Abstract
The bioluminescent bacterium Vibrio fischeri forms a mutually beneficial symbiosis with the Hawaiian bobtail squid, Euprymna scolopes, in which the bacteria, housed inside a specialized light organ, produce light used by the squid in its nocturnal activities. Upon hatching, E. scolopes juveniles acquire V. fischeri from the seawater through a complex process that requires, among other factors, chemotaxis by the bacteria along a gradient of N-acetylated sugars into the crypts of the light organ, the niche in which the bacteria reside. Once inside the light organ, V. fischeri transitions into a symbiotic, sessile state in which the quorum-signaling regulator LitR induces luminescence. In this work we show that expression of litR and luminescence are repressed by a homolog of the Vibrio cholerae virulence factor TcpP, which we have named HbtR. Further, we demonstrate that LitR represses genes involved in motility and chemotaxis into the light organ and activates genes required for exopolysaccharide production.IMPORTANCE TcpP homologs are widespread throughout the Vibrio genus; however, the only protein in this family described thus far is a V. cholerae virulence regulator. Here, we show that HbtR, the TcpP homolog in V. fischeri, has both a biological role and regulatory pathway completely unlike those in V. cholerae Through its repression of the quorum-signaling regulator LitR, HbtR affects the expression of genes important for colonization of the E. scolopes light organ. While LitR becomes activated within the crypts and upregulates luminescence and exopolysaccharide genes and downregulates chemotaxis and motility genes, it appears that HbtR, upon expulsion of V. fischeri cells into seawater, reverses this process to aid the switch from a symbiotic to a planktonic state. The possible importance of HbtR to the survival of V. fischeri outside its animal host may have broader implications for the ways in which bacteria transition between often vastly different environmental niches.
Highlights
The Gram-negative bacterium Vibrio (Aliivibrio) fischeri is a model organism for the study of biochemical processes underpinning bioluminescence, quorum sensing, and bacterial-animal symbioses
While much research has gone into understanding the mechanisms necessary for colonization of the E. scolopes light organ by V. fischeri
(37)), there has been little investigation into how the ~95% of symbiotic bacteria expelled from the light organ at dawn each day transition back into life in seawater
Summary
The Gram-negative bacterium Vibrio (Aliivibrio) fischeri is a model organism for the study of biochemical processes underpinning bioluminescence, quorum sensing, and bacterial-animal symbioses. V. fischeri cells initiate light-organ colonization through a series of steps, including chemotaxis towards N-acetylated sugars released by the squid [11, 12]. After initial colonization of the squid light organ, the symbiosis undergoes a daily cyclic rhythm of three basic stages for the remainder of the squid’s life: during the day, V. fischeri cells grow to a high density in the crypts on carbon sources provided by the squid [13, 14]; at night, the bacteria produce light that aids in camouflage for the squid [15, 16]; and at dawn, ~95% of the bacterial cells are expelled from the light organ into the seawater, where they may initiate colonization of new squid hatchlings, while the remaining ~5% repopulate the light organ [17, 18]
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