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

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.