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. 2011 May 17;108(20):8367-72.
doi: 10.1073/pnas.1018495108. Epub 2011 May 2.

Unique system of photoreceptors in sea urchin tube feet

Esther M Ullrich-Lüter  1 , Sam Dupont, Enrique Arboleda, Harald Hausen, Maria Ina Arnone
Affiliations

Unique system of photoreceptors in sea urchin tube feet

Esther M Ullrich-Lüter et al. Proc Natl Acad Sci U S A. .

Abstract

Different sea urchin species show a vast variety of responses to variations in light intensity; however, despite this behavioral evidence for photosensitivity, light sensing in these animals has remained an enigma. Genome information of the recently sequenced purple sea urchin (Strongylocentrotus purpuratus) allowed us to address this question from a previously unexplored molecular perspective by localizing expression of the rhabdomeric opsin Sp-opsin4 and Sp-pax6, two genes essential for photoreceptor function and development, respectively. Using a specifically designed antibody against Sp-Opsin4 and in situ hybridization for both genes, we detected expression in two distinct groups of photoreceptor cells (PRCs) located in the animal's numerous tube feet. Specific reactivity of the Sp-Opsin4 antibody with sea star optic cushions, which regulate phototaxis, suggests a similar visual function in sea urchins. Ultrastructural characterization of the sea urchin PRCs revealed them to be of a microvillar receptor type. Our data suggest that echinoderms, in contrast to chordates, deploy a microvillar, r-opsin-expressing PRC type for vision, a feature that has been so far documented only in protostome animals. Surprisingly, sea urchin PRCs lack any associated screening pigment. Indeed, one of the tube foot PRC clusters may account for directional vision by being shaded through the opaque calcite skeleton. The PRC axons connect to the animal internal nervous system, suggesting an integrative function beyond local short circuits. Because juveniles display no phototaxis until skeleton completion, we suggest a model in which the entire sea urchin, deploying its skeleton as PRC screening device, functions as a huge compound eye.

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Conflict of interest statement

The authors declare no conflict of interest.

