Abstract
Iron, an essential element for all organisms, acts as a cofactor of enzymes in bacterial degradation of recalcitrant aromatic compounds. The bacterial family, Sphingomonadaceae comprises various degraders of recalcitrant aromatic compounds; however, little is known about their iron acquisition system. Here, we investigated the iron acquisition system in a model bacterium capable of degrading lignin-derived aromatics, Sphingobium sp. strain SYK-6. Analyses of SYK-6 mutants revealed that FiuA (SLG_34550), a TonB-dependent receptor (TBDR), was the major outer membrane iron transporter. Three other TBDRs encoded by SLG_04340, SLG_04380, and SLG_10860 also participated in iron uptake, and tonB2 (SLG_34540), one of the six tonB comprising the Ton complex which enables TBDR-mediated transport was critical for iron uptake. The ferrous iron transporter FeoB (SLG_36840) played an important role in iron uptake across the inner membrane. The promoter activities of most of the iron uptake genes were induced under iron-limited conditions, and their regulation is controlled by SLG_29410 encoding the ferric uptake regulator, Fur. Although feoB, among all the iron uptake genes identified is highly conserved in Sphingomonad strains, the outer membrane transporters seem to be diversified. Elucidation of the iron acquisition system promises better understanding of the bacterial degradation mechanisms of aromatic compounds.
Highlights
Iron, an essential element for all organisms, acts as a cofactor of enzymes in bacterial degradation of recalcitrant aromatic compounds
While ∆tonB2 cells only showed growth retardation when grown on VA and SEMP under iron-replete conditions (Fig. 1), under ironlimited conditions, ∆tonB2 cells showed further growth retardation and almost lost the capacity to grow on VA
We conclude that the TonB2-FiuA system plays a significant role in iron acquisition in SYK-6 based on the following observations (Fig. 8): (i) tonB2 and fiuA are essential for normal growth on various carbon sources, (ii) the promoter activities of tonB2 and fiuA were activated under iron-limited conditions and suggested to be regulated by ferric uptake regulator (Fur)[1], and (iii) intracellular iron levels in ∆tonB2 and ∆fiuA cells were significantly reduced. tonB2 and fiuA constituted an operon, and a Fur box sequence was found upstream of each of tonB2 and fiuA (Fig. 4)
Summary
An essential element for all organisms, acts as a cofactor of enzymes in bacterial degradation of recalcitrant aromatic compounds. The bacterial family, Sphingomonadaceae comprises various degraders of recalcitrant aromatic compounds; little is known about their iron acquisition system. The ferrous iron transporter FeoB (SLG_36840) played an important role in iron uptake across the inner membrane. The family Sphingomonadaceae in alphaproteobacteria comprises of many unique strains capable of degrading certain recalcitrant aromatic compounds such as lignin-derived aromatic compounds, dibenzo-p-dioxin, polycyclic aromatic hydrocarbons, and pentachlorophenol[25,26,27,28]. Iron has essential roles in the catabolism of lignin-derived aromatic compounds as exemplified by the presence of ferrous iron in the active centres of ring cleavage dioxygenases and a multicomponent O-demethylase[35,36,37,38,39]. Disruption of tonB2 was seen to affect the growth of SYK-6 and decrease the activity of ferrous iron-requiring 5,5′-dehydrodivanillate O-demethylase, thereby suggesting that tonB2 plays a role in the iron acquisition process[13]
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