The hyperthermophilic bacterium Thermotoga maritima has shared many genes with archaea through horizontal gene transfer. Several of these encode putative oligopeptide ATP binding cassette (ABC) transporters. We sought to test the hypothesis that these transporters actually transport sugars by measuring the substrate affinities of their encoded substrate-binding proteins (SBPs). This information will increase our understanding of the selective pressures that allowed this organism to retain these archaeal homologs. By measuring changes in intrinsic fluorescence of these SBPs in response to exposure to various sugars, we found that five of the eight proteins examined bind to sugars. We could not identify the ligands of the SBPs TM0460, TM1150, and TM1199. The ligands for the archaeal SBPs are TM0031 (BglE), the -glucosides cellobiose and laminaribiose; TM0071 (XloE), xylobiose and xylotriose; TM0300 (GloE), large glucose oligosaccharides represented by xyloglucans; TM1223 (ManE), -1,4-mannobiose; and TM1226 (ManD), -1,4-mannobiose, -1,4-mannotriose, -1,4-mannotetraose, -1,4-galactosyl mannobiose, and cellobiose. For comparison, seven bacterial putative sugar-binding proteins were examined and ligands for three (TM0595, TM0810, and TM1855) were not identified. The ligands for these bacterial SBPs are TM0114 (XylE), xylose; TM0418 (InoE), myo-inositol; TM0432 (AguE), ␣-1,4-digalactouronic acid; and TM0958 (RbsB), ribose. We found that T. maritima does not grow on several complex polypeptide mixtures as sole sources of carbon and nitrogen, so it is unlikely that these archaeal ABC transporters are used primarily for oligopeptide transport. Since these SBPs bind oligosaccharides with micromolar to nanomolar affinities, we propose that they are used primarily for oligosaccharide transport.
Horizontal gene transfer (HGT) is nature's mechanism for sharing evolved physiological traits among the members of microbial communities. The extent to which such transfers can be successful is best illustrated by the fact that Archaea-derived genes are found in many bacterial genomes, particularly those in the hyperthermophile Thermotoga maritima. The success of these intergenomic transfers depends upon the successful transcription of the newly acquired archaeal genes using a bacterial transcription machinery that does not recognize archaeal transcriptional signals. To examine how nature solves this problem, we looked to the T. maritima genome for examples of interdomain transfers. Here we lay the groundwork to examine this problem by more clearly delineating the phylogenetic history of Archaea-derived transporter genes in this genome. We find that five of these polysaccharide transporters were derived from the Archaea and one came from the Archaea after that lineage inherited it from the Bacteria. These data can be used for more detailed examinations of the recombinations that allowed these transporters to be expressed in a bacterial host. This work will guide examinations of the genome sequences from other members of the Thermotogales, which will become available.
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