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H-nox-mediated nitric oxide sensing modulates symbiotic colonization by vibrio fischeri

Academic Article
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Overview

authors

  • Wang, Y. L.
  • Dufour, Y. S.
  • Carlson, H. K.
  • Donohue, T. J.
  • Marletta, Michael
  • Ruby, E. G.

publication date

  • May 2010

journal

  • Proceedings of the National Academy of Sciences of the United States of America  Journal

abstract

  • The bioluminescent bacterium Vibrio fischeri initiates a specific, persistent symbiosis in the light organ of the squid Euprymna scolopes. During the early stages of colonization, V. fischeri is exposed to host-derived nitric oxide (NO). Although NO can be both an antimicrobial component of innate immunity and a key signaling molecule in eukaryotes, potential roles in beneficial host-microbe associations have not been described. V. fischeri hnoX encodes a heme NO/oxygen-binding (H-NOX) protein, a member of a family of bacterial NO- and/or O(2)-binding proteins of unknown function. We hypothesized that H-NOX acts as a NO sensor that is involved in regulating symbiosis-related genes early in colonization. Whole-genome expression studies identified 20 genes that were repressed in an NO- and H-NOX-dependent fashion. Ten of these, including hemin-utilization genes, have a promoter with a putative ferric-uptake regulator (Fur) binding site. As predicted, in the presence of NO, wild-type V. fischeri grew more slowly on hemin than a hnoX deletion mutant. Host-colonization studies showed that the hnoX mutant was also 10-fold more efficient in initially colonizing the squid host than the wild type; similarly, in mixed inoculations, it outcompeted the wild-type strain by an average of 16-fold after 24 h. However, the presence of excess hemin or iron reversed this dominance. The advantage of the mutant in colonizing the iron-limited light-organ tissues is caused, at least in part, by its greater ability to acquire host-derived hemin. Our data suggest that V. fischeri normally senses a host-generated NO signal through H-NOX(Vf) and modulates the expression of its iron uptake capacity during the early stages of the light-organ symbiosis.

subject areas

  • Aliivibrio fischeri
  • Bacterial Proteins
  • Gene Deletion
  • Gene Expression Profiling
  • Heme
  • Hemin
  • Iron
  • Ligands
  • Mutation
  • Nitric Oxide
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Research

keywords

  • colonization
  • iron uptake
  • symbiosis
  • transcriptional analysis
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Identity

PubMed Central ID

  • PMC2889544

International Standard Serial Number (ISSN)

  • 0027-8424

Digital Object Identifier (DOI)

  • 10.1073/pnas.1003571107

PubMed ID

  • 20404170
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Additional Document Info

start page

  • 8375

end page

  • 8380

volume

  • 107

issue

  • 18

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