BtuJ1, a novel surface-exposed B 12 -binding protein in Bacteroidetes , functions as an extracellular vitamin reservoir that enhances fitness
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The acquisition of vitamin B 12 and related cobamides is a key determinant for the fitness of Bacteroidetes in the gut. Depending on the species, this uptake process relies on one to four transport systems centered on conserved core outer membrane (OM) complexes composed of the TonB-dependent transporter BtuB and the surface-exposed lipoprotein BtuG. Additionally, the surface-exposed lipoprotein BtuH, although not tightly associated with the BtuBG complex, contributes to cobamide uptake and provides a fitness advantage. Here, we report the functional and structural characterization of BtuJ1 from Bacteroides thetaiotaomicron (B. theta) , a novel B 12 -binding lipoprotein. Under limiting B 12 conditions, BtuJ1 is the most abundant component among the three B 12 -transport systems encoded by B. theta . BtuJ1 is surface exposed and binds vitamin B 12 and cobinamide (an intermediate in B 12 biosynthesis) with low nM affinity, conferring a fitness advantage in B 12 -limited environments. In vitro B 12 transfer experiments suggest a role for BtuJ1 as an extracellular reservoir for B 12 , expanding the functionalities of the diverse group of accessory OM proteins employed by Bacteroides to scavenge this essential cofactor in the competitive environment of the human gut.
IMPORTANCE
Understanding how key molecules support bacterial colonization of the human GI tract is essential to rationalize the structure of the complex microbial community inhabiting the distal gut. The Bacteroidetes are one of the dominant phyla in this environment. Given that most Bacteroidetes cannot make vitamin B 12 but depend on it for growth, the fitness of many species likely depends on the acquisition of vitamin B 12 . Unlike the classical model bacterium Escherichia coli , which encodes a single OM B 12 transporter, the genomes of Bacteroidetes often encode multiple uptake systems comprising a heterogeneous repertoire of surface-exposed lipoproteins. These proteins may assist OM assemblies for vitamin B 12 transport that provide fitness advantages in vivo .
