Response of Vibrio cholerae to the Catecholamine Hormones Epinephrine and Norepinephrine

Abstract

In Escherichia coli or Salmonella enterica, the stress-associated mammalian hormones epinephrine (E) and norepinephrine (NE) trigger a signaling cascade by interacting with the QseC sensor protein. Here we show that Vibrio cholerae, the causative agent of cholera, exhibits a specific response to E and NE. These catecholates (0.1 mM) enhanced the growth and swimming motility of V. cholerae strain O395 on soft agar in a medium containing calf serum, which simulated the environment within the host. During growth, the hormones were converted to degradation products, including adrenochrome formed by autooxidation with O 2 or superoxide. In E. coli, the QseC sensor kinase, which detects the autoinducer AI-3, also senses E or NE. The genome of V. cholerae O395 comprises an open reading frame coding for a putative protein with 29% identity to E. coli QseC. Quantitative reverse transcriptase PCR (qRT-PCR) experiments revealed increased transcript levels of the qseC-like gene and of pomB, a gene encoding a structural component of the flagellar motor complex, under the influence of E or NE. Phentolamine blocks the response of E. coli QseC to E or NE. A V. cholerae mutant devoid of the qseC-like gene retained the phentolamine-sensitive motility in the presence of E, whereas NE-stimulated motility was no longer inhibited by phentolamine. Our study demonstrates that V. cholerae senses the stress hormones E and NE. A sensor related to the histidine kinase QseC from E. coli is identified and is proposed to participate in the sensing of NE. IMPORTANCEVibrio cholerae is a Gram-negative bacterium that may cause cholera, a severe illness with high mortality due to acute dehydration caused by diarrhea and vomiting. Pathogenic V. cholerae strains possess virulence factors like the cholera toxin (CTX) and the toxin-coregulated pilus (TCP) produced in response to signals provided by the host. In pathogenic enterobacteria, the stressassociated hormones epinephrine (E) and norepinephrine (NE) of the human host act as signal molecules for the production of virulence factors and promote bacterial growth by the sequestration of iron from the host. Here we show that V. cholerae, like some enterobacteria, benefits from these stress hormones and possesses a sensor to recognize them. Stress enhances the susceptibility of a mammalian host to infection by bacteria. The stress-associated mammalian hormones epinephrine (E) and norepinephrine (NE), for example, support the growth (1-3) and motility (4, 5) of the enterobacteria Escherichia coli, Salmonella enterica serovar Typhimurium, and Klebsiella pneumoniae (6), of Pseudomonas aeruginosa (7,8), and of some Vibrio species (9) in a serum-based bacteriostatic medium. As E and NE share structural similarities to the bacterial catechol siderophores-a benzene ring with two adjacent hydroxyl groups-it was suggested that these stress hormones may be involved in the binding and uptake of iron by bacteria, thus promoting growth or motility (1-5). Recently, the mechanism by which catecholamine hormo...

The stress hormone norepinephrine increases the growth and virulence of Aeromonas hydrophila

“…However, this result was in contrast to previous reports that 10 μM NE could induce log-fold changes in A. hydrophila growth (Dong et al, 2016;Kinney et al, 1999). This difference may be attributed to the variation of experimental conditions including transferrin levels, bacterial strains, and inoculum densities in different studies (O'Donnell et al, 2006 (Halang et al, 2015), Aeromonas hydrophilia (Dong et al, 2016),…”

“…Based on preliminary tests, we found that NE significantly enhanced the growth of Aeromonas hydrophilia AH196 in the medium with ABS and FBS, and a higher growth stimulation of Aeromonas hydrophilia AH196 was observed in serum‐SAPI medium containing FBS rather than that of ABS (data not shown). The previous studies also have chosen serum‐SAPI medium supplemented FBS as a culture medium to assess the effect of NE on the growth of Vibrio cholerae (Halang et al., ), Aeromonas hydrophilia (Dong et al., ), Campylobacter jejuni (Xu et al., ), and Vibrio parahaemolyticus (Nakano, Takahashi, Sakai, & Nakaya, ).…”

Salmonella enterica Serovar Typhimurium Strategies for Host Adaptation

“…Importantly, several of the strategies used by S. Tm to adapt to host environments are conserved among several organisms such as pathogenic E. coli , Listeria monocytogenes , Brucella abortus , and Staphylococcus aureus . For example, pathogens adapt to the host or regulate virulence by utilizing and/or sensing nitrate ( Spees et al, 2013 ; Winter et al, 2013 ), epi/NE ( Curtis et al, 2014 ; Halang et al, 2015 ; Moreira et al, 2016 ; Rooks et al, 2017 ), ethanolamine ( Maadani et al, 2007 ; Kendall et al, 2012 ; DebRoy et al, 2014 ; Gonyar and Kendall, 2014 ; Mellin et al, 2014 ; Subashchandrabose et al, 2014 ), iron ( Almirón et al, 2001 ; Zimbler et al, 2012 ; Hammer et al, 2013 , 2014 ; Mashruwala et al, 2015 ; Palmer and Skaar, 2016 ), and pH ( Heinzen et al, 1996 ; Sturgill-Koszycki and Swanson, 2000 ; Singh et al, 2008 ; Vandal et al, 2008 ). Additionally, T6SS are widely conserved, particularly within Proteobacteria and Bacteroidetes ( Hood et al, 2017 ), and promote colonization of intestinal pathogens ( Fu et al, 2013 ; Sana et al, 2017 ).…”

Metabolic Reprogramming of Vibrio cholerae Impaired in Respiratory NADH Oxidation Is Accompanied by Increased Copper Sensitivity

“…Strains were grown in the presence of 50 g liter Ϫ1 streptomycin at 37°C on mixed amino acids (LB; 10 g liter Ϫ1 tryptone, 5 g liter Ϫ1 yeast extract, 1 g liter Ϫ1 NaCl) or in phosphate-or Tris-buffered M9 minimal medium containing 18.7 mM NH 4 Cl, 0.1 mM CaCl 2 , 0.1 mM MgSO 4 , 40 mg liter Ϫ1 each of methionine, threonine, histidine, and leucine, and 2 mg liter Ϫ1 thiamine, with 0.2% (wt/vol) glucose as a carbon source at pH 7.2. In addition, phosphate-M9 contained 7 g liter Ϫ1 Na 2 HPO 4 , 3 g liter Ϫ1 KH 2 PO 4 , 0.5 g liter Ϫ1 NaCl; Tris-M9 contained 20 mM Tris-HCl, pH 7.2, 1.36 g liter Ϫ1 KH 2 PO 4 , and 2.3 g liter Ϫ1 NaCl (51). It should be noted that 18.7 mM NH 4 Cl is a limiting ammonium concentration for growth of E. coli (29), whereas the amount of phosphate (10 mM KH 2 PO 4 ) in Tris-buffered medium is not limiting for V. cholerae (52).…”