Phylogenetic Diversity and Cosymbiosis in the Bioluminescent Symbioses of “Photobacterium mandapamensis”

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Abstract
“Photobacterium mandapamensis” (proposed name) andPhotobacterium leiognathiare 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) ofluxFand, as shown here, by the sequence divergence of genes involved in the synthesis of riboflavin,ribBHA. To gain insight into the possibility thatP. mandapamensisandP. leiognathiare ecologically distinct, we used these phylogenetic criteria to determine the incidence ofP. mandapamensisas a bioluminescent symbiont of marine animals. Five fish species,Acropoma japonicum(Perciformes, Acropomatidae),Photopectoralis panayensisandPhotopectoralis bindus(Perciformes, Leiognathidae),Siphamia versicolor(Perciformes, Apogonidae), andGadella jordani(Gadiformes, Moridae), were found to harborP. mandapamensisin their light organs. Specimens ofA. japonicus,P. panayensis, andP. bindusharboredP. mandapamensisandP. leiognathitogether as cosymbionts of the same light organ. Regardless of cosymbiosis,P. mandapamensiswas the predominant symbiont ofA. japonicum, and it was the apparently exclusive symbiont ofS. versicolorandG. jordani. In contrast,P. leiognathiwas found to be the predominant symbiont ofP. panayensisandP. 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 betweenP. mandapamensisand 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 thatP. leiognathiis not the exclusive light organ symbiont of leiognathid fishes, demonstrate that the host species ranges ofP. mandapamensisandP. leiognathiare substantially distinct. The host range difference underscores possible differences in the environmental distributions and physiologies of these two bacterial species.

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