A lasting symbiosis: how the Hawaiian bobtail squid finds and keeps its bioluminescent bacterial partner

Abstract

For over 30 years, the association between the Hawaiian bobtail squid, Euprymna scolopes, and the bioluminescent bacterium, Vibrio fischeri, has been studied as a model system for the colonization of animal epithelia by symbiotic bacteria. The squid-vibrio light-organ system provides the exquisite resolution only possible with the study of a binary partnership. The impact of this relationship on the partners' biology has been broadly characterized, including their ecology and evolutionary biology as well as the underlying molecular mechanisms of symbiotic dynamics. Much has been learned about the factors that foster initial light-organ colonization, and more recently about the maturation and long-term maintenance of the association. This Review synthesizes the results of recent research on the light-organ association and also describes the development of new horizons for E. scolopes as a model organism that promises to inform biology and biomedicine about the basic nature of host-microorganism interactions.

Getting the Message Out: the Many Modes of Host-Symbiont Communication during Early-Stage Establishment of the Squid-Vibrio Partnership

“…Before outlining host-symbiont interactions, we describe here the landscape in which the dialogue develops in the squid-vibrio partnership ( 4 , 5 ). As in likely all horizontally transmitted symbioses, during embryogenesis, the host creates a complex nascent symbiotic organ that poises specific animal tissues to recruit the symbiont upon hatching ( 6 ).…”

“…Shortly after the hatching from the egg, two events occur: (i) the migratory pathway of the most mature crypt expands ( 10 ), and (ii) the cilia on the organ surface begin to beat, and the associated epithelia shed mucus in a nonspecific response to environmental PGN released by the ambient bacterioplankton ( 4 ). The environment in which the symbionts will be enriched is biochemically harsh ( Fig.…”

“…In the presence of an experimental inoculum of 1,000 to 5,000 V. fischeri cells/ml of seawater, over the course of 3 h, the host aggregates only 5 to 10 of them into regions above the pores on each side of the organ. Other Gram-negative bacteria in the seawater can also aggregate, but when V. fischeri cells are present, they dominate ( 4 ). This dominance is not due to growth, as these aggregated bacteria are not growing, but rather, it is due to a competitive dominance by the candidate symbionts at that site.…”

“…1 ). Thus, the signal/effector functions of NO must be carefully balanced ( 4 ). Finally, in a recent report of immune system suppression, a small RNA (sRNA) of the bacterial symbionts (SsrA) enters the host cells and turns down gene expression of RIG-1, an RNA-binding protein that mediates immune responses in animals ( 40 ).…”

“…The gills were chosen as they are an immune organ in squids, while the eyes were included as they show a significant molecular, developmental, and morphological convergence with the light organ. Both the eyes and light organ function to modulate light and coordinate to control the counterillumination behavior of the host ( 4 ).…”