Abstract
The beneficial symbiosis between the Hawaiian bobtail squid, Euprymna scolopes, and the bioluminescent bacterium, Vibrio fischeri, provides a unique opportunity to study host/microbe interactions within a natural microenvironment. Colonization of the squid light organ by V. fischeri begins a lifelong association with a regulated daily rhythm. Each morning the host expels an exudate from the light organ consisting of 95% of the symbiont population in addition to host hemocytes and shed epithelial cells. We analyzed the host and symbiont proteomes of adult squid exudate and surrounding light organ epithelial tissue using 1D- and 2D-polyacrylamide gel electrophoresis and multidimensional protein identification technology (MudPIT) in an effort to understand the contribution of both partners to the maintenance of this association. These proteomic analyses putatively identified 1581 unique proteins, 870 proteins originating from the symbiont and 711 from the host. Identified host proteins indicate a role of the innate immune system and reactive oxygen species (ROS) in regulating the symbiosis. Symbiont proteins detected enhance our understanding of the role of quorum sensing, two-component signaling, motility, and detoxification of ROS and reactive nitrogen species (RNS) inside the light organ. This study offers the first proteomic analysis of the symbiotic microenvironment of the adult light organ and provides the identification of proteins important to the regulation of this beneficial association.
Highlights
The light organ symbiosis between the Hawaiian bobtail squid, Euprymna scolopes, and the bioluminescent bacterium, Vibrio fischeri, is used as a model association for understanding host/microbe interactions [1,2,3]
At night the light organ crypt spaces contain the highest densities of bacteria (109/adult squid; [5]), and the light provided by these symbionts is used to avoid predation [6]
Exudate samples collected from adult E. scolopes light organs were analyzed using a number of proteomic techniques. 1D- and 2D-PAGE revealed that the host soluble fraction of the exudate, derived from host hemocytes and apical surfaces of shed light organ crypt epithelial cells, was comprised of a complex mixture of proteins and peptides, the majority of which are represented between the isoelectric points of 4 to 7 and a size of 7 to 100 kilodaltons (Fig. 2A, B)
Summary
The light organ symbiosis between the Hawaiian bobtail squid, Euprymna scolopes, and the bioluminescent bacterium, Vibrio fischeri, is used as a model association for understanding host/microbe interactions [1,2,3]. While in the light organ, the bacteria are connected directly to the external environment through ciliated ducts and pores (Fig. 1). This conduit is important as it serves as an interface between the host and the environment and is used in a daily venting of the symbionts. The remaining bacteria repopulate the crypts ensuring a full complement of symbionts by the following nightfall. This venting mechanism helps regulate the symbiont population in the light organ as well as increases the concentration of V. fischeri in the immediate squid habitat, allowing future generations to be colonized [1,8]
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