visscher, P. T.: Exopolymeric substances of sulfate-reducing bacteria: interactions with calcium at alkaline pH and implication for formation of carbonate minerals, G eobiology, 5, 401–411, 2007.
Bundeleva, I. A., Shirokova, L. S., Bénézeth, P., Pokrovsky, O. S., Kompantseva, E. I., and Balor, S.: Calcium carbonate precipitation by anoxygenic phototrophic bacteria, Chem. Geol., 291, 116–131, https://doi.org/10.1016/j.chemgeo.2011.10.003, 2012.
Bundeleva, I. A., Shirokova, L. S., Pokrovsky, O. S., Bénézeth, P., Ménez, B., Gérard, E., and Balor, S.: Experimental modeling of calcium carbonate precipitation by cyanobacterium Gloeocapsa sp., Chem. Geol., 374–375, 44–60, https://doi.org/10.1016/j.chemgeo.2014.03.007, 2014.
Burnap, R., Hagemann, M., and Kaplan, A.: Regulation of CO2 Concentrating Mechanism in Cyanobacteria, Life, 5, 348–371, https://doi.org/10.3390/life5010348, 2015.
Callieri, C. and Stockner, J.: Picocyanobacteria success in oligotrophic lakes: fact or fiction?, J. Limnol., 59, 72, https://doi.org/10.4081/jlimnol.2000.72, 2000.
Callieri, C., Lami, A., and Bertoni, R.: Microcolony Formation by Single-Cell Synechococcus Strains as a Fast Response to UV Radiation, Appl. Environ. Microbiol., 77, 7533–7540, https://doi.org/10.1128/AEM.05392-11, 2011.
Campbell, L. and Carpenter, E. J.: Diel patterns of cell division in marine Synechococcus spp. (Cyanobacteria): use of the frequency of dividing cells technique to measure growth rate, Mar. Ecol.-Prog. Ser., 32, 139–148, 1986.
Ciebiada, M., Kubiak, K., and Daroch, M.: Modifying the Cyanobacterial Metabolism as a Key to Efficient Biopolymer Production in Photosynthetic Microorganisms, Int. J. Mol. Sci., 21, 7204, https://doi.org/10.3390/ijms21197204, 2020.
Clark, D. R. and Flynn, K. J.: The relationship between the dissolved inorganic carbon concentration and growth rate in marine phytoplankton, P. R. Soc. Lond. B, 267, 953–959, https://doi.org/10.1098/rspb.2000.1096, 2000.
Coates, J.: Interpretation of infrared spectra, a practical approach, John Wiley & Sons, Ltd, Chichester, UK, https://doi.org/10.1002/9780470027318.a5606, 2000.
Coello-Camba, A. and Agustí, S.: Picophytoplankton Niche Partitioning in the Warmest Oligotrophic Sea, Front. Mar. Sci., 8, 651877, https://doi.org/10.3389/fmars.2021.651877, 2021.
Dean, J. A.: Table 3.21 Physical constants of inorganic compounds, Lange’s Handbook of Chemistry, McGraw-Hill Inc., New York, 1999.
De Philippis, R., Sili, C., and Vincenzini, M.: Response of an exopolysaccharide-producing heterocystous cyanobacterium to changes in metabolic carbon flux, J. Appl. Phycol., 8, 275–281, 1996.
De Philippis, R., Sili, C., Paperi, R., and Vincenzini, M.: Exopolysaccharide-producing cyanobacteria and their possible exploitation: a review, J. Appl. Phycol., 13, 293–299, 2001.
Decho, A. W. and Gutierrez, T.: Microbial extracellular polymeric substances (EPSs) in ocean systems, Front. Microbiol., 8, 922, 2017.
Decho, A. W. and Kawaguchi, T.: Extracellular polymers (EPS) and calcification within modern marine stromatolites, in: Fossil and Recent Biofilms, edited by: Krumbein, W. E., Paterson, D. M., and Zavarzin, G. A., Springer, Dordrecht, 227–240, https://doi.org/10.1007/978-94-017-0193-8_14, 2003.
Diaz, M. R., Eberli, G. P., Blackwelder, P., Phillips, B., and Swart, P. K.: Microbially mediated organomineralization in the formation of ooids, Geology, 45, 771–774, https://doi.org/10.1130/G39159.1, 2017.
