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CALCAREOUS ALGAE Bibliography CALCIFICATION CALCIFIED C CALCAREOUS ALGAE CALCIFIED CYANOBACTERIA The term “calcareous algae” refers to various kinds of Robert Riding benthic and planktonic algae whose thalli contain biochem- University of Tennessee, Knoxville, TN, USA ically precipitated calcium carbonate (CaCO3) as skeletal material (Wray, 1977; Braga and Riding, 2005). Precipita- Definition tion of CaCO3 (as calcite and/or aragonite) may occur Cyanobacteria are alga-like bacteria that can perform oxy- within or on the algal bodies. The term may also include genic photosynthesis and nitrogen fixation (Whitton and mechanically accreted deposits of calcium carbonate caused Potts, 2000; Herrero and Flores, 2008). They have a long by algae, usually as an interaction of biological and physical history and are diverse and widespread in marine, fresh- processes. Calcareous algae are a highly artificial group that water, and terrestrial environments at the present-day, constitutes calcifying members of the Chlorophyta (green where they are key primary producers in both microbial algae), Rhodophyta (red algae), and Phaeophyta (brown mat and planktic ecosystems. As the initiators of plastids, algae) and is sometimes also used for Cyanobacteria. At they have played a fundamental role in algal and plant present, calcareous algae are one of the most important reef evolution (Raven, 2002). Cyanobacteria occupy benthic “ ” builders (see Carbonate Environments ). For a detailed substrates and can also drift in the water column. Their “ ” reading, please refer to Algae (Eukaryotic). photosynthetic uptake of inorganic carbon can stimulate CaCO3 precipitation. This calcification can produce fila- Bibliography mentous microfossils in benthic mats that are preserved as stromatolites and thrombolites, and can also cause Braga, J. C., and Riding, R., 2005. Calcareous algae. In Selley, R., Cocks, L. R. M., and Plimer, I. R. (eds.), Encyclopedia of Geol- water column precipitation of carbonate mud that settles ogy. Amsterdam: Elsevier, pp. 428–436. to lake and sea floors. Wray, J. L., 1977. Calcareous Algae. Developments in Palaeontology and Stratigraphy. Amsterdam: Elsevier, Vol. 4, 185 pp. Introduction However, cyanobacterial calcification is not obligatory and is directly dependent on environmental conditions. This accounts for apparent discrepancies between the CALCIFICATION geological ranges of organic-walled and calcified cyanobacterial fossils. Calcified cyanobacteria have not See entries “Animal Biocalcification, Evolution,” been recognized in marine sediments older than 1200 “Biofilms and Fossilization,”“Calcified Cyanobacteria,” Ma ago (Kah and Riding, 2007), whereas there is evidence “Calcite Precipitation, Microbially Induced,”“Calcium that cyanobacteria appeared in the late Archaean or Biogeochemistry,”“Carbonate Environments,”“Dolomite, Palaeoproterozoic, in the range 2900–2150 Ma ago Microbial,”“Microbialites, Modern,”“Microbialites, Stro- (Cavalier-Smith et al., 2006; Hofmann, 1976). This mid- matolites, and Thrombolites,” and “Pedogenic Proterozoic appearance of sheath-calcified cyanobacteria Carbonates.” is thought to reflect the development of CO2-concentrating Joachim Reitner & Volker Thiel (eds.), Encyclopedia of Geobiology, DOI 10.1007/978-1-4020-9212-1, # Springer Science+Business Media B.V. 2011 212 CALCIFIED CYANOBACTERIA mechanisms (CCMs) as atmospheric CO2 levels declined among which phosphate inhibition of CaCO3 precipitation (Riding, 2006). Calcified cyanobacterial fossils remained (Raistrick, 1949) may be important (Hägele et al., 2006). conspicuous components of marine stromatolites and CO2-concentrating mechanisms: Photosynthetic car- thrombolites through much of the Neoproterozoic, bon uptake can directly influence cyanobacterial calcifica- Palaeozoic, and Mesozoic, but became vanishingly scarce tion. Diffusive entry of CO2 into the cell may not in the Cenozoic, including present-day seas (Riding, significantly affect ambient pH, but active bicarbonate 1982), probably due to decline in seawater saturation for uptake increases pH near the cell (Miller and Colman, CaCO minerals (Riding, 1993, p. 514; 2000, p. 200; 1980) that promotes calcification (Thompson and Ferris, 3 À Kempe and Kazmierczak, 1994). Cyanobacterial calcifi- 1990). Bicarbonate (HCO3 ) is actively transported into cation is thus a good example of “induced,” as opposed the cell and intracellularly converted to CO2 for photosyn- to “controlled” biocalcification. Its close environmental thesis. These processes lead to increased pH in the imme- dependence can be used to interpret changes in past diate vicinity of the cell. Where ambient waters are conditions such as carbonate saturation state and the sufficiently saturated for CaCO3 minerals then this local- availability of inorganic carbon for photosynthesis. In ized pH increase can trigger the nucleation of CaCO3 crys- addition to their sedimentological importance, calcified tallites on or near the cell surface or in the enveloping cyanobacteria can therefore assist in the reconstruction of mucilaginous sheath (Figures 1 and 2): seawater chemistry and atmospheric composition over À þ 2þ ! þ þ long geological time scales. 