Calcite crystal orientation patterns in the bilayers of laminated shells of benthic rotaliid foraminifera

Yin, Xiaofei; Griesshaber, Erika; Checa, António; Nindiyasari-Behal, F.; Sánchez-Almazo, Isabel; Ziegler, Andreas; Schmahl, Wolfgang W.

doi:10.1016/j.jsb.2021.107707

Cited by 20 publications

(19 citation statements)

References 82 publications

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“…The EBSD map of the hyaline planktic foraminifer G. ruber albus shows 3-10 μm sized regions of coherent crystallographic orientation to be strongly aligned with the c-axis oriented perpendicular to the chamber surface (Figure 5). This organization seems to be a common principle observed in a variety of planktic and benthic foraminifers, with similar reports of grain sizes for planktic (∼10 μm) and benthic (∼20 μm) species (Pabich et al, 2020;Read, 2019;Yin et al, 2021). The strict crystallographic orientation of the test calcite c-axes is thought to reflect the presence of a tightly controlled, biochemically-governed mechanism in hyaline foraminifers, which is facilitated by epitaxial crystallisation on organic templates (Ní Fhlaithearta et al, 2013;Towe & Cifelli, 1967;Weiner & Erez, 1984).…”

Section: Micrometer Sized Regions Of Coherent Scatteringsupporting

confidence: 79%

“…At the same time, the lattice orientation remains the same between different nanocrystallites of the same mesocrystal, which results in diffraction patterns similar to single crystals for each distinct mesocrystal, visible as, for example, spots instead of rings in XRD (Bergström et al., 2015; Cölfen & Antonietti, 2005; Gal et al., 2014; Jehannin et al., 2019; Sturm & Cölfen, 2016). This is confirmed for hyaline foraminiferal calcite by EBSD (micrometer‐sized regions of coherent crystallographic orientation, Figure 5; and Pabich et al., 2020; Read, 2019; Yin et al., 2021).…”

Section: Discussionmentioning

confidence: 61%

“…Based on light‐microscopy observations and electron backscatter diffraction (EBSD) measurements, which show an alignment of test crystallite c ‐axes towards the outer surface of the chamber in hyaline planktic and benthic foraminifers, it has been hypothesized that organic layers act as a template for the directed crystallisation of foraminifer test calcite (Read, 2019; Towe & Cifelli, 1967; Weiner & Lowenstam, 1986; Yin et al., 2021). To date, investigations in (mostly) benthic foraminifer species reveal that the organic matter occluded in the test calcite contains sulfonated polysaccharides and a variety of proteins and polypeptides, but neither the exact role nor location of these macromolecules in the biomineralization process have yet been identified (Frontalini et al., 2019; King & Hare, 1972; Nagai, Uematsu, Chen, et al., 2018; Nagai, Uematsu, Wani, et al., 2018; Ní Fhlaithearta et al., 2013; Robbins & Brew, 1990; Robbins & Donachy, 1991; Sabbatini et al., 2014; Stathoplos & Tuross, 1991; Tyszka et al., 2021; Weiner & Erez, 1984).…”

Section: Introductionmentioning

confidence: 99%

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Mesocrystalline Architecture in Hyaline Foraminifer Shells Indicates a Non‐Classical Crystallisation Pathway

Arns

Evans

Schiebel

et al. 2022

Geochem Geophys Geosyst

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Calcareous foraminifers are an abundant group of planktic and benthic marine unicellular organisms, which together constitute an important component of the global carbon cycle (Langer, 2008;Schiebel, 2002). Foraminifer shells (tests) can resist dissolution and diagenesis over millions of years, and hence provide an outstanding archive for climate reconstruction at high time resolution from sediment cores, which is possible via empirical calibration of chemical or physical characteristics of the shells of recent species (e.g., Fischer & Wefer, 1999;Katz et al., 2010). Despite their importance as a paleoclimate archive, the biomineralization of foraminifers is not mechanistically understood in detail, which leaves the fundamental relationship between environmental parameters and proxy data enigmatic. For example, the possible presence of residues of metastable carbonate phases such as vaterite was only recently discovered (Jacob et al., 2017), and the delivery of ions to the biomineralization site is an ongoing topic of debate (

