Research ArticleSTRUCTURAL BIOLOGY

Chiral switching in biomineral suprastructures induced by homochiral l-amino acid

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Science Advances  01 Aug 2018:
Vol. 4, no. 8, eaas9819
DOI: 10.1126/sciadv.aas9819
  • Fig. 1 Hierarchically organized chiral biomineralized architectures constructed of calcium carbonate.

    (A) Scanning electron microscopy (SEM) image showing coexistence of adjacent imbricated, calcitic coccolith skeletal-plate layers (cycles) oriented in the clockwise direction centrally (yellow) and in the counterclockwise direction peripherally (green) in Umbilicosphaera foliosa [reprinted with permission from (9)]. (B) Rounded, chiral (clockwise, yellow arrow) pathologic calcium carbonate vaterite otoconia from the inner ear of an aged patient [reprinted with permission from (29)]. (C) Synthetic chiral (clockwise, yellow arrow) suprastructure of hierarchically organized vaterite induced by the amino acid l-Asp as prepared in a laboratory setting.

  • Fig. 2 Chiral switching of hierarchically organized vaterite suprastructures induced by a single chiral enantiomer of amino acid.

    (A) SEM image of an initial vaterite helicoid with right-handed (counterclockwise), inclined spiraling chirality (green) as grown in the presence of l-Asp for 24 hours. (B) Achiral vaterite helicoid with straight-radiating (relative to the centroid, blue) vertical vaterite platelets formed after 3 days of growth. (C) With time, chiral switching appears first as a left-handed (clockwise, yellow) spiraling vaterite helicoid consisting of vertical vaterite platelets after 1 week of growth. (D) Again, with more time (2 weeks), achiral vaterite helicoids are formed having horizontal-surrounding vertical platelet orientation (relative to the centroid, blue). (E) Right-handed (counterclockwise, green) vaterite helicoids are found at 1 month with interlacing vertical platelets assembled into the helicoidal suprastructure (F). All platelets have nanoparticle subunit structure [inset in (F)].

  • Fig. 3 Coexistence of enantiomorphs of hierarchically organized vaterite helicoids induced by a single amino acid enantiomer (l-Asp) at high supersaturation conditions.

    SEM images of small, counterclockwise vaterite helicoids (short green arrow) having inclined platelets, medium clockwise helicoids (yellow) having vertical platelets, and large counterclockwise helicoids (long green arrows) having vertical platelets.

  • Fig. 4 Platelet layer-by-layer inclination decreases vaterite helicoid chirality toward an achiral, vertical platelet organization.

    (A to C) SEM images of the gradual decrease in chirality (green, pseudocolored at 8, 16, and 32 hours of growth) of vaterite helicoids grown in the presence of l-Asp. The helicoids are composed of inclined platelets originating from an initial achiral substrate disc core, growing to the point (note decreasing magnification) where the helicoid is symmetric and achiral [blue in (D), at 72 hours) with vertically oriented platelets at the helicoid surface, and with an increase in overall helicoid size. (E) SEM image of a cross section of a small intermediate counterclockwise chiral vaterite helicoid after FIB cutting, whose interior is composed of two regions—an initial core disc/dome and an inclined-platelet region (top panel). In the inclined-platelet region, the layer-by-layer growth produces inclined-platelet organization having an angle of 6° between a consequential daughter platelet layer (white dashed line on the daughter platelet) arising from a mother platelet layer (white solid line on the mother platelet), which leads to the decrease and disappearance of chirality of the vaterite helicoid as the platelets ascend to the vertical orientation. (F) Side view schematic of growth in the layer-by-layer inclination model where 6° inclination of 15 continuously forming platelet layers arising from an initially flat achiral core disc ascend to the first vertical platelet layer (15th dark blue line). (G) The exposed crystalline vaterite face changes from being initially the basal (001) vaterite plane (light blue) to the (100) plane (dark blue) after the formation of 15 successional nanostructured vaterite platelet layers, with all platelets formed from subunit tilted nanohexagons (19).

  • Fig. 5 Chiral switching by vertical platelet layer-by-layer rotation correlates with increasing size of vaterite helicoids during growth evolution in the presence of l-Asp.

    (A to C) SEM images at low (top) and corresponding high (bottom) magnification of clockwise (yellow arrows) vaterite helicoids during their growth evolution extending from the first transitional straight-radiating (0° reference start point) achiral vaterite helicoid as depicted previously in Fig. 4D. As helicoids grow and increase in size, vertical platelets then successionally rotate by 22.5° in the clockwise direction in each layer to reach first 22.5°, then 45°, then 67.5° relative to the start point (small yellow bars). (D) When the vertical platelets in the uppermost layer continue to rotate clockwise to the horizontal position (90° from the reference start point), the helicoid becomes achiral having the horizontal-surrounding platelet orientation (gray double-headed arrow and bar). (E to G) With further clockwise rotational growth (to reach first 112.5°, then 135°, and then 157.5°; green bars), helicoids have a counterclockwise chiral structure (green arrows). (H) Finally with additional growth, a transitional achiral state of the helicoid (180°) again appears (gray double-headed arrow, gray bar), completing a cycle to again form an achiral structure with the same morphology as that of the original straight-radiating platelet orientation (0°) of achiral helicoids (as shown earlier in Fig. 4D), but now having a much larger size attributable to the additional growth by platelet layer additions.

