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Chapter 2 : The Dynamic Bacterial Genome

Author: Jeffrey G. Lawrence1
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Affiliations: 1: Pittsburgh Bacteriophage Institute and Department of Biological Sciences, University of Pittsburgh, Pittsburgh, PA 15260
Content Type: Monograph
Publication Year: 2005

Category: Microbial Genetics and Molecular Biology; Bacterial Pathogenesis

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Abstract:

The model of a static bacterial chromosome arose from early comparisons of the genetic maps of and . Analyses of complete genome sequences by several methods revealed that the differences in gene content were the result of two complementary processes: the gain of new genes by horizontal gene transfer from distantly related organisms, and the loss of ancestral genes from descendent lineages. Directional mutation pressures provide a distinct ‘‘fingerprint’’ to a bacterial genome owing to the differential mutational proclivities of DNA polymerases, the nature and number of mismatch correction systems, the numbers and abundances of tRNA species, and even relative concentrations of precursor nucleotide pools. Thus, genes which appear atypical in their current genomic context may reflect the direction pressures of a donor genome. Aside from changes in gene content, gene order has also been found to be more plastic than once assumed. Mechanisms for DNA rearrangement are well known and have been well measured in the laboratory. Yet despite the opportunities for chromosomal rearrangement, the genetic maps of and seemed to be largely congruent, save the inversion about the terminus of replication. The genome, with all its dynamic parts, steers the organism into the environmental space it is best suited to exploit. Rather than a stale collection of genes having reached optimal performance after billions of years of evolution, one may view a bacterial genome as an ever-changing consortium of genes which cooperate in perpetuating their host organism.

Citation: Lawrence J. 2005. The Dynamic Bacterial Genome, p 19-37. In Higgins N (ed), The Bacterial Chromosome. ASM Press, Washington, DC. doi: 10.1128/9781555817640.ch2

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Mobile Genetic Elements
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The Dynamic Bacterial Genome
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Citation: Lawrence J. 2005. The Dynamic Bacterial Genome, p 19-37. In Higgins N (ed), The Bacterial Chromosome. ASM Press, Washington, DC. doi: 10.1128/9781555817640.ch2
/content/10.1128/9781555817640.chap2.fig2-1
Figure 1.

Correspondence between the first genetic maps of ( ), whose loci are denoted on the inside of the circle, and serovar Typhimurium ( ), whose loci are denoted on the outside of the circle. Genes whose positions were less defined are depicted in parentheses; spacing between genes was adjusted to allow for facile alignment of the two maps. The loci shared between the maps show remarkable conservation of order.

10.1128/9781555817640/fig2-1_thmb.gif
10.1128/9781555817640/fig2-1.gif
Image of Figure 1.
Figure 1.

Correspondence between the first genetic maps of ( ), whose loci are denoted on the inside of the circle, and serovar Typhimurium ( ), whose loci are denoted on the outside of the circle. Genes whose positions were less defined are depicted in parentheses; spacing between genes was adjusted to allow for facile alignment of the two maps. The loci shared between the maps show remarkable conservation of order.

Citation: Lawrence J. 2005. The Dynamic Bacterial Genome, p 19-37. In Higgins N (ed), The Bacterial Chromosome. ASM Press, Washington, DC. doi: 10.1128/9781555817640.ch2
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Figure 2.

Mechanisms of gene transfer and their effects on inferring phylogeny. Homologous recombination serves to unify strains within bacterial taxa; as a result, phylogenies of different genes within these groups will not be congruent, but phylogenies of the same genes found in different lineages—that is, those which do not exchange genes because of the imposition of mismatch correction systems ( )—will be congruent. This system has been invoked to define bacterial species ( ). Gene exchange across large phylogenetic distances does not disrupt these patterns as long as the donor taxa are not included in the analyses. Limitations of this approach are discussed elsewhere ( ).

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Image of Figure 2.
Figure 2.

