Relative contributions of norspermidine synthesis and signaling pathways to the regulation of Vibrio cholerae biofilm formation

The polyamine norspermidine is one of the major polyamines synthesized by Vibrionales and has also been found in various aquatic organisms. Norspermidine is among the environmental signals that positively regulate Vibrio cholerae biofilm formation. The NspS/MbaA signaling complex detects extracellul...

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Published in:	PloS one Vol. 12; no. 10; p. e0186291
Main Authors:	Wotanis, Caitlin K, Brennan, 3rd, William P, Angotti, Anthony D, Villa, Elizabeth A, Zayner, Josiah P, Mozina, Alexandra N, Rutkovsky, Alexandria C, Sobe, Richard C, Bond, Whitney G, Karatan, Ece
Format:	Journal Article
Language:	English
Published:	United States Public Library of Science 18-10-2017 Public Library of Science (PLoS)
Subjects:	Aquatic organisms Bacteria Bacteriology Binding Binding proteins Biofilms Biofilms - growth & development Biology Biology and Life Sciences Catechols - metabolism Clonal deletion Cyclic GMP - analogs & derivatives Cyclic GMP - metabolism Enzymes Gene deletion Infections Intracellular Iron Iron - metabolism Medicine and Health Sciences Microbial mats Mutants Oxazoles - metabolism Pathogens Periplasmic Binding Proteins - genetics Periplasmic Binding Proteins - metabolism Phosphodiesterase Phosphoric Diester Hydrolases - genetics Phosphoric Diester Hydrolases - metabolism Polyamines Proteins Research and analysis methods Scholarships & fellowships Signal Transduction Spermidine - analogs & derivatives Spermidine - biosynthesis Spermidine - metabolism Synthesis Vibrio Vibrio cholerae Vibrio cholerae - genetics Vibrio cholerae - growth & development Vibrio cholerae - pathogenicity Water-borne diseases Waterborne diseases North Carolina United States > US
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Summary:	The polyamine norspermidine is one of the major polyamines synthesized by Vibrionales and has also been found in various aquatic organisms. Norspermidine is among the environmental signals that positively regulate Vibrio cholerae biofilm formation. The NspS/MbaA signaling complex detects extracellular norspermidine and mediates the response to this polyamine. Norspermidine binding to the NspS periplasmic binding protein is thought to inhibit the phosphodiesterase activity of MbaA, increasing levels of the biofilm-promoting second messenger cyclic diguanylate monophosphate, thus enhancing biofilm formation. V. cholerae can also synthesize norspermidine using the enzyme NspC as well as import it from the environment. Deletion of the nspC gene was shown to reduce accumulation of bacteria in biofilms, leading to the conclusion that intracellular norspermidine is also a positive regulator of biofilm formation. Because V. cholerae uses norspermidine to synthesize the siderophore vibriobactin it is possible that intracellular norspermidine is required to obtain sufficient amounts of iron, which is also necessary for robust biofilm formation. The objective of this study was to assess the relative contributions of intracellular and extracellular norspermidine to the regulation of biofilm formation in V. cholerae. We show the biofilm defect of norspermidine synthesis mutants does not result from an inability to produce vibriobactin as vibriobactin synthesis mutants do not have diminished biofilm forming abilities. Furthermore, our work shows that extracellular, but not intracellular norspermidine, is mainly responsible for promoting biofilm formation. We establish that the NspS/MbaA signaling complex is the dominant mediator of biofilm formation in response to extracellular norspermidine, rather than norspermidine synthesized by NspC or imported into the cell.
Bibliography:	ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 Competing Interests: The authors have declared that no competing interests exist.
ISSN:	1932-6203 1932-6203
DOI:	10.1371/journal.pone.0186291