Abstract
Nitric oxide (NO) signaling in vertebrates is well characterized and involves the heme-nitric oxide/oxygen-binding (H-NOX) domain of soluble guanylate cyclase as a selective NO sensor. In contrast, little is known about the biological role or signaling output of bacterial H-NOX proteins. Here, we describe a molecular pathway for H-NOX signaling in Shewanella oneidensis. NO stimulates biofilm formation by controlling the levels of the bacterial secondary messenger cyclic diguanosine monophosphate (c-di-GMP). Phosphotransfer profiling was used to map the connectivity of a multicomponent signaling network that involves integration from two histidine kinases and branching to three response regulators. A feed-forward loop between response regulators with phosphodiesterase domains and phosphorylation-mediated activation intricately regulated c-di-GMP levels. Phenotypic characterization established a link between NO signaling and biofilm formation. Cellular adhesion may provide a protection mechanism for bacteria against reactive and damaging NO. These results are broadly applicable to H-NOX-mediated NO signaling in bacteria.
Copyright © 2012 Elsevier Inc. All rights reserved.
Publication types
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Research Support, N.I.H., Extramural
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Research Support, Non-U.S. Gov't
MeSH terms
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3',5'-Cyclic-GMP Phosphodiesterases / chemistry
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3',5'-Cyclic-GMP Phosphodiesterases / genetics
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3',5'-Cyclic-GMP Phosphodiesterases / metabolism
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Amino Acid Sequence
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Bacterial Proteins / chemistry
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Bacterial Proteins / genetics
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Bacterial Proteins / metabolism
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Biofilms / growth & development*
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Cyclic GMP / analogs & derivatives*
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Cyclic GMP / metabolism
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Gammaproteobacteria / genetics
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Gammaproteobacteria / physiology
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Guanylate Cyclase / chemistry
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Guanylate Cyclase / genetics
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Guanylate Cyclase / metabolism
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Histidine Kinase
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Models, Biological
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Molecular Sequence Data
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Nitric Oxide / metabolism*
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Phosphorylation
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Protein Kinases / chemistry
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Protein Kinases / genetics
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Protein Kinases / metabolism
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Protein Structure, Tertiary
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Receptors, Cytoplasmic and Nuclear / chemistry
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Receptors, Cytoplasmic and Nuclear / genetics
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Receptors, Cytoplasmic and Nuclear / metabolism
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Second Messenger Systems
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Sequence Homology, Amino Acid
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Shewanella / genetics
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Shewanella / physiology*
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Signal Transduction
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Soluble Guanylyl Cyclase
Substances
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Bacterial Proteins
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Receptors, Cytoplasmic and Nuclear
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Nitric Oxide
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bis(3',5')-cyclic diguanylic acid
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Protein Kinases
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Histidine Kinase
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3',5'-Cyclic-GMP Phosphodiesterases
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Guanylate Cyclase
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Soluble Guanylyl Cyclase
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Cyclic GMP