Challenges in Establishing Criteria for the Recognition of Biominerals (Biosignature)

Morphology and uniform size of extracellular or intracellular biominerals are often taken as evidence of biological activity in natural environments and ancient rocks. However, morphology alone is insufficient and a deeper understanding of the crystal growth mechanisms in abiotic and biogenic systems is necessary if we are to establish criteria for recognizing biominerals in natural systems in both terrestrial and extraterrestrial environments. To distinguish between exclusively inorganic and biologically controlled crystallization, we conducted comparative abiotic and biogenic laboratory experiments and investigated the nucleation and growth characteristics of carbonate and phosphate (hydroxyapatite) minerals. Advanced imaging and analytical techniques, including cryo-electron tomography (cryo-ET), immunogold labeling, freeze-fracture and nano secondary ion mass spectrometry (NanoSIMS), revealed that both protein and inorganic ions influence the crystal growth and morphology. Nevertheless, the mode of crystal growth was distinct in the two modes of crystallization. Deviation from the ideal crystal habit was more pronounced in protein-based nucleation and growth compared to the abiotic system. For hydroxyapatite, size, shape and composition of the crystals were identical for the three different biogenic systems (i.e., serum, bacteria, and mammalian cells). In contrast, crystal morphology in the abiotic system was variable and dependent upon the initial composition of the solution and experimental conditions. These results suggest that in biogenic systems there is a common mechanism for the precipitation of biominerals. As we observed an association of specific proteins with crystal growth, it is likely that the nucleation and growth of biominerals is mainly controlled by the proteins; however, the nature of the interaction of the protein with the crystal faces remains unresolved. Although the differences in growth patterns between abiotic and biogenic crystals may provide potential indicators of biological activity within geological systems, it is difficult to apply this approach to ancient samples.