Coralline algal calcification: A morphological and process-based understanding

Abstract

Research purpose and findingsCoralline algae are key biological substrates of many carbonate systems globally. Their capacity to build enduring crusts that underpin the formation of tropical reefs, rhodolith beds and other benthic substrate is dependent on the formation of a calcified thallus. However, this important process of skeletal carbonate formation is not well understood. We undertook a study of cellular carbonate features to develop a model for calcification. We describe two types of cell wall calcification; 1) calcified primary cell wall (PCW) in the thin-walled elongate cells such as central medullary cells in articulated corallines and hypothallial cells in crustose coralline algae (CCA), 2) calcified secondary cell wall (SCW) with radial Mg-calcite crystals in thicker-walled rounded cortical cells of articulated corallines and perithallial cells of CCA. The distinctive banding found in many rhodoliths is the regular transition from PCW-only cells to SCW cells. Within the cell walls there can be bands of elevated Mg with Mg content of a few mol% higher than radial Mg-calcite (M-type), ranging up to dolomite composition (D-type).Model for calcificationWe propose the following three-step model for calcification. 1) A thin (< 0.5 μm) PCW forms and is filled with a mineralising fluid of organic compounds and seawater. Nanometer-scale Mg-calcite grains precipitate on the organic structures within the PCW. 2) Crystalline cellulose microfibrils (CMF) are extruded perpendicularly from the cellulose synthase complexes (CSC) in the plasmalemma to form the SCW. 3) The CMF soaks in the mineralising fluid as it extrudes and becomes calcified, retaining the perpendicular form, thus building the radial calcite. In Clathromorphum, SCW formation lags PCW creating a zone of weakness resulting in a split in the sub-surface crust. All calcification seems likely to be a bioinduced rather than controlled process. These findings are a substantial step forward in understanding how corallines calcify.

Radiation of the coralline red algae (Corallinophycidae, Rhodophyta) crown group as inferred from a multilocus time-calibrated phylogeny

“…The physiological process of calcification is still poorly known. Borowitzka (1977) proposed that calcification is controlled by a protein-polysaccharide matrix ("Organic Matrix Theory") but more recently, Nash et al (2019) argued that calcification is likely bioinduced. These latter authors also described two types of cell wall calcification (primary and secondary) that are found among different cells of both geniculate and non-geniculate taxa (Nash et al 2019).…”

“…Borowitzka (1977) proposed that calcification is controlled by a protein-polysaccharide matrix ("Organic Matrix Theory") but more recently, Nash et al (2019) argued that calcification is likely bioinduced. These latter authors also described two types of cell wall calcification (primary and secondary) that are found among different cells of both geniculate and non-geniculate taxa (Nash et al 2019). The three fully calcified orders show inner wall crystals or blade-like crystals perpendicular to cell surface and interfilament calcite crystals elongate and tangentially oriented to the cell surface (Flajs, 1977) that are particularly conspicuous in the cold-water Clathromorphum (Adey et al, 2013); by contrast, the crystals of calcite husks reported in Rhodogorgonales are small and rhombohedral (Pueschel et al, 1992).…”

Plasticity of adult coralline algae to prolonged increased temperature and pCO2 exposure but reduced survival in their first generation

“…Although the genus Sporolithon is not a primary reef builder, they have a similar calcification process to reef building CCA species (e.g. Nash et al [14]) and are important members of the benthic community in tropical reefs, and the negative response of the germlings to combined environmental stressors may impact some essential functions of CCA in coral reefs under future global change scenarios.…”

“…The responses of CCA to changes in their environment are variable, having been found to be mostly either vulnerable or insensitive to both increasing ocean temperature and/or OA [9][10][11][12]. CCA secrete the most soluble polymorph of CaCO 3 , high Mg-calcite [13] and their process of calcification is suggested to be biologically induced rather than controlled [14], and therefore are thought to be particularly sensitive to changes in seawater carbonate chemistry that occur with OA [15][16][17][18][19]. In saying this, however, there are examples of CCA taxa that are well adapted to extreme environments, such as the freshwater CCA Pneophyllum cetinaensis [20], and the arctic-subarctic Clathromorphum genus [21,22], which is able to calcify under dark conditions [23].…”

“…Sporolithon spp. mineralise high Mg-calcite within their cell walls like the primary reef building CCA species [14]. Therefore, furthering our knowledge on the responses of Sporolithon to elevated temperature and OA [40] is not only relevant to, but vital for understanding the effects of such stressors on benthic reef communities more broadly and those species that function to cement the framework of coral reefs.…”