Biomineralization Within Vesicles: The Calcite of Coccoliths

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200 Young & HenriksenThe Coccolithus structure is similar, but more complex—the V-unit again forms thedistal shield but also extends onto the proximal surface as a lower tube element. The R-unit forms the proximal shield, but extends on the distal surface as an upper tube element(Fig. 3A-B). As a result, the two crystal unit types are intergrown and the proto-coccolithring is embedded within the coccolith structure and only visible on broken specimens(Fig. 4D-E). Additional complexity is seen on the proximal shield with development ofseparate upper and lower elements growing at different angles. The upper unit isapproximately radially directed (and elongate approximately parallel to the c-axis), whilethe lower element is oblique to this (Fig. 4F). Finally on complete coccoliths, the centralarea elements on both the proximal and distal surfaces appear to be composed of a massof minute elements, but interconnections between them are often visible, and atintermediate growth phases the morphology is simpler; hence these are evidently aproduct of less regular growth at a late phase.The Emiliania structure (Westbroek et al. 1989; Young 1989; Didymus et al. 1994) isunusual in being composed essentially of R-units, with the V-units confined to the protococcolithring (Fig. 6A). As a result, the individual R-units have particularly complex form,being constructed of proximal shield, distal shield, inner tube and central area elements,each of which represents a separate growth direction from the nucleation site.Ophiaster has a simple rim of alternating V- and R-units but the central area isfloored by separate elements. These elements interdigitate with the rim units, but arecrystallographically separate and have sub-tangential c-axis orientations. This structurewith three separate crystal unit types has been described in detail for Syracosphaerapulchra (Young et al. in press).NucleationThe most remarkable common feature of the heterococcoliths is the development ofthe rim from a proto-coccolith ring of simple calcite crystals with alternating sub-verticaland sub-radial c-axis orientations—the V/R structure of Young et al. (1992). This isshown by each of the illustrated examples and has been demonstrated in numerous others(e.g., Young and Bown 1997; Marsh 1999; Young et al. 1999). In some cases, it has onlybeen possible to demonstrate that the rim consists of two alternating crystal unit types,not to prove that these have different c-axis orientations. For instance, in thePapposphaeraceae the rim is clearly formed from two alternating crystal unit types (e.g.,Manton and Oates 1975), but because the entire coccoliths are usually only 1-2 micronslong and specimens are rare, it has not been possible for crystallographic orientations tobe determined. However, it seems reasonable to predict that these fit the basic V/Rmodel. This means that the first stage of biomineralization is nucleation of a ring ofcalcite nuclei with alternating orientations. This is a distinctive feature ofheterococcoliths with no obvious parallels in any other biomineralization systems and hasdemonstrably remained constant through more than 200 million years of coccolithevolution (Young et al. 1992, 1999). Moreover, nucleation controls total calciteorientation, i.e., not simply c-axis orientation, but also a-axis orientation. This isevidenced by the fact that crystal faces on adjacent elements are sub-parallel (e.g., Fig. 1,3C−G, 5A). It has also been demonstrated using SAED study of Emiliania huxleyicoccoliths (Davis et al. 1995) and AFM study of Coccolithus pelagicus and Oolithotusfragilis (Henriksen et al. in press a).A final distinctive, nucleation-related feature is that all heterococcoliths showchirality. This is seen for instance in element orientations and cross-polarized lightextinction crosses. The lower proximal shield elements of Coccolithus (Figs. 3A, 4F) area good example. These grow at an oblique angle and always show clockwise offset from
Biomineralization Within Vesicles 201the radial direction in proximal view. This chirality is related to departures of thenucleation orientations from simple orthogonal radial and vertical directions, i.e., thenucleation is chiral (Didymus et al 1994; Young et al. 1999).Thus, heterococcolith rim nucleation is characterized by a suite of features:alternation of c-axis orientations, control of a-axis orientations, stability throughevolutionary history and chirality. This very precise nucleation control can most easily beexplained in terms of control from a macromolecular template substrate. The principalalternative would be random nucleation followed by selection of favorably orientednuclei, but this should only lead to selection of c-axis directions, as is seen in many otherbiomineral systems, not total crystal orientation, which is much more rare. Similarly,chirality is a predictable result of nucleation on a biochemical substrate since virtually allorganic macromolecules are chiral and occur in natural systems as only oneenantiomorph. Therefore, a plausible model for the precise nucleation control around themargin of the organic baseplate is that a belt of macromolecular substrate occurs in thisposition with arrays of potential binding sites for calcium or carbonate ions whichpromotes nucleation of oriented calcite crystallites. Young et al. (1992, 1999), and Marsh(1999) speculated on possible geometries of such a template that could result in the V/Rpattern of evolutionarily stable alternation of nucleation directions.This hypothesis is tempting, but it has not been substantiated by direct evidence.Furthermore, although all heterococcoliths appear to have rims conforming to the V/Rmodel, additional, separately-nucleated crystals that do not fit this model often occur inthe central area of heterococcoliths. Ophiaster illustrates one rather common pattern, seenin numerous coccoliths produced by the families Syracosphaeraceae andRhabdosphaeraceae (Young et al. in press), an apparent pattern of V/R/T alternation. Thiswould require a more complex template but could still conform to the general model.Such coccoliths, however, also often have additional elements separate from the rim.There are a few such elements visible in Ophiaster (Fig. 6C). A more extreme and verybeautiful example is provided by Rhabdosphaera (Fig. 7). Here the rim, with inferredV/R structure, is very narrow and encloses a large mass of lamellar crystal units and acentral spine of intergrown crystals (Kleijne 1992). The spine structure is remarkablyelegant, consisting of five interwound spirals of crystals (Fig. 7C). The componentcrystals of the spine show regular rhombohedral faces with perfectly regular alignmentspiraling up the structure. Evidently, nucleation here is not confined to the narrow beltaround the baseplate but occurs across the base and up the spine, still with regular crystalalignment and consistent chirality. If a template is involved, it is unclear where it islocated and it lacks the V/R alternation.GrowthRegulation of calcite growth by coccolithophores is almost as remarkable as theregulation of nucleation. The crystal units sketched in Figures 3 and 6 are each singlecrystals of calcite, and their shapes are radically different from that of inorganic calcite.However, such crystals do not exist in isolation, but are parts of the complete coccolith, andmuch of the morphology is a product of interaction between adjacent crystals. Further, it isclear from the cytological observations that there is no precursor matrix for the coccolith,but rather that the coccolith grows in an expanding vesicle. The final structure of thecompleted coccoliths to a large extent an emergent result of inorganic growth of thecrystals defined by the nucleation stage, within a space defined by the expanding vesicle.Because inorganic growth directions are utilized, the precise orientation of the calcitecrystal lattice in coccolith elements is important for developing morphology. Using atomicforce microscopy, we have investigated C. pelagicus and O. fragilis coccoliths from
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Biomineralization Within Vesicles: The Calcite of Coccoliths

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