2HCO3 Ca CH2O CaCO3 O2 Active bicarbonate uptake and its conversion within the Controls on calcification cell to CO2 by carbonic anhydrase are adaptations to reduced availability of CO2. They constitute CCMs The ability of cyanobacteria to grow and reproduce (Kaplan and Reinhold, 1999). CCM induction can be trig- whether they are calcified or uncalcified illustrates the gered by localized carbon limitation, e.g., within micro- non-obligate nature of their calcification (Pentecost and bial mats or phytoplankton blooms, and also by fall in Riding, 1986). Two factors that directly influence global atmospheric CO levels. Modeled estimates sug- cyanobacterial calcification are the saturation state of 2 gest that atmospheric CO2 has fluctuated widely during ambient waters and the mechanism of photosynthetic the Phanerozoic, up to levels that are 25 or more times uptake of inorganic carbon (Riding, 2006). higher than present atmospheric level (PAL) (Berner Carbonate saturation state: Cyanobacterial calcifica- and Kothavala, 2001). CCMs are well-developed in tion requires waters in which CaCO3 precipitation is ther- cyanobacteria (Kaplan et al., 1980; Giordano et al., modynamically favored (Pentecost, 1981; Kempe and 2005) and experiments suggest that they are induced when Kazmierczak, 1994; Merz-Preib and Riding, 1999). It ambient CO2 falls below a critical threshold that is roughly has been very common in marine environments at times equivalent to 10 PAL (Badger et al., 2002). It therefore since the Neoproterozoic, but these episodes are markedly seems likely that CCM induction plays a significant role episodic and can be interspersed by long periods when in cyanobacterial calcification (Thompson and Ferris, cyanobacterial calcification is scarce (Riding, 1992). 1990; Merz, 1992), especially at times in the geological Cyanobacterial sheath calcification has not been confi- past when CO2 levels have been below 10 PAL (Riding, dently recognized in present-day marine environments, 2006, p. 302). and is rare to absent throughout the Cenozoic (Riding, 1982; Arp et al., 2001). In contrast, cyanobacterial calcifi- cation is locally well-developed in present-day calcareous streams and lakes, and is often significantly involved in Sites of calcification the formation of tufa and oncoids (Golubic, 1973; Pedley, Calcification in cyanobacteria is close, but external, to the 1990; Pentecost, 2005). In streams, calcification reflects cell. CaCO3 crystals nucleate either within the protective increased saturation state that results from warming and mucilaginous sheath, or on or close to the cell surface degassing of spring waters, especially in turbulent zones, (Thompson and Ferris, 1990; Merz, 1992). Sheath together with the stimulus of photosynthetic carbon impregnation by crystallites (Figure 1) can produce coher- removal (Merz-Preib and Riding, 1999; Bissett et al., ent tubular and shrub-like calcified structures that preserve 2008). In lakes, precipitation is stimulated by seasonal the sheath morphology and can be preserved as microfos- warming as well as the activity of phytoplankton blooms sils for hundreds of millions of years (Riding, 1991). that include cyanobacteria (Kelts et al., 1978; Thompson In contrast, if isolated crystals form near the cell surface, and Ferris, 1990). These present-day environments are they do not form a preservable shape but can be released vulnerable to pollutants such as agricultural fertilizers. as allochthonous particles (“whitings”)(Figure 2). These Cyanobacterial calcification has declined over the past can accumulate as masses of micron-size carbonate century in temperate climate hardwater streams and lakes mud sediment on lake and sea floors and can also survive of Europe and North America, largely in response to these as ancient geological deposits. However, they are not anthropogenic changes (Pentecost, 2005, pp. 283–287), known to possess features that distinguish them as CALCIFIED CYANOBACTERIA 213 Calcified Cyanobacteria, Figure 1 Model of in vivo sheath calcification in a filamentous cyanobacterium related to CO2- concentrating mechanism (CCM)-enhanced photosynthesis (based on information in Riding, 2006, Fig. 3). The CCMs involve active carbon transport into the cell and conversions that liberate OHÀ ions. Calcification is stimulated by photosynthetic carbon uptake and OHÀ release which elevates sheath
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