Figures

Fig. 1.
Fig. 1.
Tube foot expression of r-opsin in S. purpuratus. (A) Adult specimen. (Inset) Tube feet extended between spines. (B) Sp-opsin4 RNA probe (black) and antibody (yellow) clearly colocalize in disk PRCs (for details, see Fig. S2). (C) Sp-Opsin4–positive PRCs (red) at base and disk of primary podia in an early juvenile counterstained with anti-Synaptotagmin B (green), a general echinoderm nervous system marker. (D) Disk PRCs arranged around the rim of an adult tube foot disk. Sp-Opsin4 antibody labeling (red). Confocal z-stack projected onto confocal laser-scanning microscopic transmission picture. (E) Sp-Opsin4 antibody labeling of decalcified adult epidermis reveals PRC clusters at the base of two tube feet. View from former skeletal inside toward external. Note axons and single Sp-Opsin4–positive cells within the lateral nerve (latn) originally leading through tube foot pores (tf, tube foot; orange dotted line: tube foot base where it normally attaches to the skeleton; for details see Fig. S3). (F) Schematic drawing (tube foot morphology adapted from Goldschmid) (53) of disk (dPRCs) and basal (bPRCs) PRCs (red) connecting to the nervous system (green) (amp, tube foot ampulla; ske, calcite endoskeleton; tfn, tube foot nerve). (G) SEM of adult skeleton. Each tube foot covers one double-pore, one of them bearing an extra channel to accommodate the tube foot lateral nerve (arrowhead) (see also H and Fig. 4C). Orange dotted line indicates insertion of tube foot in intact animal. (H) Illustration depicting Sp-Opsin4–positive PRCs embedded in a depression of the upper tube foot nerve channel. (PRCs clipped out from fluorescent microscope picture of decalcified specimen and projected onto SEM picture of calcite skeleton of another specimen). [Scale bars, 100 μm (C–E, and G) and 10 μm (B and H).]
Fig. 2.
Fig. 2.
Tube foot expression of pax6 in S. pupuratus. (A) Tube foot whole mount (picture composed of three single photographs). Sp-pax6 RNA (purple) expressed in the stalk (note insert depicting stalk portion with peeled off epidermis) and Sp-Opsin4–positive PRCs in the disk (red). Nerve fibers stained by anti–acetylated-α-tubulin (green). (B) Sp-pax6–positive field (purple) and embedded Sp-Opsin4–positive basal PRCs (red); decalcified specimen. (C–E) Tube foot disk, lateral view; same staining methods and color depiction as applied in A (ac tub, acetylated tubulin). To enhance Sp-pax6 RNA staining, Cy3-tyramide amplification was used. (D and E) A magnification of the box in C, demonstrating presence of cell nuclei (nu; cyan) in the Sp-pax6–positive (purple) region. (F) Strong Sp-pax6 expression (purple) and Sp-Opsin4–positive PRCs (red) in developing tube feet of a juvenile sea urchin (m, mouth; sp, spine; tf, tube foot; tfn, tube foot nerve). [Scale bars, 100 μm (B and F) and 50 μm (C–E).]
Fig. 3.
Fig. 3.
Tube foot visual complex: cytological structure and connection to the nervous system. (A) Sp-Opsin4 immunostaining of sucker PRCs (hot red) close to bundles of cilia (anti–acetylated-α-tubulin immunostaining) (green). (B) SEM of ciliary field on tube foot disk epidermis. (C) TEM ultrasection showing PRC detected by immunogold labeling against Sp-Opsin4 (ep, epidermis) (for details, see Fig. S4). (D) Apical region of PRC bearing numerous microvilli (mv) and a cilium (ci) as well as a huge amount of vesicles (v) (conventional TEM). (E) EM-based scheme of tube foot disk PRC. (F) Disk Sp-Opsin4–positive PRCs connecting to apical branches of the tube foot nerve (tfn) double localized by anti–Sp-Opsin4 (red) and anti–acetylated-α-tubulin (green) (ax, axon). (G) Lateral nerve from decalcified adult epidermis. Anti–Sp-Opsin4 staining (hot red) and Sp-pax6 mRNA (dark purple). (H) S. purpuratus juvenile: Sp-Opsin4–positive basal PRCs (red) projecting axons into the developing radial nerves (radn) (green) stained by anti-SynaptotagminB. (I) Scheme of the sea urchin internal nervous system (green): the five radial nerves connecting to the oral nerve ring (onr) (a, anus; m, mouth; ske, skeleton). (J) Scheme of tube foot and spine innervations (green) and relative position of Sp-Opsin4–positive PRCs (s, spine). [Schemes (I and J) modified after Burke (10).] [Scale bars, 10 μm (A), 2.5 μm (B–D), and 25 μm (F and G).]
Fig. 4.
Fig. 4.
Visual r-opsin in sea star and phototaxis-related function of the sea urchin skeleton. (A) Juvenile Asterias rubens with optic cushions (oc) and developing tube feet (tf); (Inset) adult specimen. (B) R-opsin protein (red) in optic cushion and nerve cells labeled (green) by anti-SynaptotagminB. (C–E) 3D-visualized μCT data. (C) Volume-rendered 3D model showing two tube feet double-pores of an adult specimen of S. purpuratus and depiction of tube foot insertion (orange dotted line). One of the double-pores shows a depression leading inside the tube foot pore (tfp) (sd, skeletal depression; spb, spine base). (D) Volume-rendered 3D model showing virtual cross section of the skeleton with tube foot pore leading diagonally through the calcite stereom (ske, skeleton). Note the depression in the apical part of the pore. (E) Virtual vertical cross section of a tube foot pore showing the morphology of the skeletal depression and the resulting illumination angle (Inset: illumination angle α: 88°). (F) Early, nonphototactic, S. purpuratus juvenile, at the onset of stereom skeletogenesis. (G and H) Details from F showing basal (G) and disk (H) Sp-Opsin4–positive PRCs detected by antibody staining (red). (I) Developing skeletal elements visualized by reflection confocal laser-scanning microscopy (blue) being exclusively present at primary spine bases. (J) One-month-old, phototactic S. purpuratus juvenile with complete skeleton. (K) Detail from J showing basal and disk Sp-Opsin4–positive PRCs (red) in tube foot counterstained with anti–acetylated-α-tubulin (green). [Scale bars, 5 μm (B), 300 μm (D and E), and 100 μm (I–K).]
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