Abstract
In this study, we show that Bacteroides species utilize Fe(III)‐xenosiderophores as the only source of exogenous iron to support growth under iron‐limiting conditions in vitro anaerobically. Bacteroides fragilis was the only species able to utilize Fe(III)‐ferrichrome while Bacteroides vulgatus ATCC 8482 and Bacteroides thetaiotaomicron VPI 5482 were able to utilize both Fe(III)‐enterobactin and Fe(III)‐salmochelin S4 as the only source of iron in a dose‐dependent manner. We have investigated the way B. fragilis assimilates Fe(III)‐ferrichrome as initial model to understand the utilization of xenosiderophores in anaerobes. B. fragilis contains two outer membrane TonB‐dependent transporters (TBDTs), FchA1 and FchA2, which are homologues to Escherichia coli ferrichrome transporter FhuA. The disruption of fchA1 gene had only partial growth defect on Fe(III)‐ferrichrome while the fchA2 mutant had no growth defect compared to the parent strain. The genetic complementation of fchA1 gene restored growth to parent strain levels indicating that it plays a role in Fe(III)‐ferrichrome assimilation though we cannot rule out some functional overlap in transport systems as B. fragilis contains abundant TBDTs whose functions are yet not understood. However, the growth of B. fragilis on Fe(III)‐ferrichrome was abolished in a feoAB mutant indicating that Fe(III)‐ferrichrome transported into the periplasmic space was reduced in the periplasm releasing ferrous iron prior to transport through the FeoAB transport system. Moreover, the release of iron from the ferrichrome may be linked to the thiol redox system as the trxB deletion mutant was also unable to grow in the presence of Fe(III)‐ferrichrome. The genetic complementation of feoAB and trxB mutants completely restored growth on Fe(III)‐ferrichrome. Taken together, these findings show that Bacteroides species have developed mechanisms to utilize ferric iron bound to xenosiderophores under anaerobic growth conditions though the regulation and role in the biology of Bacteroides in the anaerobic intestinal environment remain to be understood.
Highlights
The human colon is the most densely populated organ with commensal microbes and Bacteroides species are among the predominant members of that microbiota (Eckburg et al, 2005; Gibson & Roberfroid, 1999; Hooper, Midtvedt, & Gordon, 2002; Savage, 1977)
We have demonstrated that Bacteroides species have developed strategies for acquisition of Fe(III)-bound siderophores produced by other organisms in vitro
Progress has been made in recent years in the understanding of the structures and functions of the SusC-like protein family of TonB- dependent transporters (TBDTs) (Foley, Cockburn, & Koropatkin, 2016; Martens et al, 2011, 2014), very little is known about Bacteroides TBDTs role in the assimilation of iron-chelate complexes
Summary
The human colon is the most densely populated organ with commensal microbes and Bacteroides species are among the predominant members of that microbiota (Eckburg et al, 2005; Gibson & Roberfroid, 1999; Hooper, Midtvedt, & Gordon, 2002; Savage, 1977). Bacteroides spp. can reach numbers in excess of 1011 cells/g of feces and account for about 30–40% of total bacteria where at least 500 different species have been so far reported (Hooper et al, 2002; Smith, Rocha, & Paster, 2006; Xu & Gordon, 2003; Xu et al, 2003). The presence of ferric iron in the colon correlates with recent studies demonstrating that E. coli mono- or dual-associated with Bacteroides thetaiotaomicron in the colonic mucus layer of germ- free mice induces the expression of genes required for synthesis and uptake of catechol-type siderophore enterobactin as well as for the uptake of the hydroxamate-type ferrichrome for the acquisition of ferric iron (Li et al, 2015) These studies indicate that both ferrous and ferric forms of iron are present in the colon but their availability is likely to be limited (Kortman, Raffatellu, Swinkels, & Tjalsma, 2014). We show that Bacteroides have the capability to grow in the presence of Fe(III)- xenosiderophores under iron-limiting conditions anaerobically in vitro
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