Catecholamine-Stimulated Growth of Requires the TonB2 Energy Transduction System but Is Independent of the Amonabactin Siderophore

Overview

Journal Front Cell Infect Microbiol

Specialties Cell Biology
Infectious Diseases
Microbiology

Date 2016 Dec 27

PMID 28018865

Citations 9

Authors

Yuhao Dong

Jin Liu

Maoda Pang

Hechao Du

Nannan Wang

Furqan Awan

Chengping Lu

Yongjie Liu

Affiliations

Soon will be listed here.

Abstract

The growth-stimulating effects of catecholamine stress hormones have been demonstrated in many pathogens. However, catecholamine-induced growth and its underlying mechanisms remain poorly understood in . The present study sought to demonstrate that norepinephrine (NE), epinephrine (Epi), dopamine (Dopa), and L-dopa stimulate the growth of in iron-restricted media containing serum. NE exhibited the strongest growth stimulation, which could be blocked by adrenergic antagonists. Furthermore, it was demonstrated that NE could sequester iron from transferrin, thereby providing a more accessible iron source for utilization by . The deletion of the gene associated with amonabactin synthesis revealed that the amonabactin siderophore is not required for NE-stimulated growth. However, the deletion of the TonB2 energy transduction system resulted in the loss of growth promotion by NE, indicating that a specific TonB-dependent outer membrane receptor might be involved in the transport of iron from transferrin. Collectively, our data show that catecholamine sensing promotes the growth of in a manner that is dependent on the TonB2 energy transduction system.

Citing Articles

Effects of the stress hormone norepinephrine on the probiotic properties of : antibacterial colonization, anti-inflammation, and antioxidation.

Niu L, Gao M, Li Y, Wang C, Zhang C, Duan H Front Microbiol. 2025; 16:1526362.

PMID: 39996081 PMC: 11849050. DOI: 10.3389/fmicb.2025.1526362.

The dual role of TonB genes in turnerbactin uptake and carbohydrate utilization in the shipworm symbiont .

Naka H, Haygood M Appl Environ Microbiol. 2023; 89(12):e0074423.

PMID: 38009998 PMC: 10734418. DOI: 10.1128/aem.00744-23.

In Vitro Antibiofilm Activity of Resveratrol against .

Qin T, Chen K, Xi B, Pan L, Xie J, Lu L Antibiotics (Basel). 2023; 12(4).

PMID: 37107048 PMC: 10135085. DOI: 10.3390/antibiotics12040686.

Norepinephrine and Serotonin Can Modulate the Behavior of the Probiotic NCIMB10415 towards the Host: Is a Putative Surface Sensor Involved?.

Scardaci R, Bietto F, Racine P, Boukerb A, Lesouhaitier O, Feuilloley M Microorganisms. 2022; 10(3).

PMID: 35336063 PMC: 8954575. DOI: 10.3390/microorganisms10030487.

Inter-Kingdom Signaling of Stress Hormones: Sensing, Transport and Modulation of Bacterial Physiology.

Boukerb A, Cambronel M, Rodrigues S, Mesguida O, Knowlton R, Feuilloley M Front Microbiol. 2021; 12:690942.

PMID: 34690943 PMC: 8526972. DOI: 10.3389/fmicb.2021.690942.

References

Li L, Xu Z, Zhou Y, Sun L, Liu Z, Chen H . Global effects of catecholamines on Actinobacillus pleuropneumoniae gene expression. PLoS One. 2012; 7(2):e31121. PMC: 3275570. DOI: 10.1371/journal.pone.0031121. View

Marchal K, De Keersmaecker S, Monsieurs P, van Boxel N, Lemmens K, Thijs G . In silico identification and experimental validation of PmrAB targets in Salmonella typhimurium by regulatory motif detection. Genome Biol. 2004; 5(2):R9. PMC: 395753. DOI: 10.1186/gb-2004-5-2-r9. View

Galindo C, Gutierrez Jr C, Chopra A . Potential involvement of galectin-3 and SNAP23 in Aeromonas hydrophila cytotoxic enterotoxin-induced host cell apoptosis. Microb Pathog. 2006; 40(2):56-68. DOI: 10.1016/j.micpath.2005.11.001. View

Sandrini S, Alghofaili F, Freestone P, Yesilkaya H . Host stress hormone norepinephrine stimulates pneumococcal growth, biofilm formation and virulence gene expression. BMC Microbiol. 2014; 14:180. PMC: 4105557. DOI: 10.1186/1471-2180-14-180. View

Melton-Witt J, McKay S, Portnoy D . Development of a single-gene, signature-tag-based approach in combination with alanine mutagenesis to identify listeriolysin O residues critical for the in vivo survival of Listeria monocytogenes. Infect Immun. 2012; 80(6):2221-30. PMC: 3370594. DOI: 10.1128/IAI.06196-11. View

