Initial Symbiont Contact Orchestrates Host-Organ-wide Transcriptional Changes that Prime Tissue Colonization

• Contact with a few V. fischeri induces specific gene-expression changes in host squid
• V. fischeri-induced host genes include a catalytically active chitotriosidase
• Chitotriosidase is secreted into the acidic mucus where chitin derivatives are present
• Chitin degradation promotes V. fischeri chemoattraction and efficient host colonization

SummaryUpon transit to colonization sites, bacteria often experience critical priming that prepares them for subsequent, specific interactions with the host; however, the underlying mechanisms are poorly described. During initiation of the symbiosis between the bacterium Vibrio fischeri and its squid host, which can be observed directly and in real time, approximately five V. fischeri cells aggregate along the mucociliary membranes of a superficial epithelium prior to entering host tissues. Here, we show that these few early host-associated symbionts specifically induce robust changes in host gene expression that are critical to subsequent colonization steps. This exquisitely sensitive response to the host’s specific symbiotic partner includes the upregulation of a host endochitinase, whose activity hydrolyzes polymeric chitin in the mucus into chitobiose, thereby priming the symbiont and also producing a chemoattractant gradient that promotes V. fischeri migration into host tissues. Thus, the host responds transcriptionally upon initial symbiont contact, which facilitates subsequent colonization.

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