8.04 Biomineralization H. C. W. Skinner Yale University, New Haven, CT, USA and A. H. Jahren Johns Hopkins University, Baltimore, MD, USA 8.04.1 INTRODUCTION 118 8.04.1.1 Outline of the Chapter 118 8.04.1.2 Definitions and General Background on Biomineralization 119 8.04.2 BIOMINERALS 120 8.04.2.1 Calcium Carbonates 120 8.04.2.1.1 Calcite 120 8.04.2.1.2 Aragonite 122 8.04.2.1.3 Vaterite 124 8.04.2.2 Silica 124 8.04.2.2.1 Opal 124 8.04.2.3 Bioapatite 125 8.04.2.4 Iron Oxides and Hydroxides 127 8.04.2.4.1 Magnetite 127 8.04.3 EXAMPLES OF BIOMINERALIZATION 129 8.04.3.1 Introduction 129 8.04.3.2 Sulfur Biomineralization 129 8.04.3.2.1 Sulfur oxidizers 130 8.04.3.2.2 Sulfate reducers 130 8.04.3.2.3 Formation of elemental sulfur 130 8.04.3.2.4 Sulfate biomineralization 131 8.04.3.3 Iron Biomineralization 131 8.04.3.3.1 Roles of iron in archea and bacteria 131 8.04.3.3.2 Bacterial iron mineral formation 132 8.04.3.3.3 Magnetotactic bacteria 132 8.04.3.4 Carbonate Biomineralization 134 8.04.3.4.1 Cyanobacteria 134 8.04.3.4.2 Cnidaria (coelenterates) 136 8.04.3.4.3 Coccoliths 137 8.04.3.4.4 Foraminifera 139 8.04.3.4.5 Echinoids 140 8.04.3.4.6 Mollusks 141 8.04.3.4.7 Arthropods 144 8.04.3.5 Silica Biomineralization 145 8.04.3.5.1 Radiolarians 145 8.04.3.5.2 Diatoms 146 8.04.3.5.3 Sponges 150 8.04.3.6 Plant Biomineralization 152 8.04.3.6.1 Introduction 152 8.04.3.6.2 Plant biominerals 152 8.04.3.6.3 Phytoliths: indicators of the environment and paleoenvironment 154 8.04.3.6.4 Funghi and lichen biomineralization 158 8.04.3.7 Vertebrate Biomineralization 158 8.04.3.7.1 Introduction 158 117 118 Biomineralization 8.04.3.7.2 Bones and bone tissues 159 8.04.3.7.3 Cartilage 165 8.04.3.7.4 Antlers 167 8.04.3.7.5 Teeth 168 8.04.3.7.6 Otoliths 171 8.04.4 SUMMARY: WHY BIOMINERALIZE? 172 8.04.4.1 Physical or Macrobiomineralization Contributions 174 8.04.4.1.1 Defense and protection through biomineralization 174 8.04.4.2 Chemical or Microbiomineralization Contributions 174 ACKNOWLEDGMENTS 175 REFERENCES 175 8.04.1 INTRODUCTION will continue to do so, an essential ingredient for establishing and maintaining Earth’s environment Biomineralization is the process by which in the future as in the past (Figure 1). living forms influence the precipitation of mineral materials. The process creates heterogeneous accumulations, composites composed of biologic 8.04.1.1 Outline of the Chapter (or organic) and inorganic compounds, with inhomogeneous distributions that reflect the It is only with the advent of more sensitive, environment in which they form. The products higher-resolution techniques that we can identify are, however, disequilibrium assemblages, created the exact mineral components, and appreciate the and maintained during life by dynamic meta- precision control exercised by the life forms on bolism and which, on death, may retain some of their mineralized structures, and the potential that the original characteristics. The living forms their formation and evolution are responses to the discussed in this chapter produce carbonate, environment and climatic, or any other pervasive phosphate, oxalate, silica, iron, or sulfur-contain- geochemical changes. We first present the ing minerals illustrating the remarkable range of crystal chemistry, or mineralogy, of some of the biomineralization chemistries and mechanisms. common minerals that are encountered in Biomineralization, in the broadest use of the term, biomineralization (Section 8.04.2)andthen has played a role in Earth cycles since water provide examples from the range of life forms. appeared on the surface. The general perception We start with the Archea and Bacteria although that the onset of biomineralization coincides with we are just beginning to investigate their the appearance of fossils that left “hard parts” mineralization processes. However, these primi- amenable to analysis is marked geologically as the tive forms were probably the first to generate the dawn of the Cambrian. At least for some of us, the mechanisms that led to the accumulation of origins of life, and possibly biomineralization, elements, the precursor to the formation of go back 3.8 Gyr. The startling chemical and bio- biominerals. The details of the mechanisms and logical range encompassed by the term biominera- the ranges of possible creatures in these classes lization implies that life forms have adapted and remain to be fully defined and understood. altered geoenvironments from the beginning, and However, we consider them an essential base to Figure 1 The “tree of life” (source Raven et al., 1999, figure 13.8, p. 270). Introduction 119 any biomineralization discussions. Further, and calcite formation for the group of algae the perhaps most intriguing, many other biominera- coccolithophoridae (Section 8.04.3.4.3). Another lizing forms incorporate them as symbionts. illustration of the diversity of intracellular bio- Following these opening sections, we move mineralization is