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Inception of bioluminescent symbiosis in early developmental stages of the deep-sea fish, Coelorinchus kishinouyei (Gadiformes: Macrouridae)

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Abstract

Larvae and juveniles of the macrourid fish Coelorinchus kishinouyei, captured from the near-bottom habitat (ca. 1–10 m above the seafloor) at 186 to 500 m depth in Suruga Bay, Honshu, Japan, were examined for the presence, developmental state, and bacterial colonization of the fish’s internal ventral light organ. The specimens ranged from 3.6 mm to 8.5 mm head length, and all exhibited an external cluster of melanophores expanding anteriorly from around the anus that is thought to indicate the presence of an internal light organ. Histological analysis revealed the presence of a light organ in all examined specimens. In smaller specimens, the light organ was seen as a small nub of tissue associated with the intestine near the anus; the light organ gradually elongated anteriorly in larger specimens to form a bean-shaped structure composed of hollow, finger-like chambers. Bacteria were present within the light organ chambers of some, but not all larvae and all juveniles. In light organs not yet colonized by bacteria, the chambers exhibited a generally uniform appearance over their entire length. In colonized light organs, the bacteria were consistently present at the anterior-most tips of the chambers; furthermore, cells comprising chambers colonized by bacteria were swollen, and upon bacterial colonization the orientation of the chambers began to change from anterior–posterior to dorsal–ventral. The colonizing bacteria were identified as Photobacterium kishitanii based on sequence analysis of the luxA gene. These results suggest that formation of the light organ in C. kishinouyei begins during the fish’s pelagic phase, but that bacterial colonization of the light organ occurs after the larvae have reached the near-bottom habitat. Furthermore, colonization of the nascent light organ by P. kishitanii induces morphogenetic changes in the light organ.

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Acknowledgments

We thank I. Hashigaya, captain of the Tokai University T/V Hokuto, and H. Sakata, chief engineer, for assistance with collecting fish, M. Inawashiro (Tokai University) for technical assistance, and J. Poore and J. Harrison (University of Michigan) for assistance with histology. We thank also H. Endo (Kochi University) for the kind gift of the reprint of the 1970 publication of Prof. O. Okamura. DNA sequencing was carried out by one of us (K.S.), with the assistance of the staff of Tokai University and the Laboratory of Marine Biochemistry of the University of Tokyo, and by staff of the University of Michigan DNA Sequencing Core. This work was supported by grant OISE-1027773 from the National Science Foundation.

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Authors and Affiliations

  1. Department of Ecology and Evolutionary Biology, University of Michigan, Ann Arbor, Michigan, 48109, USA

    Paul V. Dunlap & Tory A. Hendry

  2. Department of Fisheries, School of Marine Science and Technology, Tokai University, Orido Shimizu, Shizuoka, 424-8610, Japan

    Munehiro Takami, Sonoka Wakatsuki, Keijiro Sezaki & Atsushi Fukui

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  1. Paul V. Dunlap
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  2. Munehiro Takami
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  3. Sonoka Wakatsuki
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  4. Tory A. Hendry
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  5. Keijiro Sezaki
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  6. Atsushi Fukui
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Correspondence to Paul V. Dunlap.

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Dunlap, P.V., Takami, M., Wakatsuki, S. et al. Inception of bioluminescent symbiosis in early developmental stages of the deep-sea fish, Coelorinchus kishinouyei (Gadiformes: Macrouridae). Ichthyol Res 61, 59–67 (2014). https://doi.org/10.1007/s10228-013-0374-7

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