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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American Society for Microbiology
2020
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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) |
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Aliivibrio chemotaxis exopolysaccharide gene regulation luminescence symbiosis Microbiology QR1-502 |
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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 |
work_keys_str_mv |
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