Vibrio fischeri flavohaemoglobin protects against nitric oxide during initiation of the squid-Vibrio symbiosis

Mol Microbiol. 2010 Nov;78(4):903-15. doi: 10.1111/j.1365-2958.2010.07376.x. Epub 2010 Sep 29.

Abstract

Nitric oxide (NO) is implicated in a wide range of biological processes, including innate immunity against pathogens, signal transduction and protection against oxidative stress. However, its possible roles in beneficial host-microbe associations are less well recognized. During the early stages of the squid-vibrio symbiosis, the bacterial symbiont Vibrio fischeri encounters host-derived NO, which has been hypothesized to serve as a specificity determinant. We demonstrate here that the flavohaemoglobin, Hmp, of V. fischeri protects against NO, both in culture and during colonization of the squid host. Transcriptional analyses indicate that hmp expression is highly responsive to NO, principally through the repressor, NsrR. Hmp protects V. fischeri from NO inhibition of aerobic respiration, and removes NO under both oxic and anoxic conditions. A Δhmp mutant of V. fischeri initiates squid colonization less effectively than wild type, but is rescued by the presence of an NO synthase inhibitor. The hmp promoter is activated during the initial stage of colonization, during which the Δhmp strain fails to form normal-sized aggregates of colonizing cells. Taken together, these results suggest that the sensing of host-derived NO by NsrR, and the subsequent removal of NO by Hmp, influence aggregate size and, thereby, V. fischeri colonization efficiency.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Aerobiosis
  • Aliivibrio fischeri / immunology*
  • Aliivibrio fischeri / physiology*
  • Anaerobiosis
  • Animals
  • Bacterial Proteins / metabolism*
  • Decapodiformes / immunology*
  • Decapodiformes / microbiology*
  • Gene Expression Profiling
  • Hemeproteins / metabolism*
  • Nitric Oxide / metabolism*
  • Nitric Oxide / toxicity
  • Repressor Proteins / metabolism
  • Symbiosis*

Substances

  • Bacterial Proteins
  • Hemeproteins
  • Repressor Proteins
  • flavohemoprotein, Bacteria
  • Nitric Oxide