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

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 Aeromonas hydrophila. The present study sought to demonstrate that norepinephrine (NE), epinephrine (Epi), dopamine (Dopa), and L-dopa stimulate the growth of A. hydrophila 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 A. hydrophila. The deletion of the amoA 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 A. hydrophila in a manner that is dependent on the TonB2 energy transduction system.

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

“…Under lower NE concentration (12.5, 25, and 50 μM), no significant growth differences were observed in A. hydrophila AH196. 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., ; Kinney et al., ). 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., ).…”

“…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, ).…”

“…Recently, Dong et al. () reported that A. hydrophila growth stimulation by NE required the TonB2 energy transduction system instead of the amonabactin siderophore, which implies that bacteria contain stress hormone‐related iron acquisition systems.…”

“…Serum‐SAPI medium was prepared as described by Lyte and Ernst () and Dong et al. () with slight modification. Briefly, the medium contained 0.4990 g glucose, 0.5003 g NH 4 NO 3 , 0.2504 g KH 2 PO 4 , 0.2497 g KCl, and 0.1216 g MgSO 4 in one liter of 10 mM HEPES buffer, which was supplemented with 10% (v/v) fetal bovine serum (FBS, Zhejiang Tianhang Biotechnology, Hangzhou, China).…”

“…Aeromonas hydrophila strains AH33, AH189, AH196, and AH301 ( Serum-SAPI medium was prepared as described by Lyte and Ernst (1992) and Dong et al (2016)…”