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Molecular Biology and Evolution 18:362-375 (2001)
© 2001 Society for Molecular Biology and Evolution


ARTICLE

Phylogenetic Analyses of Two "Archaeal" Genes in Thermotoga maritima Reveal Multiple Transfers Between Archaea and Bacteria

Camilla L. Nesbo*, Stéphane L'Haridon, Karl O. Stetter and W. Ford Doolittle*

*Department of Biochemistry and Molecular Biology, Dalhousie University, Halifax, Canada;
{dagger}Sciences de l'Environnement Marin, Centre National de la Recherche Scientifique and Université de Bretagne Occidentale, Plouzané, France;
{ddagger}Lehrsthul fuer Mikrobiologie und Archaeenzentrum, Universitaet Regensburg, Germany

The genome sequence of Thermotoga maritima revealed that 24% of its open reading frames (ORFs) showed the highest similarity scores to archaeal genes in BLAST analyses. Here we screened 16 strains from the genus Thermotoga and other related Thermotogales for the occurrence of two of these "archaeal" genes: the gene encoding the large subunit of glutamate synthase (gltB) and the myo-inositol 1P synthase gene (ino1). Both genes were restricted to the Thermotoga species within the Thermotogales. The distribution of the two genes, along with results from phylogenetic analyses, showed that they were acquired from Archaea during the divergence of the Thermotogales. Database searches revealed that three other bacteria—Dehalococcoides ethenogenes, Sinorhizobium meliloti, and Clostridium difficile—possess archaeal-type gltBs, and the phylogenetic analyses confirmed at least two lateral gene transfer (LGT) events between Bacteria and Archaea. These LGT events were also strongly supported by gene structure data, as the three domains in bacterial-type gltB are homologous to three independent ORFs in Archaea and Bacteria with archaeal-type gltBs. The ino1 gene has a scattered distribution among Bacteria, and apart from the Thermotoga strains it is found only in Aquifex aeolicus, D. ethenogenes, and some high-G+C Gram-positive bacteria. Phylogenetic analysis of the ino1 sequences revealed three highly supported prokaryotic clades, all containing a mixture of archaeal and bacterial sequences, and suggested that all bacterial ino1 genes had been recruited from archaeal donors. The Thermotoga strains and A. aeolicus acquired this gene independently from different archaeal species. Although transfer of genes from hyperthermophilic Archaea may have facilitated the evolution of bacterial hyperthermophily, between-domain transfers also affect mesophilic species. For hyperthermophiles, we hypothesize that LGT may be as much a consequence as the cause of adaptation to hyperthermophily.


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