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Section: Micrometer Sized Regions Of Coherent Scatteringsupporting

confidence: 79%

Section: Discussionmentioning

confidence: 61%

Section: Introductionmentioning

confidence: 99%

See 1 more Smart Citation

Mesocrystalline Architecture in Hyaline Foraminifer Shells Indicates a Non‐Classical Crystallisation Pathway

Arns

Evans

Schiebel

et al. 2022

Geochem Geophys Geosyst

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“…1: adjacent crystals always have similar colors. Misorientation was observed before in various biominerals 5,6,7,8,9,10,11,12,13,14,15,16,17,18,19,20,21,22,23,24,25,26,27,28,29,30,31,32 . The nanoscale misorientation of pairs of adjacent crystals, however, were never measured directly and quantitatively, and were never compared across diverse biominerals using the same method.…”

Section: Slight Misorientations Of Adjacent Crystals In Diverse Biomi...mentioning

confidence: 81%

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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“…This important characteristic was shown first for the Recent brachiopod M. truncata (Schmahl et al 2004) and is recognized as an intrinsic feature of biologically secreted carbonate hard tissues (e.g. brachiopods, molluscs, benthic and planktonic foraminifera shells and sea urchin teeth (Schmahl et al 2004;Griesshaber et al 2007;Goetz et al 2014;Yin et al 2021). The valves of rhynchonellide and terebratulide brachiopods have a uniaxial fiber texture, while the hinge shows a bimodal, occasionally even a multimodal, distribution pattern of calcite c-axes (Figs.…”

Section: Characteristics Of the Different Texturesmentioning

confidence: 86%

The architecture of Recent brachiopod shells: diversity of biocrystal and biopolymer assemblages in rhynchonellide, terebratulide, thecideide and craniide shells

et al. 2021

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Biological hard tissues are a rich source of design concepts for the generation of advanced materials. They represent the most important library of information on the evolution of life and its environmental conditions. Organisms produce soft and hard tissues in a bottom-up process, a construction principle that is intrinsic to biologically secreted materials. This process emerged early on in the geological record, with the onset of biological mineralization. The phylum Brachiopoda is a marine animal group that has an excellent and continuous fossil record from the early Cambrian to the Recent. Throughout this time interval, the Brachiopoda secreted phosphate and carbonate shells and populated many and highly diverse marine habitats. This required great flexibility in the adaptation of soft and hard tissues to the different marine environments and living conditions. This review presents, juxtaposes and discusses the main modes of mineral and biopolymer organization in Recent, carbonate shell-producing, brachiopods. We describe shell tissue characteristics for taxa of the orders Rhynchonellida, Terebratulida, Thecideida and Craniida. We highlight modes of calcite and organic matrix assembly at the macro-, micro-, and nano-scales based on results obtained by Electron Backscatter Diffraction, Atomic Force Microscopy, Field Emission Scanning Electron Microscopy and Scanning Transmission Electron Microscopy. We show variation in composite hard tissue organization for taxa with different lifestyles, visualize nanometer-scale calcite assemblies for rhynchonellide and terebratulide fibers, highlight thecideide shell microstructure, texture and chemistry characteristics, and discuss the feasibility to use thecideide shells as archives of proxies for paleoenvironment and paleoclimate reconstructions.

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Calcite crystal orientation patterns in the bilayers of laminated shells of benthic rotaliid foraminifera

Cited by 20 publications

References 82 publications

Mesocrystalline Architecture in Hyaline Foraminifer Shells Indicates a Non‐Classical Crystallisation Pathway

Mesocrystalline Architecture in Hyaline Foraminifer Shells Indicates a Non‐Classical Crystallisation Pathway

Convergent, slightly misoriented crystals toughen corals and seashells

The architecture of Recent brachiopod shells: diversity of biocrystal and biopolymer assemblages in rhynchonellide, terebratulide, thecideide and craniide shells

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