Metabolic role of a genetically conserved aldehyde dehydrogenase in bacterial assimilation of various primary amines

Abstract

Primary amines such as n-butylamine and 2-phenylethylamine serve as good nitrogen, carbon, and energy sources for bacterial growth. In many Gram-negative bacterial species, these amines are first oxidized by a periplasmic enzyme, quinohemoprotein amine dehydrogenase (QHNDH), encoded in an operon termed ‘qhp’, consisting of eight genes (qhpABCDEFGR). A gene predicted to encode an aldehyde dehydrogenase is also highly conserved in the vicinity of the qhp operon. In this study, we found that a 5′-upstream region of the aldehyde dehydrogenase gene in Paracoccus denitrificans has a high promoter activity that responds to n-butylamine supplementation in the culture medium, indicating co-regulation with the qhp genes by the transcriptional regulator QhpR. Hence, we designate this gene as the ninth member of the qhp operon, qhpH. Disruption of qhpH in P. denitrificans neither affected bacterial growth on primary amines, nor impaired QHNDH activity, suggesting the presence of another constitutive aldehyde dehydrogenase(s) compensating for the defect of qhpH. Nevertheless, heterologous expression of qhpH along with the eight qhp genes in an amine non-assimilating bacterium, Rhodobacter sphaeroides, significantly enhanced the growth on n-butylamine, as compared to the slow growth without qhpH. The recombinant QhpH purified from Escherichia coli cells showed high aldehyde dehydrogenase activities toward various aldehydes. These findings demonstrate that the qhpH gene encodes an aldehyde dehydrogenase with broad substrate specificity and is evolutionarily conserved with the qhp operon to play a role in an efficient metabolism of various primary amines in Gram-negative bacteria.