Dittrich, M. and Obst, M.: Are picoplankton responsible for calcite precipitation in lakes?, AMBIO, 33, 559–564, 2004.
Dittrich, M. and Sibler, S.: Calcium carbonate precipitation by cyanobacterial polysaccharides, Geological Society, London, Special Publications, 336, 51–63, 2010.
Dittrich, M., Müller, B., Mavrocordatos, D., and Wehrli, B.: Induced calcite precipitation by cyanobacterium Synechococcus, Acta Hydroch. Hydrob., 31, 162–169, 2003.
Dokulil, M. T. and Teubner, K.: Cyanobacterial dominance in lakes, Hydrobiologia, 438, 1–12, https://doi.org/10.1023/A:1004155810302, 2000.
Dubois, M., Gilles, K. A., Hamilton, J. K., Rebers, P. t, and Smith, F.: Colorimetric method for determination of sugars and related substances, Anal. Chem., 28, 350–356, 1956.
Dupraz, C. and Visscher, P. T.: Microbial lithification in marine stromatolites and hypersaline mats, Trends Microbiol., 13, 429–438, 2005.
Dupraz, C., Reid, R. P., Braissant, O., Decho, A. W., Norman, R. S., and Visscher, P. T.: Processes of carbonate precipitation in modern microbial mats, Earth-Sci. Rev., 96, 141–162, https://doi.org/10.1016/j.earscirev.2008.10.005, 2009.
Ghosh, T., Chattopadhyay, K., Marschall, M., Karmakar, P., Mandal, P., and Ray, B.: Focus on antivirally active sulfated polysaccharides: From structure-activity analysis to clinical evaluation, Glycobiology, 19, 2–15, 2009.
Giordano, M., Beardall, J., and Raven, J. A.: CO2 Concentrating Mechanisms in Algae: Mechanisms, Environmental Modulation, and Evolution, Annu. Rev. Plant Biol., 56, 99–131, https://doi.org/10.1146/annurev.arplant.56.032604.144052, 2005.
Gons, H. J., Ebert, J., Hoogveld, H. L., Takkenberg, W., and Woldringh, C. J.: Observations on cyanobacterial population collapse in eutrophic lake water, Antonie Van Leeuwenhoek, 81, 319–326, https://doi.org/10.1023/a:1020595408169, 2002.
Hagström, Å., Azam, F., Andersson, A., Wikner, J., and Rassoulzadegan, F.: Microbial loop in an oligotrophic pelagic marine ecosystem: possible roles of cyanobacteria and nanoflagellates in the organic fluxes, Mar. Ecol.-Prog. Ser., 49, 171–178, https://doi.org/10.3354/meps049171, 1988.
Havens, K. E.: Cyanobacteria blooms: effects on aquatic ecosystems, Adv. Exp. Med. Biol., 619, 733–747, https://doi.org/10.1007/978-0-387-75865-7_33, 2008.
Hein, M.: Inorganic carbon limitation of photosynthesis in lake phytoplankton, Freshwater Biol., 37, 545–552, https://doi.org/10.1046/j.1365-2427.1997.00180.x, 1997.
Heisler, J., Glibert, P. M., Burkholder, J. M., Anderson, D. M., Cochlan, W., Dennison, W. C., Dortch, Q., Gobler, C. J., Heil, C. A., Humphries, E., Lewitus, A., Magnien, R., Marshall, H. G., Sellner, K., Stockwell, D. A., Stoecker, D. K., and Suddleson, M.: Eutrophication and harmful algal blooms: A scientific consensus, Harmful Algae, 8, 3–13, https://doi.org/10.1016/j.hal.2008.08.006, 2008.
Hodell, D. A., Schelske, C. L., Fahnenstiel, G. L., and Robbins, L. L.: Biologically induced calcite and its isotopic composition in Lake Ontario, Limnol. Oceanogr., 43, 187–199, 1998.
Huisman, J., Codd, G. A., Paerl, H. W., Ibelings, B. W., Verspagen, J. M. H., and Visser, P. M.: Cyanobacterial blooms, Nat. Rev. Microbiol., 16, 471–483, https://doi.org/10.1038/s41579-018-0040-1, 2018.
