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Applied and Environmental Microbiology, May 2007, p. 3173-3182, Vol. 73, No. 10
0099-2240/07/$08.00+0     doi:10.1128/AEM.02212-06
Copyright © 2007, American Society for Microbiology. All Rights Reserved.

Phylogenetic Diversity and Cosymbiosis in the Bioluminescent Symbioses of "Photobacterium mandapamensis"{triangledown} ,{dagger}

Allison J. Kaeding,1 Jennifer C. Ast,1 Meghan M. Pearce,1,{ddagger} Henryk Urbanczyk,1 Seishi Kimura,2 Hiromitsu Endo,3 Masaru Nakamura,4 and Paul V. Dunlap1*

Department of Ecology and Evolutionary Biology, University of Michigan, Ann Arbor, Michigan,1 Fisheries Research Laboratory, Mie University, Shima, Mie 517-0703, Japan,2 Laboratory of Marine Biology, Kochi University, Kochi 780-8520, Japan,3 Tropical Biosphere Research Center, University of the Ryukyus, Motobu, Okinawa 905-0227, Japan4

Received 20 September 2006/ Accepted 12 March 2007

"Photobacterium mandapamensis" (proposed name) and Photobacterium leiognathi are closely related, phenotypically similar marine bacteria that form bioluminescent symbioses with marine animals. Despite their similarity, however, these bacteria can be distinguished phylogenetically by sequence divergence of their luminescence genes, luxCDAB(F)E, by the presence (P. mandapamensis) or the absence (P. leiognathi) of luxF and, as shown here, by the sequence divergence of genes involved in the synthesis of riboflavin, ribBHA. To gain insight into the possibility that P. mandapamensis and P. leiognathi are ecologically distinct, we used these phylogenetic criteria to determine the incidence of P. mandapamensis as a bioluminescent symbiont of marine animals. Five fish species, Acropoma japonicum (Perciformes, Acropomatidae), Photopectoralis panayensis and Photopectoralis bindus (Perciformes, Leiognathidae), Siphamia versicolor (Perciformes, Apogonidae), and Gadella jordani (Gadiformes, Moridae), were found to harbor P. mandapamensis in their light organs. Specimens of A. japonicus, P. panayensis, and P. bindus harbored P. mandapamensis and P. leiognathi together as cosymbionts of the same light organ. Regardless of cosymbiosis, P. mandapamensis was the predominant symbiont of A. japonicum, and it was the apparently exclusive symbiont of S. versicolor and G. jordani. In contrast, P. leiognathi was found to be the predominant symbiont of P. panayensis and P. bindus, and it appears to be the exclusive symbiont of other leiognathid fishes and a loliginid squid. A phylogenetic test for cospeciation revealed no evidence of codivergence between P. mandapamensis and its host fishes, indicating that coevolution apparently is not the basis for this bacterium's host preferences. These results, which are the first report of bacterial cosymbiosis in fish light organs and the first demonstration that P. leiognathi is not the exclusive light organ symbiont of leiognathid fishes, demonstrate that the host species ranges of P. mandapamensis and P. leiognathi are substantially distinct. The host range difference underscores possible differences in the environmental distributions and physiologies of these two bacterial species.

* Corresponding author. Mailing address: Department of Ecology and Evolutionary Biology, 830 North University Avenue, University of Michigan, Ann Arbor, MI 48109-1048. Phone: (734) 615-9099. Fax: (734) 763-0544. E-mail: pvdunlap{at}umich.edu

{triangledown} Published ahead of print on 16 March 2007.

{dagger} Supplemental material for this article may be found at http://aem.asm.org/.

{ddagger} Present address: Integrated Graduate Program, Feinberg School of Medicine, Northwestern University, Chicago, IL 60611-3008.

Applied and Environmental Microbiology, May 2007, p. 3173-3182, Vol. 73, No. 10
0099-2240/07/$08.00+0     doi:10.1128/AEM.02212-06
Copyright © 2007, American Society for Microbiology. All Rights Reserved.



This article has been cited by other articles:

  • Dunlap, P. V., Davis, K. M., Tomiyama, S., Fujino, M., Fukui, A. (2008). Developmental and Microbiological Analysis of the Inception of Bioluminescent Symbiosis in the Marine Fish Nuchequula nuchalis (Perciformes: Leiognathidae). Appl. Environ. Microbiol. 74: 7471-7481 [Abstract] [Full Text]  
  • Urbanczyk, H., Ast, J. C., Kaeding, A. J., Oliver, J. D., Dunlap, P. V. (2008). Phylogenetic Analysis of the Incidence of lux Gene Horizontal Transfer in Vibrionaceae. J. Bacteriol. 190: 3494-3504 [Abstract] [Full Text]  
  • O'Grady, E. A., Wimpee, C. F. (2008). Mutations in the lux Operon of Natural Dark Mutants in the Genus Vibrio. Appl. Environ. Microbiol. 74: 61-66 [Abstract] [Full Text]  
  • Ast, J. C., Urbanczyk, H., Dunlap, P. V. (2007). Natural Merodiploidy of the lux-rib Operon of Photobacterium leiognathi from Coastal Waters of Honshu, Japan. J. Bacteriol. 189: 6148-6158 [Abstract] [Full Text]  


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