found in the freshwater green onto CaCO3 deposition associated with cyano- alga Spirogyra hatillensis T. that contains calcium phytes (photosynthetic cyanobacteria) that marks oxalate inclusions. The inclusions are not asso- the end of the Precambrian period, ,0.6 Gyr ago ciated with the central vacuole, but instead are in (Riding, 1982). At the start of the Cambrian period cytoplasmic strands (Pueschel, 2001). (,570 Myr ago), calcareous skeletons appear; With the advent of eukaryotes, subdivisions rapidly and dramatically (within 40–50 Myr) within the cell, or compartments, were created. some form of biomineralized structures appear Within these subcellular compartments, or specia- in all existing phyla. Since that time only corals, lized anatomical sites, mineralization may be some algae, and the vertebrates have developed facilitated, with the result that biomineralization new skeletons in the marine habitat (Simkiss and became more extensive and diverse. By creating Wilbur, 1989); thus, the obvious developments of lipid membranes, the eukaryotes could selectively biomineralization are concentrated into ,1% of “pump” ions and bioaccumulate them in a small Earth’s history, along with all other major volume. In plants, this subcellular compartment is diversifications of life. We present information, usually a vacuole (Matile, 1978), whose membrane and include references to works we think will be may serve both as a pre-existing surface for most helpful to geochemists, on selected inverte- nucleation and as the ultimate determinant of brate and vertebrate skeletons many of which mineral shape, as the crystal(s) grow to fill the have a vast literature available. We select a few vacuole (Simkiss and Wilbur, 1989). Most ion structures, such as teeth (in chitons and humans), pumps translocate ions against electrochemical because they are examples of different minerali- gradients (Carapoli and Scarpa, 1982) accom- zing systems whose tissue textures, and mech- plished either by attaching the ion to a carrier anisms, are unique, and because they may be, or molecule that is moving with an electrochemical have been, important to geochemical studies. In gradient, or by directly using ATP as an energy looking to future opportunities we include brief source for the translocation. Often described introductions to otoliths and antlers, because they for Ca2þ transport, similar transport mechanisms offer novel sampling sites to test geochemical have been suggested to supply the anions that variations in the present environment. control the onset of mineral deposition in cells The importance of the survival of land-based (Simkiss and Wilbur, 1989). Like cations, anions communities on plants suggested that our purview are involved in a wide variety of cell activities. must include plant biomineralization, the Primary among them is the ability of anionic materials, mechanisms, and strategies. For our complexes, e.g., carbonate and phosphate, to act as summary we ask “why biomineralize?” and offer a inorganic pH buffers. In support of the anion- few suggestions based predominantly on plant supply hypothesis, it has long been recognized that researches. The reasons for biomineralization we there is a positive relationship between photosyn- have outlined are appropriate to other mineral- thetic rate (acquisition of CO2) and rate of calcite producing life forms, and have often been biomineralization in algae. Specific studies have discussed. However, in the process of reviewing shown that when Corallina officianalis algae the evolutionary development, some novel achieve a certain level of photosynthesis, the approaches, if not answers, to this basic question relationship between calcite biomineralization are preferred. rate and CO2 acquisition is roughly linear (Pentecost, 1978). An organic matrix or pre-existing nucleation 8.04.1.2 Definitions and General Background surface is usually considered to be the determining on Biomineralization feature in many systems, especially the higher biomineralizing systems, such as the vertebrates We classify biomineralization in our examples (Section 8.04.3.7). Organic matrices within bio- either as extracellular or as intracellular (Pentecost, mineralizing plant vacuoles (Webb et al., 1995) 1985a) and include the specific cell types if provide the sites where “seed” cations bind as loose known. We follow the standard definitions of chelates (Tyler and Simkiss, 1958), and can be Borowitzka (1982) that extracellular biominerali- alternately soluble and insoluble (Wheeler et al., zation involves inorganic, often crystalline, 1981), or a combination of the two (Degens, 1976). materials forming on the outer wall of the cell, Several nucleation centers may be present within a within the cell wall, or in the immediate surround- matrix, and each may grow independently, and ing tissue areas, and is the usual type of perhaps produce similar crystallographically biomineralization.