Vibrio fischeri lux genes play an important role in colonization and development of the host light organ

The bioluminescent bacterium Vibrio fischeri and juveniles of the squid Eup rymna scolopes specifically recognize and respond to one another during the formation of a persistent colonization within the host's nascent Light-emi tting organ. The resulting fully developed light organ contains brightly lu minescing bacteria and has undergone a bacterium-induced program of tissue differentiation, one component of which is a swelling of the epithelial cel ls that line the symbiont-containing crypts. While the luminescence (lux) g enes of symbiotic V. fischeri have been shown to be highly induced within t he crypts, the role of these genes in the initiation and persistence of the symbiosis has not been rigorously examined. We have constructed and examin ed three mutants (luxA, luxI, and luxR), defective in either luciferase enz ymatic or regulatory proteins, All three are unable to induce normal lumine scence levels in the host and, 2 days after initiating the association, had a three- to fourfold defect in the extent of colonization. Surprisingly, t hese lax mutants also were unable to induce swelling in the crypt epithelia l cells. Complementing, in trans, the defect in light emission restored bot h normal colonization capability and induction of swelling. We hypothesize that a diminished level of oxygen consumption by a luciferase-deficient sym biotic population is responsible for the reduced fitness of lux mutants in the tight organ crypts, This study is the first to show that the capacity f or bioluminescence is critical for normal cell-cell interactions between a bacterium and its animal host and presents the first examples of V. fischer i genes that affect normal host tissue development.