Abstract
BackgroundThe mal genes that encode maltose transporters have undergone extensive lateral transfer among ancestors of the archaea Thermococcus litoralis and Pyrococcus furiosus. Bacterial hyperthermophiles of the order Thermotogales live among these archaea and so may have shared in these transfers. The genome sequence of Thermotoga maritima bears evidence of extensive acquisition of archaeal genes, so its ancestors clearly had the capacity to do so. We examined deep phylogenetic relationships among the mal genes of these hyperthermophiles and their close relatives to look for evidence of shared ancestry.ResultsWe demonstrate that the two maltose ATP binding cassette (ABC) transporter operons now found in Tc. litoralis and P. furiosus (termed mal and mdx genes, respectively) are not closely related to one another. The Tc. litoralis and P. furiosus mal genes are most closely related to bacterial mal genes while their respective mdx genes are archaeal. The genes of the two mal operons in Tt. maritima are not related to genes in either of these archaeal operons. They are highly similar to one another and belong to a phylogenetic lineage that includes mal genes from the enteric bacteria. A unique domain of the enteric MalF membrane spanning proteins found also in these Thermotogales MalF homologs supports their relatively close relationship with these enteric proteins. Analyses of genome sequence data from other Thermotogales species, Fervidobacterium nodosum, Thermosipho melanesiensis, Thermotoga petrophila, Thermotoga lettingae, and Thermotoga neapolitana, revealed a third apparent mal operon, absent from the published genome sequence of Tt. maritima strain MSB8. This third operon, mal3, is more closely related to the Thermococcales' bacteria-derived mal genes than are mal1 and mal2. F. nodosum, Ts. melanesiensis, and Tt. lettingae have only one of the mal1-mal2 paralogs. The mal2 operon from an unknown species of Thermotoga appears to have been horizontally acquired by a Thermotoga species that had only mal1.ConclusionThese data demonstrate that the Tc. litoralis and P. furiosus mdx maltodextrin transporter operons arose in the Archaea while their mal maltose transporter operons arose in a bacterial lineage, but not the same lineage as the two maltose transporter operons found in the published Tt. maritima genome sequence. These Tt. maritima maltose transporters are phylogenetically and structurally similar to those found in enteric bacteria and the mal2 operon was horizontally transferred within the Thermotoga lineage. Other Thermotogales species have a third mal operon that is more closely related to the bacterial Thermococcales mal operons, but the data do not support a recent horizontal sharing of that operon between these groups.
Highlights
The mal genes that encode maltose transporters have undergone extensive lateral transfer among ancestors of the archaea Thermococcus litoralis and Pyrococcus furiosus
Evolution of the mal and mdx genes in the Thermococcales Previous sequence comparisons using BLAST analyses indicated that one mal operon transferred from an ancestor of Tc. litoralis to an ancestor of P. furiosus, likely involving a transposition mediated by the insertion sequences found in P. furiosus [8]
The top 250 hits were aligned using ClustalX and used to construct neighbor joining trees. Using these preliminary relationships as a guide, sequences were chosen from archaea, Thermotogales species, and bacteria closely related to the archaeal sequences to represent a broad spectrum of taxa
Summary
The mal genes that encode maltose transporters have undergone extensive lateral transfer among ancestors of the archaea Thermococcus litoralis and Pyrococcus furiosus. Bacterial hyperthermophiles of the order Thermotogales live among these archaea and so may have shared in these transfers. The genome sequence of Thermotoga maritima bears evidence of extensive acquisition of archaeal genes, so its ancestors clearly had the capacity to do so. The genome sequence of the bacterial hyperthermophile Thermotoga maritima revealed evidence of extensive horizontal gene transfer (HGT) with archaea [1]. Many of the genes that have been shared with archaea encode ATP binding cassette (ABC) transporters. Its genome encodes the second highest proportion of ATP-dependent transporter genes (including ABC transporters) among currently sequenced bacterial and archaeal genomes [5]. Some of the Tt. maritima transporters have been experimentally shown to encode sugar binding proteins [4] including two proteins that bind maltose [6]
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