An exclusive contract: specificity in the Vibrio fischeri-Euprymna scolopes partnership.

In the threatening world of dog eat dog, or rather, fish eat fish, marine animals have adopted many strategies for protection against predators (25). The Hawaiian squid Euprymna scolopes is no exception. When startled, this small, shallowwater invertebrate rapidly swims away while releasing a blob of ink, meant to mimic the form of its body, to fool and detain its would-be predator. In addition, E. scolopes hosts a symbiotic colony of the bioluminescent bacterium Vibrio fischeri as an even more sophisticated antipredation measure. During its nocturnal feeding period, the squid emits light downward and modulates it to match the intensity of moonlight, thus preventing the formation of a tell-tale shadow on the ocean floor below. Maintenance of this bioluminescent bacterial partner is therefore important for survival of the squid, which has evolved a special organ in the center of its body cavity for promoting growth of the bacteria and controlling the emission of light (24). A monospecific culture of V. fischeri inhabits this light-emitting organ (3, 4), or light organ, at a cell density upwards of 10 cells per cm (31). The bacteria are concentrated in crypts, or small spaces within the light organ, which are lined by columnar epithelial cells. Although the bacterial cells are extracellular, they are in intimate contact with the microvilli of the epithelium (16, 23). This bacterium-containing tissue is flanked by reflector, lens, and ink sac tissues that serve to modulate and direct the bacterial bioluminescence (23). In contrast to the adult light organ, which is exquisitely adapted for the control of luminescence (23), the light organ of a newly hatched juvenile has a completely different morphology (29) and, importantly, contains no bacteria (27, 39). A symbiotic colonization rapidly ensues within hours of hatching, triggering a series of morphological and developmental changes in both organisms that serve to enhance the interaction (16, 28, 33). Specificity in this association is achieved through a reciprocal dialogue between the host and symbiont in a series of stages that ultimately result in the establishment of a stable relationship that endures throughout the lifetime of the host. These stages include the initial encounter between the two organisms, early negotiation for entry and attachment by the correct bacterial species, commitment to the relationship by the partners, and equilibrium associated with a longterm dynamic relationship. To better understand the depth of the challenge associated with achieving specificity in these processes, it is important to grasp the nature of the landscape and the scale over which the process of colonization takes place by putting into context the relationship of the bacterial macroecology to the microecology of the host’s body cavity. This minireview seeks to place the role of specificity in the development of this cooperative light organ symbiosis into such a conceptual framework.