Ibelings, B. W. and Maberly, S. C.: Photoinhibition and the availability of inorganic carbon restrict photosynthesis by surface blooms of cyanobacteria, Limnol. Oceanogr., 43, 408–419, 1998.
Ionescu, D., Spitzer, S., Reimer, A., Schneider, D., Daniel, R., Reitner, J., de Beer, D., and Arp, G.: Calcium dynamics in microbialite-forming exopolymer-rich mats on the atoll of Kiritimati, Republic of Kiribati, Central Pacific, Geobiology, 13, 170–180, https://doi.org/10.1111/gbi.12120, 2015.
Kamennaya, N., Ajo-Franklin, C., Northen, T., and Jansson, C.: Cyanobacteria as Biocatalysts for Carbonate Mineralization, Minerals, 2, 338–364, https://doi.org/10.3390/min2040338, 2012.
Kansiz, M., Heraud, P., Wood, B., Burden, F., Beardall, J., and McNaughton, D.: Fourier Transform Infrared microspectroscopy and chemometrics as a tool for the discrimination of cyanobacterial strains, Phytochemistry, 52, 407–417, https://doi.org/10.1016/S0031-9422(99)00212-5, 1999.
Kavita, K., Mishra, A., and Jha, B.: Isolation and physico-chemical characterisation of extracellular polymeric substances produced by the marine bacterium Vibrio parahaemolyticus, Biofouling, 27, 309–317, https://doi.org/10.1080/08927014.2011.562605, 2011.
Kawaguchi, T. and 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. Biotech., 32, 51–63, 2002.
Kieft, B., Li, Z., Bryson, S., Hettich, R. L., Pan, C., Mayali, X., and Mueller, R. S.: Phytoplankton exudates and lysates support distinct microbial consortia with specialized metabolic and ecophysiological traits, P. Natl. Acad. Sci. USA, 118, e2101178118, https://doi.org/10.1073/pnas.2101178118, 2021.
Kjelleberg, S., Hermansson, M., Marden, P., and Jones, G. W.: The transient phase between growth and non-growth of heterotrophic bacteria, with emphasis on the marine environment, Annu. Rev. Microbiol., 41, 25–49, 1987.
Kupriyanova, E. V. and Pronina, N. A.: Carbonic anhydrase: Enzyme that has transformed the biosphere, Russ. J. Plant Physl.+, 58, 197–209, https://doi.org/10.1134/S1021443711020099, 2011.
Kupriyanova, E. V., Sinetova, M. A., Bedbenov, V. S., Pronina, N. A., and 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, 164, 576–586, 2018.
Larson, E. B. and Mylroie, J. E.: A review of whiting formation in the Bahamas and new models, Carbonate. Evaporite., 29, 337–347, 2014.
Liu, L., Huang, Q., and Qin, B.: Characteristics and roles of Microcystis extracellular polymeric substances (EPS) in cyanobacterial blooms: a short review, J. Freshwater Ecol., 33, 183–193, https://doi.org/10.1080/02705060.2017.1391722, 2018.
Lürling, M., Mello, M. M. e, van Oosterhout, F., de Senerpont Domis, L., and Marinho, M. M.: Response of Natural Cyanobacteria and Algae Assemblages to a Nutrient Pulse and Elevated Temperature, Front. Microbiol., 9, 1851, https://doi.org/10.3389/fmicb.2018.01851, 2018.
Maberly, S. C.: Diel, episodic and seasonal changes in pH and concentrations of inorganic carbon in a productive lake, Freshwater Biol., 35, 579–598, https://doi.org/10.1111/j.13652427.1996.tb01770.x, 1996.
Maeda, H., Kawai, A., and Tilzer, M. M.: The water bloom of Cyanobacterial picoplankton in Lake Biwa, Japan, Hydrobiologia, 248, 93–103, https://doi.org/10.1007/BF00006077, 1992.
Maeda, K., Okuda, Y., Enomoto, G., Watanabe, S., and Ikeuchi, M.: Biosynthesis of a sulfated exopolysaccharide, synechan, and bloom formation in the model cyanobacterium Synechocystis sp. strain PCC 6803, Elife, 10, e66538, https://doi.org/10.7554/eLife.66538, 2021.
Marin, F., Corstjens, P., de Gaulejac, B., de Vrind-De Jong, E., and 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., 275, 20667–20675, 2000.
