Limitations of Compositional Approach to Identifying Horizontally Transferred Genes

Abstract. Genes with atypical G+C content and pattern of codon usage in a certain genome are possibly of exotic origin, and this idea has been applied to identify horizontal events. In this way, it was postulated that a total of 755 genes in the E. coli genome are relics of horizontal events after the divergence of E. coli from the Salmonella lineage 100 million years ago (Lawrence and Ochman, 1998). In this paper we propose a new way to study sequence composition more thoroughly. We found that although the 755 genes differ in composition from other genes in the E. coli genome, the difference is minor. If we accepted that these genes are horizontally transferred, then (1) it would be more likely that they were transferred from genomes evolutionarily closely related to E. coli; but (2) the dating method used by Lawrence and Ochman (1997, 1998) largely underestimated the average age of introduced sequences in the E. coli genome, in particular, most of the 755 genes should be introduced into E. coli before, instead of after, the divergence of E. coli from the Salmonella lineage. Our study reveals that atypical G+C content and pattern of codon usage are not reliable indicators of horizontal gene transfer events.

[1]  W. Fitch,et al.  Evidence from nuclear sequences that invariable sites should be considered when sequence divergence is calculated. , 1989, Molecular biology and evolution.

[2]  H. Ochman,et al.  Molecular archaeology of the Escherichia coli genome. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[3]  E N Trifonov,et al.  Linguistic measure of taxonomic and functional relatedness of nucleotide sequences. , 1990, Journal of biomolecular structure & dynamics.

[4]  E Pennisi,et al.  Genome Data Shake Tree of Life , 1998, Science.

[5]  D. Labie,et al.  Molecular Evolution , 1991, Nature.

[6]  T. Gaasterland,et al.  Archaeal genomics. , 1999, Current opinion in microbiology.

[7]  E V Koonin,et al.  Evidence for massive gene exchange between archaeal and bacterial hyperthermophiles. , 1998, Trends in genetics : TIG.

[8]  R. Ivarie,et al.  Mono- through hexanucleotide composition of the Escherichia coli genome: a Markov chain analysis. , 1987, Nucleic acids research.

[9]  N. Sueoka.  Variation and heterogeneity of base composition of deoxyribonucleic acids: A compilation of old and new data , 1961 .

[10]  S. Salzberg,et al.  Evidence for lateral gene transfer between Archaea and Bacteria from genome sequence of Thermotoga maritima , 1999, Nature.

[11]  Peer Bork,et al.  Lateral Gene Transfer, Genome Surveys, and the Phylogeny of Prokaryotes , 1999 .

[12]  G. Olsen,et al.  Archaeal and bacterial hyperthermophiles: horizontal gene exchange or common ancestry? , 1999, Trends in genetics : TIG.

[13]  Michael Y. Galperin,et al.  Comparison of archaeal and bacterial genomes: computer analysis of protein sequences predicts novel functions and suggests a chimeric origin for the archaea , 1997, Molecular microbiology.

[14]  J. Lake,et al.  Horizontal gene transfer among genomes: the complexity hypothesis. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[15]  H. Ochman,et al.  Lateral gene transfer and the nature of bacterial innovation , 2000, Nature.

[16]  E. Pennisi.  Is It Time to Uproot the Tree of Life? , 1999, Science.

[17]  R. Overbeek,et al.  The winds of (evolutionary) change: breathing new life into microbiology. , 1996, Journal of bacteriology.

[18]  S Karlin,et al.  Compositional biases of bacterial genomes and evolutionary implications , 1997, Journal of bacteriology.

[19]  H. Ochman,et al.  Amelioration of Bacterial Genomes: Rates of Change and Exchange , 1997, Journal of Molecular Evolution.

[20]  R. Doolittle,et al.  Determining Divergence Times of the Major Kingdoms of Living Organisms with a Protein Clock , 1996, Science.

[21]  L. Orgel,et al.  Phylogenetic Classification and the Universal Tree , 1999 .

[22]  J. Lake,et al.  Genomic evidence for two functionally distinct gene classes. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[23]  Doolittle Wf.  Phylogenetic Classification and the Universal Tree , 1999 .

[24]  S Karlin,et al.  Compositional differences within and between eukaryotic genomes. , 1997, Proceedings of the National Academy of Sciences of the United States of America.