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Substrate Specificities and Expression Patterns Reflect the Evolutionary Divergence of Maltose ABC Transporters in Thermotoga maritima

Dhaval M. Nanavati, Tu N. Nguyen, and Kenneth M. Noll^*

Department of Molecular and Cell Biology, University of Connecticut, Storrs, Connecticut

Received 22 October 2004/ Accepted 12 December 2004

Duplication of transporter genes is apparent in the genome sequence of the hyperthermophilic bacterium Thermotoga maritima. The physiological impacts of these duplications are not well understood, so we used the bacterium's two putative maltose transporters to begin a study of the evolutionary relationship between a transporter's function and the control of expression of its genes. We show that the substrate binding proteins encoded by these operons, MalE1 and MalE2, have different substrate specificities and affinities and that they are expressed under different growth conditions. MalE1 binds maltose (dissociation constant [K_D], 24 ± 1 µM), maltotriose (K_D, 8 ± 0.5 nM), and ß-(14)-mannotetraose (K_D, 38 ± 1 µM). In contrast, MalE2 binds maltose (K_D, 8.4 ± 1 µM), maltotriose (K_D, 11.5 ± 1.5 µM), and trehalose (K_D, 9.5 ± 1.0 µM) confirming the findings of Wassenberg et al. (J. Mol. Biol. 295:279-288, 2000). Neither protein binds lactose. We examined the expression of these operons at both the transcriptional and translational levels and found that MalE1 is expressed in cells grown on lactose or guar gum and that MalE2 is highly expressed in starch- and trehalose-grown cells. Evidence is provided that malE1, malF1, and perhaps malG1 are cotranscribed and so constitute an operon. An open reading frame encoding a putative transcriptional regulatory protein adjacent to this operon (TM1200) is also up-regulated in response to growth on lactose. These evolutionarily related transporter operons have diverged both in function and expression to assume apparently different physiological roles.

Present address: Center for Microbial Pathogenesis, University of Connecticut Health Center, Farmington, CT 06030-3710.

This article has been cited by other articles:

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