Complex morphologies of biogenic crystals emerge from anisotropic growth of symmetry-related facets

Avrahami, Emanuel M.; Houben, Lothar; Aram, Lior; Gal, Assaf

doi:10.1126/science.abm1748

Cited by 42 publications

(52 citation statements)

References 34 publications

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“…In spiders, prismatic crystals were proposed to form on sheets within a crystal vesicle( 24 ) and to be comprised of 25 nm-thick crystal lamellas stacks ( 25 ). Studies on inorganic biocrystals suggest that crystal morphogenesis is controlled by physical confinement of growth by the delimiting membrane of the organelle( 26 ). The rationale here being that confinement allows for growth rate manipulations, which are sufficient to produce a variety of complex shapes.…”

Section: Figurementioning

confidence: 99%

“…The formation of thin plate-like guanine crystals requires overriding the strong intrinsic tendency of crystals to grow as prisms and to preferentially express the thermodynamically disfavored (100) face (parallel to the H-bonded plane)( 10 ). Recent studies suggest that the control over morphology of certain biocrystals can be obtained via confinement, i.e., a physical block of growth by the delimiting membrane( 26 ). However, we found that the initial crystal formation within the iridosome lumen occurs at a considerable distance from the delimiting membrane.…”

Section: Figurementioning

confidence: 99%

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Biogenic plate-like guanine crystals form via templated nucleation of thin crystal leaflets on amyloid scaffolds

Eyal

Deis

Varsano

et al. 2022

Preprint

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Controlling the morphology of crystalline materials is challenging, as crystals have a strong tendency towards thermodynamically stable structures. Yet, organisms form crystals with distinct morphologies, such as the plate-like guanine crystals produced by many terrestrial and aquatic species for light manipulation. Regulation of crystal morphogenesis was hypothesized to entail physical growth restriction by the surrounding membrane, combined with fine-tuned interactions between organic molecules and the growing crystal. Using cryo electron tomography of developing zebrafish larvae, we found that guanine crystals form via templated nucleation of thin leaflets on preassembled scaffolds made of 20-nm-thick amyloid fibers. These leaflets then merge and coalesce into a single plate-like crystal. Our findings provide new insights into how organisms control the morphology and, thereby, the optical properties of crystals.

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Section: Figurementioning

confidence: 99%

Section: Figurementioning

confidence: 99%

Biogenic plate-like guanine crystals form via templated nucleation of thin crystal leaflets on amyloid scaffolds

Eyal

Deis

Varsano

et al. 2022

Preprint

Self Cite

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“…Understanding how organisms control the formation of biogenic crystals is the central, widely studied question of (inorganic) biomineralization [1][2][3][4][5][6] . However, the mechanisms underlying the formation of organic bio-crystals, which are ubiquitous in animals [6][7][8][9] and plants 10 , remain a mystery.…”

Section: Introductionmentioning

confidence: 99%

The Formation of Biogenic Guanine Crystals Closely Resembles Melanosome Morphogenesis

Wagner

Upcher

Maria

et al. 2022

Preprint

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Animals precisely control the morphology and assembly of highly reflective guanine crystals to produce diverse optical phenomena used in coloration and vision. However, little is known about how organisms regulate crystallization to produce optically useful crystal morphologies which express highly reflective crystal faces. Guanine crystals form inside iridosome vesicles within specialized chromatophore cells called iridophores. By following the formation of iridosomes in developing scallop eyes we show that, despite their different physical properties, the morphogenesis of iridosomes bears a striking resemblance to melanosome morphogenesis in vertebrates. A key finding is that pre-assembled intravesicular fibrillar sheets template crystal nucleation, growth, and orientation, dictating the formation of optically functional, but thermodynamically disfavored plate-like habits. The common control mechanisms for melanin and guanine formation inspire new approaches for manipulating the morphologies and properties of molecular materials.

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“…Biominerals are crystalline composites formed by living organisms 25,33,34,35,36,37,38,39,40 . Different animals, such as corals, sea urchins, and mollusks diverged from one another 600-800 million years ago (Ma) 3,4 , but started making their biominerals during the Phanerozoic (541 Mapresent), with the oldest fossils of biominerals for these three phyla being 510, 270, and 535 Ma, respectively 3,41,42,43 .…”

Section: Introductionmentioning

confidence: 99%

Convergent, slightly misoriented crystals toughen corals and seashells

Gilbert

Lew

Stifler

et al. 2022

Preprint

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The hardest and toughest tissues formed by living organisms are organic-mineral composites termed biominerals 1,2. When they are crystalline, their mesostructure includes the nano- and micro-scale crystallite size, shape, arrangement, and orientation. Mesostructures vary enormously across marine CaCO3 biominerals (aragonite, vaterite, calcite) because they result from divergent evolution: biominerals were formed long after organisms diverged from one another 3,4. Despite such diversity, CaCO3 marine biominerals share a convergent character: adjacent crystals are similarly oriented 5-32. The reason for such convergence is unclear. Here, we show with quantitative, precise measurements at the nanoscale that the slight misorientation is consistently between 1°-40° in diverse biominerals. Can this slight misorientation confer a desirable materials property and therefore an evolutionary advantage to the forming organisms? We test and confirm this hypothesis with nanoindentation in diverse biominerals, geologic aragonite, and in abiotic, slightly misoriented, synthetic spherulites. Molecular dynamics (MD) simulations of bicrystals reveal that aragonite, vaterite, calcite, exhibit toughness peaks when they are misoriented by 10°, 20°, 30°, respectively, demonstrating that slight misorientation alone increases crack deflection and therefore fracture toughness. Slight misorientation, along with other previously known and co-existing toughening mechanisms, was selected repeatedly and convergently, during the course of evolution, to postpone fracture and thus provide organisms with competitive advantage. We anticipate slight misorientation-toughening to be a starting point for more sophisticated materials synthesis and additive manufacturing in many fields. Compared to previously known toughening mechanisms, in fact, the advantages of slight misorientation are that it can and does occur in synthetic materials, it requires one material only and no specific top-down architecture, it is easily achieved by self-assembly of organic molecules (e.g. aspirin, chocolate), polymers, metals, and ceramics 29 well beyond biominerals.

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Complex morphologies of biogenic crystals emerge from anisotropic growth of symmetry-related facets

Cited by 42 publications

References 34 publications

Biogenic plate-like guanine crystals form via templated nucleation of thin crystal leaflets on amyloid scaffolds

Biogenic plate-like guanine crystals form via templated nucleation of thin crystal leaflets on amyloid scaffolds

The Formation of Biogenic Guanine Crystals Closely Resembles Melanosome Morphogenesis

Convergent, slightly misoriented crystals toughen corals and seashells

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