The role of the immune system in the initiation and persistence of the Euprymna scolopes--Vibrio fischeri symbiosis

Abstract

The squid-vibrio symbiosis is an experimental system being studied as a model of the chronic colonization of animal epithelia by bacterial partners. One principal question being asked with this model is: what is the role of the immune system in the dynamics of the onset and maintenance of the symbiotic state? This review focuses upon results of research to date, which have demonstrated that both cell-mediated and cell-free components of the innate immune system are involved in these processes.

Fig. 1

The nascent symbiotic tissues of the host. A. The light organ of the juvenile squid, which will become colonized by the symbiont, can be seen through the translucent dorsal mantle as a dark region in the center of the mantle cavity (white arrow). B. A ventral view of the light organ (white arrowhead) reveals the juvenile-specific morphology. C. A higher magnification of the organ shows the elaborate ciliated fields on each lateral surface (dotted circle, one circumscribed field). The pores where the symbionts will enter host tissues occur in the center of each field (white arrow). D. A histological section through the organ reveals the path through which the symbionts will invade host tissues. After aggregating in host-shed mucus, the symbionts will migrate into a pore (p), through ducts (d) and into the crypts spaces (e), where they interact with the crypt epithelium (e) and a population of hemocytes (h).

Fig. 2

The dynamics of the V. fischeri populations during initiation and maintenance of the symbiosis. A. Whereas the host tissues are devoid of symbionts during embryogenesis (white portion of the host life cycle), they colonize within minutes and are present persistently (grey portion). In the minutes following hatching, the symbiont specificity of the crypts spaces is resolved. B. The symbiont population in the host organ is controlled by a daily venting of the symbionts into the surrounding environment.

Fig. 3

Host hemocytes as key cellular components of the symbiosis. A. Hemocytes migrate into each blood sinus (bs) of superficial epithelial fields (sef) of the juvenile organ in response to interactions with symbiont MAMPs. (p, two of the three pores of one lateral surface). B/C. Hemocytes phagocytose bacteria that they encounter. B. A confocal/differential-interference-contrast image shows extracellular bacteria on the surface of the hemocyte (white arrow) and phagocytosed cells (black arrow). C. A transmission electron micrograph localizes bacterial cells (black arrows) to the cytoplasm of the hemocyte.

Fig. 4

Interpreting the “language” of the squid/vibrio symbiosis. Studies over the past twenty years have identified a number of host responses and effector mechanisms that are either induced or repressed by colonization of host tissues by V. fischeri. For many of these, the symbiont signal that induces these host effects can be linked to MAMPs such as LPS, PGN, or TCT. However, the molecular mechanisms behind some of these processes have yet to be characterized.