Catecholamines Promote Actinobacillus pleuropneumoniae Growth by Regulating Iron Metabolism

Abstract

Catecholamines are host stress hormones that can induce the growth of many bacteria by facilitating iron utilization and/or regulate the expression of virulence genes through specific hormone receptors. Whether these two responsive pathways are interconnected is unknown. In our previous study, it was found that catecholamines can regulate the expression of a great number of genes of Actinobacillus pleuropneumoniae, an important swine respiratory pathogen. However, bacterial growth was not affected by catecholamines in rich medium. In this study, it was discovered that catecholamines affected A. pleuropneumoniae growth in chemically defined medium (CDM). We found that serum inhibited A. pleuropneumoniae growth in CDM, while epinephrine, norepinephrine and dopamine promoted A. pleuropneumoniae growth in the CDM containing serum. The known bacterial hormone receptor QseC didn’t play roles in this process. Ion-supplementation and transcriptome analysis indicated that serum addition resulted in iron-restricted conditions which were alleviated by the addition of catecholamines. Transferrin, one of the components in serum, inhibited the growth of A. pleuropneumoniae in CDM, an effect reversed by addition of catecholamines in a TonB2-dependent manner. Our data demonstrate that catecholamines promote A. pleuropneumoniae growth by regulating iron-acquisition and metabolism, which is independent of the adrenergic receptor QseC.

Overexpression of Porcine Beta-Defensin 2 Enhances Resistance to Actinobacillus pleuropneumoniae Infection in Pigs

“…A. pleuropneumoniae 4074 (serovar 1) was cultured on tryptic soy agar (TSA) or in tryptic soy broth (TSB; Difco Laboratories, USA) supplemented with 10 g/ml of NAD and 10% (vol/vol) filtered cattle serum at 37°C as described previously (14). The susceptibility of the TG pigs to A. pleuropneumoniae infection was evaluated in two infection studies.…”

Update onActinobacillus pleuropneumoniae-knowledge, gaps and challenges

“…Iron metabolism is of high importance for the pathogen to survive and multiply in the host. It has been shown recently that catecholamine binding to App facilitates iron uptake, although iron availability is highly decreased during acute infection as a physiological acute reaction during inflammation (Humann‐Ziehank et al., ; Li et al., ). The fact that more than 50 App genes are involved in iron uptake and metabolism (Xu et al., ), some of which are differentially expressed during infection (Deslandes et al., ; Klitgaard, Friis, Jensen, Angen, & Boye, ), supports the major importance of this bacterial adaptation strategy for disease pathogenesis (Bossé et al., ).…”

“…The effect of stress hormones such as catecholamine on virulence factor expression in App has been shown at a molecular level (Li et al., ). In addition, a status of well‐being of pigs in an enriched housing system had an influence on immune parameters and led to a reduction of lung alterations after experimental infection (van Dixhoorn et al., ).…”

Functional characterization of Aggregatibacter actinomycetemcomitans QSEBC : a bacterial adrengeric receptor and global regulator of virulence.

“…For E.coli, Salmonella, and A. pleuropneumoniae, it was found that the stimulation of planktonic growth was independent of QseC since a mutant strain still underwent catecholamine mediated planktonic growth stimulation [57,80,92]. This is consistent with the results of the CAT-Fe mediated planktonic growth stimulation in A. actinomycetemcomitans, which was also independent of a functional QseC.…”

“…This stimulation of planktonic growth is independent of a functional QseC [92], but biofilm formation is attenuated for a QseC mutant in the presence of catecholamines [119]. In addition, the stimulation of planktonic growth in E. coli can be blocked by the addition of adrenergic receptor antagonists [80,55].…”