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The genes and enzymes for the catabolism of galactitol, D-tagatose, and related carbohydrates in Klebsiella oxytoca M5a1 and other enteric bacteria display convergent evolution

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Abstract

Enteric bacteria (Enteriobacteriaceae) carry on their single chromosome about 4000 genes that all strains have in common (referred to here as “obligatory genes”), and up to 1300 “facultative” genes that vary from strain to strain and from species to species. In closely related species, obligatory and facultative genes are orthologous genes that are found at similar loci. We have analyzed a set of facultative genes involved in the degradation of the carbohydrates galactitol, D-tagatose, D-galactosamine and N-acetyl-galactosamine in various pathogenic and non-pathogenic strains of these bacteria. The four carbohydrates are transported into the cell by phosphotransferase (PTS) uptake systems, and are metabolized by closely related or even identical catabolic enzymes via pathways that share several intermediates. In about 60% of Escherichia coli strains the genes for galactitol degradation map to a gat operon at 46.8 min. In strains of Salmonella enterica, Klebsiella pneumoniae and K. oxytoca, the corresponding gat genes, although orthologous to their E. coli counterparts, are found at 70.7 min, clustered in a regulon together with three tag genes for the degradation of D-tagatose, an isomer of D-fructose. In contrast, in all the E. coli strains tested, this chromosomal site was found to be occupied by an aga/kba gene cluster for the degradation of D-galactosamine and N-acetyl-galactosamine. The aga/kba and the tag genes were paralogous either to the gat cluster or to the fru genes for degradation of D-fructose. Finally, in more then 90% of strains of both Klebsiella species, and in about 5% of the E. coli strains, two operons were found at 46.8 min that comprise paralogous genes for catabolism of the isomers D-arabinitol (genes atl or dal) and ribitol (genes rtl or rbt). In these strains gat genes were invariably absent from this location, and they were totally absent in S. enterica. These results strongly indicate that these various gene clusters and metabolic pathways have been subject to convergent evolution among the Enterobacteriaceae. This apparently involved recent horizontal gene transfer and recombination events, as indicated by major chromosomal rearrangements found in their immediate vicinity.

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Acknowledgments

We would like to thank E. Placke and L. Schmieding for help in preparing the manuscript, the Deutsche Forschungsgemeinschaft for grants awarded to A. Shakeri-Garakani and A. Brinkkötter through the Graduiertenkolleg “Molekulare Zellbiologie/Membranbiologie”, and to J.W. Lengeler, K. Schmid, and S. Turgut through SFB171 and SFB 431, and the Verband der Chemischen Industrie for financial support to J.W. Lengeler.

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  1. Fachbereich Biologie/Chemie, Universität Osnabrück, Barbarastr.11, 49069, Osnabrück, Germany

    A. Shakeri-Garakani, A. Brinkkötter, K. Schmid, S. Turgut & J. W. Lengeler

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  1. A. Shakeri-Garakani
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  2. A. Brinkkötter
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  3. K. Schmid
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  4. S. Turgut
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  5. J. W. Lengeler
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Correspondence to J. W. Lengeler.

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Communicated by A. Kondorosi

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Shakeri-Garakani, A., Brinkkötter, A., Schmid, K. et al. The genes and enzymes for the catabolism of galactitol, D-tagatose, and related carbohydrates in Klebsiella oxytoca M5a1 and other enteric bacteria display convergent evolution. Mol Genet Genomics 271, 717–728 (2004). https://doi.org/10.1007/s00438-004-1022-8

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