Eisenhofer G, Aneman A, Hooper D, Rundqvist B, Friberg P . Mesenteric organ production, hepatic metabolism, and renal elimination of norepinephrine and its metabolites in humans. J Neurochem. 1996; 66(4):1565-73. DOI: 10.1046/j.1471-4159.1996.66041565.x. View

Schwyn B, NEILANDS J . Universal chemical assay for the detection and determination of siderophores. Anal Biochem. 1987; 160(1):47-56. DOI: 10.1016/0003-2697(87)90612-9. View

Lindqvist R, Barmark G . Specific growth rate determines the sensitivity of Escherichia coli to lactic acid stress: implications for predictive microbiology. Biomed Res Int. 2014; 2014:471317. PMC: 4109666. DOI: 10.1155/2014/471317. View

Kasvosve I, Delanghe J . Total iron binding capacity and transferrin concentration in the assessment of iron status. Clin Chem Lab Med. 2002; 40(10):1014-8. DOI: 10.1515/CCLM.2002.176. View

10.

Freestone P, Lyte M . Microbial endocrinology: experimental design issues in the study of interkingdom signalling in infectious disease. Adv Appl Microbiol. 2008; 64:75-105. DOI: 10.1016/S0065-2164(08)00402-4. View

11.

Abolghait S . Suicide plasmid-dependent IS1-element untargeted integration into Aeromonas veronii bv. sobria generates brown pigment-producing and spontaneous pelleting mutant. Curr Microbiol. 2013; 67(1):91-9. DOI: 10.1007/s00284-013-0335-4. View

12.

Barghouthi S, Payne S, Arceneaux J, Byers B . Cloning, mutagenesis, and nucleotide sequence of a siderophore biosynthetic gene (amoA) from Aeromonas hydrophila. J Bacteriol. 1991; 173(16):5121-8. PMC: 208203. DOI: 10.1128/jb.173.16.5121-5128.1991. View

13.

Reading N, Torres A, Kendall M, Hughes D, Yamamoto K, Sperandio V . A novel two-component signaling system that activates transcription of an enterohemorrhagic Escherichia coli effector involved in remodeling of host actin. J Bacteriol. 2007; 189(6):2468-76. PMC: 1899401. DOI: 10.1128/JB.01848-06. View

14.

Freestone P, Haigh R, Williams P, Lyte M . Involvement of enterobactin in norepinephrine-mediated iron supply from transferrin to enterohaemorrhagic Escherichia coli. FEMS Microbiol Lett. 2003; 222(1):39-43. DOI: 10.1016/S0378-1097(03)00243-X. View

15.

Lacoste A, Jalabert F, Malham S, Cueff A, Poulet S . Stress and stress-induced neuroendocrine changes increase the susceptibility of juvenile oysters (Crassostrea gigas) to Vibrio splendidus. Appl Environ Microbiol. 2001; 67(5):2304-9. PMC: 92871. DOI: 10.1128/AEM.67.5.2304-2309.2001. View

16.

Tenenbaum T, Bloier C, Adam R, Reinscheid D, Schroten H . Adherence to and invasion of human brain microvascular endothelial cells are promoted by fibrinogen-binding protein FbsA of Streptococcus agalactiae. Infect Immun. 2005; 73(7):4404-9. PMC: 1168575. DOI: 10.1128/IAI.73.7.4404-4409.2005. View

17.

Bansal T, Englert D, Lee J, Hegde M, Wood T, Jayaraman A . Differential effects of epinephrine, norepinephrine, and indole on Escherichia coli O157:H7 chemotaxis, colonization, and gene expression. Infect Immun. 2007; 75(9):4597-607. PMC: 1951185. DOI: 10.1128/IAI.00630-07. View

18.

Nakano M, Takahashi A, Sakai Y, Kawano M, Harada N, Mawatari K . Catecholamine-induced stimulation of growth in Vibrio species. Lett Appl Microbiol. 2007; 44(6):649-53. DOI: 10.1111/j.1472-765X.2007.02136.x. View

19.

Pang M, Jiang J, Xie X, Wu Y, Dong Y, Kwok A . Novel insights into the pathogenicity of epidemic Aeromonas hydrophila ST251 clones from comparative genomics. Sci Rep. 2015; 5:9833. PMC: 4444815. DOI: 10.1038/srep09833. View

20.

Lyte M . Microbial endocrinology and infectious disease in the 21st century. Trends Microbiol. 2004; 12(1):14-20. DOI: 10.1016/j.tim.2003.11.004. View