Martinez, R. E., Gardés, E., Pokrovsky, O. S., Schott, J., and Oelkers, E. H.: Do photosynthetic bacteria have a protective mechanism against carbonate precipitation at their surfaces?, Geochim. Cosmochim. Ac., 74, 1329–1337, https://doi.org/10.1016/j.gca.2009.11.025, 2010.
Martinho de Brito, M., Bundeleva, I., Marin, F., Vennin, E., Wilmotte, A., Plasseraud, L., and Visscher, P. T.: Effect of Culture pH on Properties of Exopolymeric Substances from Synechococcus PCC7942: Implications for Carbonate Precipitation, Geosciences, 12, 210, https://doi.org/10.3390/geosciences12050210, 2022.
Marvasi, M., Visscher, P. T., and Casillas Martinez, L.: Exopolymeric substances (EPS) from Bacillus subtilis: polymers and genes encoding their synthesis, FEMS Microbiol. Lett., 313, 1–9, 2010.
Mayo, W. P., Elrifi, I. R., and Turpin, D. H.: The Relationship between Ribulose Bisphosphate Concentration, Dissolved Inorganic Carbon (DIC) Transport and DIC-Limited Photosynthesis in the Cyanobacterium Synechococcus leopoliensis Grown at Different Concentrations of Inorganic Carbon, Plant Physiol., 90, 720–727, https://doi.org/10.1104/pp.90.2.720, 1989.
Miller, A. G., Turpin, D. H., and Canvin, D. T.: Growth and Photosynthesis of the Cyanobacterium Synechococcus leopoliensis in HCO−3 – Limited Chemostats, Plant Physiol., 75, 1064–1070, https://doi.org/10.1104/pp.75.4.1064, 1984.
Mitterer, R. M. and Cunningham, R.: The interaction of natural organic matter with grain surfaces: implications for calcium carbonate precipitation, Soc. Econ. Paleont. Mineral., Spec. Publ., 36, 17–31, 1985.
Murphy, L. S. and Haugen, E. M.: The distribution and abundance of phototrophic ultraplankton in the North Atlantic, Limnol. Oceanogr., 30, 47–58, https://doi.org/10.4319/lo.1985.30.1.0047, 1985.
Myklestad, S. and Haug, A.: Production of carbohydrates by the marine diatom Chaetoceros affinis var. willei (Gran) Hustedt. I. Effect of the concentration of nutrients in the culture medium, J. Exp. Mar. Biol. Ecol., 9, 125–136, 1972.
Myklestad, S., Holm-Hansen, O., Vårum, K. M., and Volcani, B. E.: Rate of release of extracellular amino acids and carbohydrates from the marine diatom Chaetoceros affinis, J. Plankton Res., 11, 763–773, https://doi.org/10.1093/plankt/11.4.763, 1989.
Obst, M., Dynes, J. J., Lawrence, J. R., Swerhone, G. D., Benzerara, K., Karunakaran, C., Kaznatcheev, K., Tyliszczak, T., and 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. Ac., 73, 4180–4198, 2009.
O’Neil, J. M., Davis, T. W., Burford, M. A., and Gobler, C. J.: The rise of harmful cyanobacteria blooms: The potential roles of eutrophication and climate change, Harmful Algae, 14, 313–334, https://doi.org/10.1016/j.hal.2011.10.027, 2012.
Paerl, H.: Nutrient and other environmental controls of harmful cyanobacterial blooms along the freshwater-marine continuum, Adv. Exp. Med. Biol., 619, 217–237, https://doi.org/10.1007/978-0-387-75865-7_10, 2008.
Paerl, H. W. and Huisman, J.: Blooms Like It Hot, Science, 320, 57–58, https://doi.org/10.1126/science.1155398, 2008.
Paerl, H. W., Fulton, R. S., Moisander, P. H., and Dyble, J.: Harmful Freshwater Algal Blooms, With an Emphasis on Cyanobacteria, Sci. World J., 1, 76–113, https://doi.org/10.1100/tsw.2001.16, 2001.
Pannard, A., Pédrono, J., Bormans, M., Briand, E., Claquin, P., and Lagadeuc, Y.: Production of exopolymers (EPS) by cyanobacteria: impact on the carbon-to-nutrient ratio of the particulate organic matter, Aquat. Ecol., 50, 29–44, https://doi.org/10.1007/s10452-015-9550-3, 2016.
