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Applied and Environmental Microbiology, December 2008, p. 7471-7481, Vol. 74, No. 24
0099-2240/08/$08.00+0 doi:10.1128/AEM.01619-08
Copyright © 2008, American Society for Microbiology. All Rights Reserved.
Developmental and Microbiological Analysis of the Inception of Bioluminescent Symbiosis in the Marine Fish Nuchequula nuchalis (Perciformes: Leiognathidae)
Paul V. Dunlap,1*
Kimberly M. Davis,1,
Shinichi Tomiyama,2,
Misato Fujino,2 and
Atsushi Fukui2
Department of Ecology and Evolutionary Biology, University of Michigan, Ann Arbor, Michigan 48109,1 School of Marine Science and Technology, Tokai University, Orido, Shimizu, Shizuoka 424-8610, Japan2
Received 15 July 2008/ Accepted 22 October 2008
Many marine fish harbor luminous bacteria as bioluminescent symbionts. Despite the diversity, abundance, and ecological importance of these fish and their apparent dependence on luminous bacteria for survival and reproduction, little is known about developmental and microbiological events surrounding the inception of their symbioses. To gain insight on these issues, we examined wild-caught larvae of the leiognathid fish Nuchequula nuchalis, a species that harbors Photobacterium leiognathi as its symbiont, for the presence, developmental state, and microbiological status of the fish's internal, supraesophageal light organ. Nascent light organs were evident in the smallest specimens obtained, flexion larvae of 6.0 to 6.5 mm in notochord length (NL), a developmental stage at which the stomach had not yet differentiated and the nascent gasbladder had not established an interface with the light organ. Light organs of certain of the specimens in this size range apparently lacked bacteria, whereas light organs of other specimens of 6.5 mm in NL and of all larger specimens harbored large populations of bacteria, representatives of which were identified as P. leiognathi. Bacteria identified as Vibrio harveyi were also present in the light organ of one larval specimen. Light organ populations were composed typically of two or three genetically distinct strain types of P. leiognathi, similar to the situation in adult fish, and the same strain type was only rarely found in light organs of different larval, juvenile, or adult specimens. Light organs of larvae carried a smaller proportion of strains merodiploid for the lux-rib operon, 79 of 249 strains, than those of adults (75 of 91 strains). These results indicate that light organs of N. nuchalis flexion and postflexion larvae of 6.0 to 6.7 mm in NL are at an early stage of development and that inception of the symbiosis apparently occurs in flexion larvae of 6.0 to 6.5 mm in NL. Ontogeny of the light organ therefore apparently precedes acquisition of the symbiotic bacteria. Furthermore, bacterial populations in larval light organs near inception of the symbiosis are genetically diverse, like those of adult fish.
* Corresponding author. Mailing address: University of Michigan, Department of Ecology and Evolutionary Biology, 830 North University Avenue, Ann Arbor, MI 48109-1048. Phone: (734) 615-9099. Fax: (734) 763-0544. E-mail: pvdunlap{at}umich.edu
Published ahead of print on 31 October 2008.
Present address: Department of Microbiology, University of Pennsylvania, Philadelphia, PA 19104.
Present address: Marine Science Museum, Social Education Center, Tokai University, Miho, Shimizu, Shizuoka 424-8620, Japan.
Applied and Environmental Microbiology, December 2008, p. 7471-7481, Vol. 74, No. 24
0099-2240/08/$08.00+0 doi:10.1128/AEM.01619-08
Copyright © 2008, American Society for Microbiology. All Rights Reserved.
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