  • Fig. 6 Mechanism leading to chiral switching as induced by chiral amino acid enantiomer.

    (A) SEM image of a nearly achiral vaterite helicoid showing the clockwise rotation of 22.5° between two connected vertical platelets in adjacent mother (blue) and daughter (purple) layers in the rotated-platelet region. (B) A model at the (100) plane for two adjacent vertical and rotated vaterite platelet layers showing details of a consequential rotated daughter vertical platelet position relative to the mother vertical platelet position, with intervening amino acid layer, as identified by RosettaSurface computational simulation fixing the clockwise rotation at 22.5°. Vaterite crystal atoms: Ca, green; C, gray in mother layer and yellow in daughter layer; O, red. (C) High-resolution simplified image showing the configuration at the 22.5°rotation between the bottom mother vaterite layer with exposed surface calcium (green), the intervening middle l-Asp layer (blue), and the top daughter vaterite layer with exposed surface carbonates (yellow). (D) Schematic summary (of a top view) of the chiral switching of surface structures in vaterite helicoids caused by the 22.5° layer-by-layer clockwise rotation in the presence of the l-enantiomer of Asp, whose replication/amplification with further growth leads to the 180° chiral switch cycle. The entire cycle is composed of four steps with eight continuous 22.5° clockwise-rotated layers: (i) an achiral straight-radiating vertical platelet start point at 0°; (ii) a first clockwise platelet rotational step of 22.5°, which repeats in subsequent growth layers to reach 45°, and then 67.5° from the start point resulting in a clockwise chiral helicoid; (iii) a transitional horizontal-surrounding platelet orientation step that occurs at 90° from the start point, resulting in an achiral helicoid; and (iv) continued 22.5° clockwise platelet rotations to reach 112.5°, then 135°, and then 157.5° from the start point, resulting in a counterclockwise chiral helicoid. (E and F) Two-dimensional (2D) (top view) and 3D (side view) schematics of the relationship at one location for one chiral switching cycle of eight successional clockwise rotations of 22.5° of vertical platelet layer configurations, and the chiral status of the corresponding whole vaterite helicoids, as produced in the presence of the l-enantiomer of Asp.

Supplementary Materials

  • Supplementary material for this article is available at http://advances.sciencemag.org/cgi/content/full/4/8/eaas9819/DC1

    Supplementary Text

    Fig. S1. Growth of hierarchically organized vaterite suprastructures stabilized by amino acids.

    Fig. S2. Chiral switching of hierarchically organized vaterite helicoid suprastructures in the presence of single chiral d-enantiomer of amino acid (d-Asp).

    Fig. S3. Size-related uniformity among vaterite helicoids having chiral switching when grown in the presence of a single chiral enantiomer of amino acid (d-Asp) at low supersaturation conditions.

    Fig. S4. Growth evolution of hierarchically organized vaterite helicoids with respect to size and height.

    Fig. S5. Multilayering within chiral vaterite helicoids.

    Fig. S6. Instability of adjacent rotated vertical vaterite platelets caused by the addition of chiral amino acid enantiomer.

    Fig. S7. Chiral switching by platelet layer-by-layer rotation correlates with size/growth of very large helicoids.

    Fig. S8. Layer-by-layer growth models as a potential general strategy for switching chiral structures as observed in biology.

    Fig. S9. Prediction of three as-yet unfound forms of human pathologic vaterite otoconia based on the vaterite helicoid chiral switching growth model.

    Movie S1. Animation showing chiral switching in vaterite helicoidal suprastructures occurring by a vertical platelet layer-by-layer rotation mechanism in the presence of a single chiral enantiomer of acidic amino acid.

    Reference (53)

  • Supplementary Materials

    The PDF file includes:

    • Supplementary Text
    • Fig. S1. Growth of hierarchically organized vaterite suprastructures stabilized by amino acids.
    • Fig. S2. Chiral switching of hierarchically organized vaterite helicoid suprastructures in the presence of single chiral d-enantiomer of amino acid ( d-Asp).
    • Fig. S3. Size-related uniformity among vaterite helicoids having chiral switching when grown in the presence of a single chiral enantiomer of amino acid ( d-Asp) at low supersaturation conditions.
    • Fig. S4. Growth evolution of hierarchically organized vaterite helicoids with respect to size and height.
    • Fig. S5. Multilayering within chiral vaterite helicoids.
    • Fig. S6. Instability of adjacent rotated vertical vaterite platelets caused by the addition of chiral amino acid enantiomer.
    • Fig. S7. Chiral switching by platelet layer-by-layer rotation correlates with size/growth of very large helicoids.
    • Fig. S8. Layer-by-layer growth models as a potential general strategy for switching chiral structures as observed in biology.
    • Fig. S9. Prediction of three as-yet unfound forms of human pathologic vaterite otoconia based on the vaterite helicoid chiral switching growth model.
    • Legend for movie S1
    • Reference (53)

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    Other Supplementary Material for this manuscript includes the following:

    • Movie S1 (.mov format). Animation showing chiral switching in vaterite helicoidal suprastructures occurring by a vertical platelet layer-by-layer rotation mechanism in the presence of a single chiral enantiomer of acidic amino acid.

    Files in this Data Supplement:

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