H-NOX-mediated nitric oxide sensing modulates symbiotic colonization by Vibrio fischeri.
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.
Wang
Yanling
Y
Department of Medical Microbiology and Immunology, University of Wisconsin, Madison, WI 53706, USA.
Dufour
Yann S
YS
Carlson
Hans K
HK
Donohue
Timothy J
TJ
Marletta
Michael A
MA
Ruby
Edward G
EG
D048908:Aliivibrio fischeri / Q000254:growth & development* / Q000378:metabolism*; D001426:Bacterial Proteins / Q000235:genetics / Q000378:metabolism*; D017353:Gene Deletion; D020869:Gene Expression Profiling; D006418:Heme / Q000378:metabolism; D006427:Hemin / Q000378:metabolism; D007501:Iron / Q000378:metabolism; D008024:Ligands; D009154:Mutation; D009569:Nitric Oxide / Q000378:metabolism*
D001426:Bacterial Proteins; D008024:Ligands; D009569:Nitric Oxide; D006418:Heme; D006427:Hemin; D007501:Iron
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