Pereira, S., Zille, A., Micheletti, E., Moradas-Ferreira, P., De Philippis, R., and Tamagnini, P.: Complexity of cyanobacterial ex-opolysaccharides: composition, structures, inducing factors and putative genes involved in their biosynthesis and assembly, FEMS Microbiol. Rev., 33, 917–941, 2009.
Phlips, E. J., Badylak, S., and Lynch, T. C.: Blooms of the picoplanktonic cyanobacterium Synechococcus in Florida Bay, a subtropical inner-shelf lagoon, Limnol. Oceanogr., 44, 1166–1175, https://doi.org/10.4319/lo.1999.44.4.1166, 1999.
Ploug, H.: Cyanobacterial surface blooms formed by Aphanizomenon sp. and Nodularia spumigena in the Baltic Sea: Small-scale fluxes, pH, and oxygen mi-croenvironments, Limnol. Oceanogr., 53, 914–921, https://doi.org/10.4319/lo.2008.53.3.0914, 2008.
Pomar, L. and Hallock, P.: Carbonate factories: a conundrum in sedimentary geology, Earth-Sci. Rev., 87, 134–169, 2008.
Price, G. D.: Inorganic carbon transporters of the cyanobacterial CO2 concentrating mechanism, Photosynth. Res., 109, 47–57, https://doi.org/10.1007/s11120-010-9608-y, 2011.
Price, G. D., Sültemeyer, D., Klughammer, B., Ludwig, M., and Badger, M. R.: The functioning of the CO2 concentrating mechanism in several cyanobacterial strains: a review of general physiological characteristics, genes, proteins, and recent advances, Can. J. Botany, 76, 973–1002, 1998.
Price, G. D., Maeda, S., Omata, T., and Badger, M. R.: Modes of active inorganic carbon uptake in the cyanobacterium, Synechococcus sp. PCC7942, Funct. Plant Biol., 29, 131, https://doi.org/10.1071/PP01229, 2002.
Price, G. D., Badger, M. R., Woodger, F. J., and Long, B. M.: Advances in understanding the cyanobacterial CO2concentrating-mechanism (CCM): functional components, Ci transporters, diversity, genetic regulation and prospects for engineering into plants, J. Exp. Bot., 59, 1441–1461, https://doi.org/10.1093/jxb/erm112, 2008.
Rae, B. D., Long, B. M., Whitehead, L. F., Förster, B., Badger, M. R., and Price, G. D.: Cyanobacterial Carboxysomes: Micro-compartments that Facilitate CO2 Fixation, Microb. Physiol., 23, 300–307, https://doi.org/10.1159/000351342, 2013.
Raven, J. A., Beardall, J., and Sánchez-Baracaldo, P.: The possible evolution and future of CO2-concentrating mechanisms, J. Exp. Bot., 68, 3701–3716, 2017.
Reynolds, C. S.: Cyanobacterial Water-Blooms, in: Advances in Botanical Research, edited by: Callow, J. A., Academic Press, 67–143, https://doi.org/10.1016/S0065-2296(08)60341-9, 1987.
Reynolds, C. S. and Walsby, A. E.: WATER-BLOOMS, Biol. Rev., 50, 437–481, https://doi.org/10.1111/j.1469185X.1975.tb01060.x, 1975.
Rippka, R., Deruelles, J., Waterbury, J. B., Herdman, M., and Stanier, R. Y.: Generic assignments, strain histories and properties of pure cultures of cyanobacteria, Microbiology, 111, 1–61, 1979.
Robbins, L. and Blackwelder, P.: Biochemical and ultrastructural evidence for the origin of whitings: A biologically induced calcium carbonate precipitation mechanism, Geology, 20, 464–468, 1992.
Rossi, F. and De Philippis, R.: Role of cyanobacterial exopolysaccharides in phototrophic biofilms and in complex microbial mats, Life, 5, 1218–1238, 2015.
Sandrini, G., Tann, R. P., Schuurmans, J. M., van Beusekom, S. A. M., Matthijs, H. C. P., and Huisman, J.: Diel Variation in Gene Expression of the CO2-Concentrating Mechanism during a Harmful Cyanobacterial Bloom, Front. Microbiol., 7, 551, https://doi.org/10.3389/fmicb.2016.00551, 2016.
