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The ommatidia of Arca noae: a three-tier structure with a central light-guiding element for the receptor cell

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Abstract

The compound eyes of ark clams appear to function as an optical system to trigger shell closure against predators. We have analyzed the structure of the ommatidia of Arca noae by thin section electron microscopy and serial sectioning, Concanavalin A–gold labeling and acid phosphatase cytochemistry. Our results demonstrate that the ommatidia are a three-tier structure composed of a central single receptor cell, surrounded and covered by proximal pigment cells followed by rows of distal pigment cells. The receptor cells of Arca noae have no lens and the disks of their receptive segment are derived from sensory cilia. The distal mitochondrial segment in the cytoplasm between the nucleus and the receptive segment is surrounded by a mass of Concanavalin A-reactive glycogen particles. Although both, proximal and distal pigment cells have numerous microvilli, only those of the proximal pigment cells form a well-aligned brush border. The microvilli of the latter are ≈9–11 μm long and have a diameter of ≈70–80 nm. Numerous microlamellar bodies cover them. The microlamellar bodies are stored in acid phosphatase-negative secretory granules of the pigment granule-free apical cytoplasm of proximal pigment cells before their secretion. Observation of living compound eyes indicated that the apex of proximal pigment cells transmitted significantly more light than the surrounding distal pigment cells. Hence, the regular geometry of the brush border seems to be a light-guiding structure for receptor cells similar to an optical fiber.

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Acknowledgments

We thank Mrs. Annette Roulier for excellent artwork. This work was supported by World Class University (WCU) program through the National Research Foundation (NRF) of Korea funded by the Ministry of Education, Science and Technology (MEST) (Grant no. R31-10086), the Kantons of Zurich, Basel and Basel-Landschaft, Switzerland and the Swiss National Science Foundation.

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Authors and Affiliations

  1. Department of Integrated OMICs for Biomedical Science, WCU Program of Graduate School, Yonsei University, 134 Shinchon-dong, Seodaemun-gu, Seoul, 120-749, South Korea

    Jürgen Roth

  2. Division of Cell and Molecular Pathology, Department of Pathology, University of Zurich, 8091, Zurich, Switzerland

    Jürgen Roth & Bruno Guhl

  3. Center for Microscopy and Image Analysis, University of Zurich-Irchel, 8057, Zurich, Switzerland

    Bruno Guhl

  4. Biozentrum, Department of Cell and Developmental Biology, University of Basel, 4056, Basel, Switzerland

    Urs Kloter & Walter J. Gehring

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  1. Jürgen Roth
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  2. Bruno Guhl
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  3. Urs Kloter
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  4. Walter J. Gehring
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Correspondence to Jürgen Roth.

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418_2011_828_MOESM1_ESM.tif

Supplemental Fig. 1. (A-C) Microvilli of proximal pigment cells form an aligned brush border (BB), whereas those of the distal pigment cells (DPC) are loosely arranged (MV). RC: receptor cells. Scale bars: 2.5 μm (A), 0.9 μm (B), 0.36 μm (C). (TIFF 5107 kb)

418_2011_828_MOESM2_ESM.tif

Supplemental Fig. 2. (A) Details from the apical cytoplasm of receptor cells containing a Golgi apparatus (GA) with associated small vesicles (arrowheads) as well as glycogen particles (asterisks). (B) Some mitochondria of the distal mitochondrial segment (DMS). The space between them and the lateral plasma membrane is filled with glycogen particles (asterisk). Arrowheads point to small vesicles in the rim of cytoplasm. Scale bars: 0.27 μm (A), 0.14 μm (B) (TIFF 3421 kb)

418_2011_828_MOESM3_ESM.tif

Supplemental Fig. 3. High resolution micrographs of longitudinal (A) and cross (B) sections from the brush border of proximal pigment cells with its microlamellar bodies. Scale bars: 0.1 μm (A), 0.19 μm (B) (TIFF 3669 kb)

418_2011_828_MOESM4_ESM.tif

Supplemental Fig. 4. Longitudinal (A) and oblique (B) sections of the brush border of proximal pigment cells. The uppermost part and the tips of the microvilli are free of microlamellar bodies, which becomes very obvious in the oblique sectioned brush border. Scale bars: 88 nm (A), 100 nm (B) (TIFF 5152 kb)

418_2011_828_MOESM5_ESM.tif

Supplemental Fig. 5. (A-C) Details from proximal pigment cells (PPC) with clusters of large vesicles (V), which contain microlamellar bodies. This part of the cytoplasm of the PPCs indents in a receptor cell (RC). BB: brush border of PPC. Gly: glycogen particles of RC. Scale bars: 0.35 μm (A, B), 0.28 μm (C) (TIFF 4754 kb)

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Roth, J., Guhl, B., Kloter, U. et al. The ommatidia of Arca noae: a three-tier structure with a central light-guiding element for the receptor cell. Histochem Cell Biol 136, 11–23 (2011). https://doi.org/10.1007/s00418-011-0828-9

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