Abstract
ABSTRACTMicrobes colonize the apical surfaces of polarized epithelia in nearly all animal taxa. In one example, the luminous bacterium Vibrio fischeri enters, grows to a dense population within, and persists for months inside, the light-emitting organ of the squid Euprymna scolopes. Crucial to the symbiont’s success after entry is the ability to trigger the constriction of a host tissue region (the “bottleneck”) at the entrance to the colonization site. Bottleneck constriction begins at about the same time as bioluminescence, which is induced in V. fischeri through an autoinduction process called quorum sensing. Here, we asked the following questions: (i) Are the quorum signals that induce symbiont bioluminescence also involved in triggering the constriction? (ii) Does improper signaling of constriction affect the normal maintenance of the symbiont population? We manipulated the presence of three factors, the two V. fischeri quorum signal synthases, AinS and LuxI, the transcriptional regulator LuxR, and light emission itself, and found that the major factor triggering and maintaining bottleneck constriction is an as yet unknown effector(s) regulated by LuxIR. Treating the animal with chemical inhibitors of actin polymerization reopened the bottlenecks, recapitulating the host’s response to quorum-sensing defective symbionts, as well as suggesting that actin polymerization is the primary mechanism underlying constriction. Finally, we found that these host responses to the presence of symbionts changed as a function of tissue maturation. Taken together, this work broadens our concept of how quorum sensing can regulate host development, thereby allowing bacteria to maintain long-term tissue associations.
Highlights
IMPORTANCE Interbacterial signaling within a host-associated population can have profound effects on the behavior of the bacteria, for instance, in their production of virulence/colonization factors; in addition, such signaling can dictate the nature of the outcome for the host, in both pathogenic and beneficial associations
We found that quorum sensing, mediated by LuxIR, is the most pronounced driver of both bottleneck constriction and successful maintenance of the symbiont population
The bottlenecks (Fig. 1B) associated with the most developed crypt type (“major crypt” crypt 1 (C1)) that were colonized by wildtype (WT) V. fischeri strain ES114 were already ;65% narrower than their uncolonized counterparts (Fig. 2)
Summary
IMPORTANCE Interbacterial signaling within a host-associated population can have profound effects on the behavior of the bacteria, for instance, in their production of virulence/colonization factors; in addition, such signaling can dictate the nature of the outcome for the host, in both pathogenic and beneficial associations. Perhaps the most widespread type of animal-microbe symbiosis is the association of extracellular bacteria along the apical surfaces of epithelial tissue [1] In such symbioses, the biochemical conversation between the microbes and their host can be strongly dependent on an underlying level of bacterium-bacterium signaling. V. fischeri is the only bacterium that can colonize the confined crypt spaces inside the light-emitting organ of the bobtail squid Euprymna scolopes [13] Within these spaces, the 3O-C6 accumulates around the dense population of symbionts, activating their luxICDABEG operon and resulting in a bioluminescence used by the host in its nocturnal behavior [14, 15]. Bacteria with mutations in the genes encoding the synthases of either C8 (ainS) or 3O-C6 (luxI) [16] can still initiate colonization; after 24 h, the luxI mutation results in a symbiotic persistence defect [4, 10]
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