J. Molec. Microbiol. Biotechnol. (1999) 1(1): 13-21. The Squid-Vibrio SymbiosisJMMB as a Biomedical Symposium Model 13 The Euprymna scolopes -Vibrio fischeri Symbiosis: A Biomedical Model for the Study of Bacterial Colonization of Animal Tissue Edward G. Ruby* biological world. The principal interactions between bacteria and animal Pacific Biomedical Research Center tissue occur along the apical surfaces of host epithelial University of Hawaii, Manoa, Hawaii cells. Typically, a diverse consortium of microorganisms and host cells forms a dynamic, cooperating unit that helps maintain a healthy microenvironment within the colonized Abstract tissues. Such associations are ubiquitous, exhibit species specificity and, with few exceptions (Breznak and Brune, The diversity of microorganisms found in the marine 1994; Whittaker et al., 1996; Hooper et al., 1998), are poorly environment reflects the immense size, range of understood. A better understanding of the process by which physical conditions and energy sources, and bacteria and host cells exchange the signals that underlie evolutionary age of the sea. Because associations with these phenomena is an important research goal of living animal tissue are an important and ancient part biomedical research. Over the past decade the E. scolopes- of the ecology of many microorganisms, it is not V. fischeri association, a natural and experimentally facile surprising that the study of marine symbioses model system, has been used to discover the nature of (including both cooperative and pathogenic the mechanisms by which animals form beneficial interactions) has produced numerous discoveries of associations with microorganisms, and to determine how biotechnological and biomedical significance. The these mechanisms are related to, but have diverged from, association between the bioluminescent bacterium those that function in pathogenic infections. Initial studies Vibrio fischeri and the sepiolid squid Euprymna concentrated on a description of the system, leading to an scolopes has emerged as a productive model system understanding of the light organ morphology in both the for the investigation of the mechanisms by which juvenile (Montgomery and McFall-Ngai, 1993; Weis et al., cooperative bacteria initiate colonization of specific 1993; Hanlon, et al., 1997) and the adult (McFall-Ngai and host tissues. The results of the last decade of research Montgomery, 1990; Montgomery and McFall-Ngai, 1998) on this system have begun to reveal surprising animal. Similarly, the pattern of growth of V. fischeri cells similarities between this association and the during the initiation of the association (Ruby and Asato, pathogenic associations of disease-causing Vibrio 1993), and the role of the bacteria in the induction of its species, including those of interest to human health subsequent development (Foster and McFall-Ngai, 1998; and aquaculture. Studies of the biochemical and McFall-Ngai and Ruby, 1998) were described. In addition, molecular events underlying the development of the unexpected phenomena were discovered, such as the squid-vibrio symbiosis can be expected to continue pronounced and dynamic diel rhythm dominating the state to increase our understanding of the factors controlling of the association (Lee and Ruby, 1994a; Boettcher et al., both benign and pathogenic bacterial associations. 1996), and the presence of the antibacterial enzyme haloperoxidase within the contents of the light organ crypts Introduction (Weis et al., 1993). This review describes the colonization of the squid light Two areas of biomedical significance have emerged during organ by V. fischeri, emphasizing those bacterial the past 20 years. The first of these is the rise in coastal determinants that have homologs or analogs among areas across the world of bacterial diseases borne by pathogenic Vibrio species. What we have learned about marine and brackish-water bacteria in the genus Vibrio the development and specificity of this process by an (Blake, 1983; Colwell, 1996). The second is the growing examination of the host-imposed obstacles or barriers to awareness of the importance of cooperative bacterial colonization is also outlined. The review concludes with a colonization of animal tissues to the proper development discussion of the possible roles current and future studies and health of the host (McFall-Ngai, 1998a; Rook and of the E. scolopes-V. fischeri association may play in Stanford, 1998). Progress in addressing questions in both biomedically important areas of research. of these areas has been made through the investigation of a symbiotic association involving Euprymna scolopes, a The Symbiotic Partners shallow-water squid, and Vibrio fischeri, a bioluminescence bacterium. This association has developed into a paradigm Euprymna scolopes is a small, nocturnal, sepiolid squid not only for the study of symbiosis in the marine environ- (Berry, 1912) that is bioluminescent owing to the presence ment, but for the myriad of both cooperative and pathogenic of bacterial symbionts contained within a complex, bilobed, bacteria-animal host interactions that characterize the light-emitting organ (Nesis, 1987; McFall-Ngai and Montgomery, 1990). Light generated by these bacteria *For correspondence. Email [email protected]; allows the host squid to produce a controlled, diffuse, Tel. (808) 539-7309; Fax. (808) 599-4817. ventral glow as an antipredatory behavior (McFall-Ngai, © 1999 Horizon Scientific Press Further Reading Caister Academic Press is a leading academic publisher of advanced texts in microbiology, molecular biology and medical research. 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The Euprymna scolopes Symbiotic Light g Organ A ventral dissection of an anesthetized adult animal reveals the bilobed light organ (lo) in the center of the mantle cavity (McFall-Ngai and Montgomery, 1990), and partially occluded by the ink sac (black). Each lateral face of the adult light organ has a single pore through which the bacteria-containing crypts, deep in the center of the lobes of the organ (*), are connected to the outside environment (e,