Research ArticleOCEANOGRAPHY

Nanocrystals as phenotypic expression of genotypes—An example in coralline red algae

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Science Advances  12 Feb 2020:
Vol. 6, no. 7, eaay2126
DOI: 10.1126/sciadv.aay2126
  • Fig. 1 Basic CRA cell wall ultrastructure.

    SEM images of epithallial cells of L. kotschyanum (Sesoko-jima, Japan; see Supplementary Materials for lower-magnification image of the same specimen) and a sketch showing the idealized organization and features of a CRA cell with numbered rectangles representing the position of the SEM images (1) and (2): (a) rhombohedral PW crystallites of Lithophyllum (see Fig. 5); (b) SW crystallites organized in perpendicular rods typical for the Lithophyllum-type cell wall (Fig. 2); (c) cell fusions or secondary pit connection connecting two adjacent filaments; (d) primary pit connection connecting the cells within CRA filaments; (e) innermost organic layer (i.e., the plasma membrane; Fig. 2) lining the interior of the calcified SW; and (f) outermost organic cell wall layer equivalent to the surface of the ML (see Fig. 2).

  • Fig. 2 Cell wall organization and the four CRA cell wall types.

    (1) Crystallites forming along polysaccharide filaments of a recently divided cell with a not yet fully calcified cell wall (N. strictum). The model showing the organic components in the CRA cell wall (1) is based on ultrastructure research on both higher plants and algae including CRA (27, 40, 42, 45). (2) Fanning rod-like crystal aggregates formed by the SW polysaccharide matrix of the Sporolithaceae (Sporolithon spp.). (3) Dense crystal fans of the Lithothamnion-type SW present in the Hapalidiaceae (L. glaciale and Phymatolithon sp.). (4) Perpendicular rod-shaped crystal structures of the Lithophyllum-type SW (Porolithon spp., Hydrolithon sp., Lithophyllum spp., and Titanoderma sp.). (5) Mastophora-type cell wall with the SW crystallites organized in undifferentiated layers (Mastophora sp.; Neogoniolithon spp.).

  • Fig. 3 Detail of the generalized CRA thallus structure.

    (1) Overview and graphical representation of the L. kotschyanum (Guam) thallus showing two fully formed epithallial layers and several recently divided epithallial cells above meristem cells that show increasing secondary calcification toward their lower base. (2) Enlarged SEM image showing the two epithallial layers; the lower portion of the cells with alteration of the primary crystallites at the contact surface between cells of E2. This effect is likely related to ongoing calcification in the PW and the ML between cells, although dissolution due to seawater interactions cannot be fully disregarded for the alteration present in E2. (3) Further close-up of E1 showing clear ongoing calcification along the PW and ML merging individual crystallites leading to their typical appearance seen in the primary layer (= interfilament calcite).

  • Fig. 4 PW calcification.

    (1) PW crystallites covering epithallial cells of L. kotschyanum (Dubai). White arrowheads indicate the organic layer covering the crystallites. (2) Epithallial cell of N. fosliei (Safaga, Egypt) covered by rod-shaped crystallites (white arrowhead) within an organic matrix (gray arrowhead). Interior of the cell wall consists of primary crystallites (black arrowhead) surrounding the inner cell wall (= plasma membrane). (3) Recrystallization of primary crystallites along an exposed PW of S. yendoi (Japan; white arrow). Black arrowhead points to primary crystallites fusing into the PW (= ML) between the epithallial (E) and meristem cells (M); note the thickened cell wall of the trichocyte (T) and cell fusions (CF). (4) Close-up of an epithallial cell wall and fully calcified meristem cell. The dashed line separates the secondary and recrystallized PW. White arrowheads show polysaccharide microfibrils. (5) Meristem of L. pygmaeum (Guam) showing cell elongation during enhanced thallus growth. White arrows show SW terminations. Cell wall calcification above is very weak, which led to cells becoming squashed during specimen preparation (seen also in Fig. 3). (6) Close-up of the squashed part (5), with primary crystallites in the PW (white arrowheads). pPC, primary pit connection.

  • Fig. 5 Comparison of molecular and morphologic phylogeny.

    Upper phylogenetic tree shows the hierarchical position of the major diagnostic morphological characters used herein. The proposed tree is compared to the ribosomal loci (SSU and LSU) and encoding markers (psbA and COI) derived from the molecular phylogeny of Bittner et al. in 2011 (51) and allows the identification of all major molecular phylogenetic clades of Corallinacea [sensu Rösler et al. (49)] and distinguishing them from the Sporolithaceae and Hapalidiaceae based on three easily identifiable morphological features: (A) reproductive organs, (B) SW structures (see Fig. 2), and (C) the dominant morphotype of epithallial cell wall crystallites. (1) Sporolithon: granules; (2) Hapalidiaceae (Lithothamnion and Phymatolithon): blocks and granules; (3) Mastophoroideae (Mastophora sp.): rods and rhombic plates; (4) Neogoniolithideae (Neogoniolithon spp.): (hexagonal) rods; (5) Metagoniolithoideae (Porolithon spp.): rhombic blocks organized in rods; (6) Hydrolithoideae (Hydrolithon sp.): rhomboids organized in chains; (7) SHG (S. yendoi): elongated rhombic plates; (8) Lithophylloideae (Lithophyllum spp./Titanoderma sp.): rhombic plates (sometimes irregularly fused). Detailed SEM images of the diagnostic cell wall ultrastructures can be found in Supplementary Materials. The DNA sequence–based phylogenetic clades and names assigned to these clades were adapted from Bittner et al. (51) and not updated to more recent DNA sequence–based revisions of CRA phylogeny (49).