Schultze-Lam, S., Harauz, G., and Beveridge, T. J.: Participation of a cyanobacterial S layer in fine-grain mineral formation, J. Bacteriol., 174, 7971–7981, https://doi.org/10.1128/jb.174.24.79717981.1992, 1992.
Schultze-Lam, S., Schultze-Lam, S., Beveridge, T. J., and Des Marais, D. J.: Whiting events: biogenic origin due to the photosynthetic activity of cyanobacterial picoplankton, Limnol. Oceanogr., 42, 133–141, 1997.
Shen, G., Canniffe, D. P., Ho, M. Y., Kurashov, V., van der Est, A., Golbeck, J. H., and Bryant, D. A.: Characterization of chlorophyll f synthase heterologously produced in Synechococcus sp. PCC 7002, Photosynth. Res., 140, 77–92, 2019.
Shinn, E. A., Steinen, R. P., Lidz, B. H., and Swart, P. K.: Whitings, a sedimentologic dilemma, J. Sediment. Res., 59, 147–161, 1989.
Skoog, E. J., Moore, K. R., Gong, J., Ciccarese, D., Momper, L., Cutts, E. M., and Bosak, T.: Metagenomic, (bio)chemical, and microscopic analyses reveal the potential for the cycling of sulfated EPS in Shark Bay pustular mats, ISME Commun., 2, 43, https://doi.org/10.1038/s43705-022-00128-1, 2022.
Stal, L., Van Gemerden, H., and Krumbein, W.: The simultaneous assay of chlorophyll and bacteriochlorophyll in natural microbial communities, J. Microbiol. Meth., 2, 295–306, 1984.
Stanton, C., Barnes, B. D., Kump, L. R., and Cosmidis, J.: A reexamination of the mechanism of whiting events: A new role for diatoms in Fayetteville Green Lake (New York, USA), Geobiology, 21, 210–228, https://doi.org/10.1111/gbi.12534, 2023.
Tai, V. and Palenik, B.: Temporal variation of Synechococcus clades at a coastal Pacific Ocean monitoring site, ISME J., 3, 903–915, https://doi.org/10.1038/ismej.2009.35, 2009.
Takahashi, Y., Yamaguchi, O., and Omata, T.: Roles of CmpR, a LysR family transcriptional regulator, in acclimation of the cyanobacterium Synechococcus sp. strain PCC 7942 to low-CO2 and high-light conditions: High-light and low-CO2 acclimation in cyanobacteria, Mol. Microbiol., 52, 837–845, https://doi.org/10.1111/j.1365-2958.2004.04021.x, 2004.
Talling, J. F.: The Depletion of Carbon Dioxide from Lake Water by Phytoplankton, J. Ecol., 64, 79, https://doi.org/10.2307/2258685, 1976.
Thompson, J. and Ferris, F.: Cyanobacterial precipitation of gypsum, calcite, and magnesite from natural alkaline lake water, Geology, 18, 995–998, 1990.
Thompson, J. B.: Microbial Whitings, in: Microbial Sediments, edited by: Riding, R. E. and Awramik, S. M., Springer, Berlin, Heidelberg, https://doi.org/10.1007/978-3-662-04036-2_27, 2000.
Thompson, J. B., Ferris, F. G., and Smith, D. A.: Geomicrobiology and Sedimentology of the Mixolimnion and Chemocline in Fayetteville Green Lake, New York, PALAIOS, 5, 52, https://doi.org/10.2307/3514996, 1990.
Tortell, P. D.: Evolutionary and ecological perspectives on carbon acquisition in phytoplankton, Limnol. Oceanogr., 45, 744–750, https://doi.org/10.4319/lo.2000.45.3.0744, 2000.
Tortell, P. D., Rau, G. H., and Morel, F. M. M.: Inorganic carbon acquisition in coastal Pacific phytoplankton communities, Limnol. Oceanogr, 45, 1485–1500, https://doi.org/10.4319/lo.2000.45.7.1485, 2000.
Townsend, D. W., Cammen, L. M., Holligan, P. M., Campbell, D. E., and Pettigrew, N. R.: Causes and consequences of variability in the timing of spring phytoplankton blooms, Deep-Sea Res. Pt. I, 41, 747–765, https://doi.org/10.1016/0967-0637(94)90075-2, 1994.
