HbtR, a Heterofunctional Homolog of the Virulence Regulator TcpP, Facilitates the Transition between Symbiotic and Planktonic Lifestyles in <named-content content-type="genus-species">Vibrio fischeri</named-content>

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 juve...

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Autores principales: Brittany D. Bennett, Tara Essock-Burns, Edward G. Ruby
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Publicado: American Society for Microbiology 2020
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spelling oai:doaj.org-article:2b608dc030424f448c442aded0b213ea2021-11-15T16:19:08ZHbtR, a Heterofunctional Homolog of the Virulence Regulator TcpP, Facilitates the Transition between Symbiotic and Planktonic Lifestyles in <named-content content-type="genus-species">Vibrio fischeri</named-content>10.1128/mBio.01624-202150-7511https://doaj.org/article/2b608dc030424f448c442aded0b213ea2020-10-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01624-20https://doaj.org/toc/2150-7511ABSTRACT 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.Brittany D. BennettTara Essock-BurnsEdward G. RubyAmerican Society for MicrobiologyarticleAliivibriochemotaxisexopolysaccharidegene regulationluminescencesymbiosisMicrobiologyQR1-502ENmBio, Vol 11, Iss 5 (2020)
institution DOAJ
collection DOAJ
language EN
topic Aliivibrio
chemotaxis
exopolysaccharide
gene regulation
luminescence
symbiosis
Microbiology
QR1-502
spellingShingle Aliivibrio
chemotaxis
exopolysaccharide
gene regulation
luminescence
symbiosis
Microbiology
QR1-502
Brittany D. Bennett
Tara Essock-Burns
Edward G. Ruby
HbtR, a Heterofunctional Homolog of the Virulence Regulator TcpP, Facilitates the Transition between Symbiotic and Planktonic Lifestyles in <named-content content-type="genus-species">Vibrio fischeri</named-content>
description 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.
format article
author Brittany D. Bennett
Tara Essock-Burns
Edward G. Ruby
author_facet Brittany D. Bennett
Tara Essock-Burns
Edward G. Ruby
author_sort Brittany D. Bennett
title HbtR, a Heterofunctional Homolog of the Virulence Regulator TcpP, Facilitates the Transition between Symbiotic and Planktonic Lifestyles in <named-content content-type="genus-species">Vibrio fischeri</named-content>
title_short HbtR, a Heterofunctional Homolog of the Virulence Regulator TcpP, Facilitates the Transition between Symbiotic and Planktonic Lifestyles in <named-content content-type="genus-species">Vibrio fischeri</named-content>
title_full HbtR, a Heterofunctional Homolog of the Virulence Regulator TcpP, Facilitates the Transition between Symbiotic and Planktonic Lifestyles in <named-content content-type="genus-species">Vibrio fischeri</named-content>
title_fullStr HbtR, a Heterofunctional Homolog of the Virulence Regulator TcpP, Facilitates the Transition between Symbiotic and Planktonic Lifestyles in <named-content content-type="genus-species">Vibrio fischeri</named-content>
title_full_unstemmed HbtR, a Heterofunctional Homolog of the Virulence Regulator TcpP, Facilitates the Transition between Symbiotic and Planktonic Lifestyles in <named-content content-type="genus-species">Vibrio fischeri</named-content>
title_sort hbtr, a heterofunctional homolog of the virulence regulator tcpp, facilitates the transition between symbiotic and planktonic lifestyles in <named-content content-type="genus-species">vibrio fischeri</named-content>
publisher American Society for Microbiology
publishDate 2020
url https://doaj.org/article/2b608dc030424f448c442aded0b213ea
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