Supplementary Materials

  • Supplementary material for this article is available at http://advances.sciencemag.org/cgi/content/full/6/7/eaay2126/DC1

    Fig. S1. Supporting image to Fig. 1, showing the heavily calcified thallus portion of this specimen of Lithophyllum kotschyanum (Sesoko-jima, Japan).

    Fig. S2. Primary and secondary crystallization of Porolithon gardineri (Safaga, Egypt).

    Fig. S3. Morphological overviews of L. kotschyanum (Safaga, Egypt), Lithophyllum pygmaeum (Dubai, United Arab Emirates), Titanoderma byssoides (Gavdos, Greece), and S. yendoi (Sesoko-jima, Japan).

    Fig. S4. Morphological overviews of Porolithon okodes (Safaga, Egypt), P. gardineri (Safaga, Egypt), and Hydrolithon reinboldii (Hawaii, USA).

    Fig. S5. Morphological overviews of Neogoniolithon strictum (Florida, USA), Neogoniolithon fosliei (Safaga, Egypt), and Mastophora rosea (Guam).

    Fig. S6. Morphological overviews of Lithothamnion glaciale (Rebbenesøya, Norway) and Phymatolithon sp.

    Fig. S7. Plate showing the SW structure and exposed primary layers deeper in the coralline algal thallus of L. kotschyanum (Safaga, Egypt), L. pygmaeum (Guam), T. byssoides (Gavdos, Greece), Porolithon onkodes (Safaga, Egypt), Porolithon gardineri (Safaga, Egypt), H. reinboldii (Dubai, United Arab Emirates), and S. yendoi (Sesoko-jima, Japan).

    Fig. S8. Plate showing the SW structure and exposed primary layers deeper in the coralline algal thallus of L. glaciale (Rebbenesøya, Norway), Phymatholithon sp. (Rebbenesøya, Norway), Sporolithon ptychoides (Safaga, Egypt), N. strictum (Rodriguez Key, Florida, USA), N. fosliei (Safaga, Egypt), and M. rosea (Guam).

    Fig. S9. SEM image showing details of the PW crystallites present on the topmost epithallial cell row of the major CRA clades as shown in Fig. 5.

    Table S1. List of the analyzed samples with the corresponding locations where the specimens were collected.

    Table S2. Binary matrix of morphological criteria assigned for each taxon.

    References (5961)

  • Supplementary Materials

    This PDF file includes:

    • Fig. S1. Supporting image to Fig. 1, showing the heavily calcified thallus portion of this specimen of Lithophyllum kotschyanum (Sesoko-jima, Japan).
    • Fig. S2. Primary and secondary crystallization of Porolithon gardineri (Safaga, Egypt).
    • Fig. S3. Morphological overviews of L. kotschyanum (Safaga, Egypt), Lithophyllum pygmaeum (Dubai, United Arab Emirates), Titanoderma byssoides (Gavdos, Greece), and S. yendoi (Sesoko-jima, Japan).
    • Fig. S4. Morphological overviews of Porolithon okodes (Safaga, Egypt), P. gardineri (Safaga, Egypt), and Hydrolithon reinboldii (Hawaii, USA).
    • Fig. S5. Morphological overviews of Neogoniolithon strictum (Florida, USA), Neogoniolithon fosliei (Safaga, Egypt), and Mastophora rosea (Guam).
    • Fig. S6. Morphological overviews of Lithothamnion glaciale (Rebbenesøya, Norway) and Phymatolithon sp.
    • Fig. S7. Plate showing the SW structure and exposed primary layers deeper in the coralline algal thallus of L. kotschyanum (Safaga, Egypt), L. pygmaeum (Guam), T. byssoides (Gavdos, Greece), Porolithon onkodes (Safaga, Egypt), Porolithon gardineri (Safaga, Egypt), H. reinboldii (Dubai, United Arab Emirates), and S. yendoi (Sesoko-jima, Japan).
    • Fig. S8. Plate showing the SW structure and exposed primary layers deeper in the coralline algal thallus of L. glaciale (Rebbenesøya, Norway), Phymatholithon sp. (Rebbenesøya, Norway), Sporolithon ptychoides (Safaga, Egypt), N. strictum (Rodriguez Key, Florida, USA), N. fosliei (Safaga, Egypt), and M. rosea (Guam).
    • Fig. S9. SEM image showing details of the PW crystallites present on the topmost epithallial cell row of the major CRA clades as shown in Fig. 5.
    • Table S1. List of the analyzed samples with the corresponding locations where the specimens were collected.
    • Table S2. Binary matrix of morphological criteria assigned for each taxon.
    • References (5961)

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