Trichet, J. and Defarge, C.: Non-biologically supported organomineralization, Bulletin–Institut Oceanographic Monaco, Numero Special, 203–236, 1995.
Verspagen, J. M. H., Van de Waal, D. B., Finke, J. F., Visser, P. M., Van Donk, E., and Huisman, J.: Rising CO2 Levels Will Intensify Phytoplankton Blooms in Eutrophic and Hypertrophic Lakes, PLOS ONE, 9, e104325, https://doi.org/10.1371/journal.pone.0104325, 2014.
Visscher, P. T., Reid, R. P., Bebout, B. M., Hoeft, S. E., Macintyre, I. G., & Thompson, J. A.: Formation of lithified micritic laminae in modern marine stromatolites (Bahamas); the role of sulfur cycling, Am. Mineral., 83 (11–12_Part_2), 1482–1493, 1998.
Walker, J. M., Marzec, B., Lee, R. B. Y., Vodrazkova, K., Day, S. J., Tang, C. C., Rickaby, R. E. M., and Nudelman, F.: Polymorph Selectivity of Coccolith-Associated Polysaccharides from Gephyrocapsa Oceanica on Calcium Carbonate Formation In Vitro, Adv. Funct. Mater., 29, 1807168, https://doi.org/10.1002/adfm.201807168, 2019.
Wall, R. S. and Gyi, T. J.: Alcian blue staining of proteoglycans in polyacrylamide gels using the “critical electrolyte concentration” approach, Anal. Biochem., 175, 298–299, 1988.
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., and Wang, X.-K.: pH dependence of structure and surface properties of microbial EPS, Environ. Sci. Technol., 46, 737–744, 2012.
Weisse, T.: Dynamics of Autotrophic Picoplankton in Marine and Freshwater Ecosystems, in: Advances in Microbial Ecology, vol. 13, edited by: Jones, J. G., Springer US, Boston, MA, 327–370, https://doi.org/10.1007/978-1-4615-2858-6_8, 1993.
Wells, A. J. and Iling, L. V.: Present-day precipitation of calcium carbonate in the Persian Gulf, in: Deltaic and shallow-water marine deposits, edited by: van Straaten, L., Elsevier Developments in Sedimentology Series, New York, 429–435, https://doi.org/10.1016/S0070-4571(08)70517-X, 1964.
Wheeler, A., George, J. W., and Evans, C.: Control of calcium carbonate nucleation and crystal growth by soluble matrx of oyster shell, Science, 212, 1397–1398, 1981.
Whitton, B. A. and Potts, M.: Introduction to the Cyanobacteria, in: Ecology of Cyanobacteria II, edited by: Whitton, B. A., Springer Netherlands, Dordrecht, 1–13, https://doi.org/10.1007/978-94-007-3855-3_1, 2012.
Xu, H., Paerl, H. W., Qin, B., Zhu, G., Hall, N. S., and Wu, Y.: Determining Critical Nutrient Thresholds Needed to Control Harmful Cyanobacterial Blooms in Eutrophic Lake Taihu, China, Environ. Sci. Technol., 49, 1051–1059, https://doi.org/10.1021/es503744q, 2015.
Yang, G., Li, F., Deng, Z., Wang, Y., Su, Z., Huang, L., Yin, L., and Ji, C.: Abnormal Crystallization Sequence of Calcium Carbonate in the Presence of Synechococcus sp. PCC 7942, Geomicrobiol. J., 40, 34–45, https://doi.org/10.1080/01490451.2022.2100948, 2023.
Yates, K. K. and Robbins, L. L.: Production of carbonate sediments by a unicellular green alga, Ame. Mineral., 83, 1503–1509, 1998.
Zepernick, B. N., Gann, E. R., Martin, R. M., Pound, H. L., Krausfeldt, L. E., Chaffin, J. D., and 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., 12, 188, 2021.
Zhao, H., Han, G., Zhang, S., and Wang, D.: Two phytoplankton blooms near Luzon Strait generated by lingering Typhoon Parma: Lingering Typhoon-Induced Algae Blooms, J. Geophys. Res.-Biogeo., 118, 412–421, https://doi.org/10.1002/jgrg.20041, 2013.