Mechanisms of gene transfer and their effects on inferring phylogeny. Homologous recombination serves to unify strains within bacterial taxa; as a result, phylogenies of different genes within these groups will not be congruent, but phylogenies of the same genes found in different lineages—that is, those which do not exchange genes because of the imposition of mismatch correction systems ( )—will be congruent. This system has been invoked to define bacterial species ( ). Gene exchange across large phylogenetic distances does not disrupt these patterns as long as the donor taxa are not included in the analyses. Limitations of this approach are discussed elsewhere ( ).

Citation: Lawrence J. 2005. The Dynamic Bacterial Genome, p 19-37. In Higgins N (ed), The Bacterial Chromosome. ASM Press, Washington, DC. doi: 10.1128/9781555817640.ch2
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Figure 3.

The distribution of recently acquired DNA, inferred from the numbers of atypical genes, in various bacterial genomes. Gray bars denote amounts of typical protein-coding sequences, while black bars denote atypical protein-coding sequences, identified as having aberrant composition, dinucleotide fingerprints, and patterns of codon usage bias.

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10.1128/9781555817640/fig2-3.gif
Image of Figure 3.
Figure 3.

The distribution of recently acquired DNA, inferred from the numbers of atypical genes, in various bacterial genomes. Gray bars denote amounts of typical protein-coding sequences, while black bars denote atypical protein-coding sequences, identified as having aberrant composition, dinucleotide fingerprints, and patterns of codon usage bias.

Citation: Lawrence J. 2005. The Dynamic Bacterial Genome, p 19-37. In Higgins N (ed), The Bacterial Chromosome. ASM Press, Washington, DC. doi: 10.1128/9781555817640.ch2
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Figure 4.

Disruption of the operon in serogroup A strain Z2491 ( ). Letters indicate genes; non- genes are indicated by the gray boxes. The nucleotide composition plot shows the %G+C for a 200-base window starting at the position indicated.

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10.1128/9781555817640/fig2-4.gif
Image of Figure 4.
Figure 4.

Disruption of the operon in serogroup A strain Z2491 ( ). Letters indicate genes; non- genes are indicated by the gray boxes. The nucleotide composition plot shows the %G+C for a 200-base window starting at the position indicated.

Citation: Lawrence J. 2005. The Dynamic Bacterial Genome, p 19-37. In Higgins N (ed), The Bacterial Chromosome. ASM Press, Washington, DC. doi: 10.1128/9781555817640.ch2
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Figure 5.

Distribution of oligomers in the genome. Sequence is from Fleischmann et al. ( ); origin and terminus of replication are inferred from strand asymmetry analysis; triangles represent positions as direction of transcription of rRNA operons. The lower panel shows the effects of mutation biases. Strand asymmetry in the genome of is manifested by 14 different octameric oligonucleotides, which are drawn on either the forward or reverse strand. The middle panel shows sequences with both strand asymmetry and a biased distribution with respect to the terminus of replication; the distribution of 23 octamers is shown. The top panel shows a histogram of the distribution of the octamers shown in the middle panel on the leading and lagging strands for 50-kb intervals; intervals were chosen so that the terminus of replication fell between two intervals.

10.1128/9781555817640/fig2-5_thmb.gif
10.1128/9781555817640/fig2-5.gif
Image of Figure 5.
Figure 5.

Distribution of oligomers in the genome. Sequence is from Fleischmann et al. ( ); origin and terminus of replication are inferred from strand asymmetry analysis; triangles represent positions as direction of transcription of rRNA operons. The lower panel shows the effects of mutation biases. Strand asymmetry in the genome of is manifested by 14 different octameric oligonucleotides, which are drawn on either the forward or reverse strand. The middle panel shows sequences with both strand asymmetry and a biased distribution with respect to the terminus of replication; the distribution of 23 octamers is shown. The top panel shows a histogram of the distribution of the octamers shown in the middle panel on the leading and lagging strands for 50-kb intervals; intervals were chosen so that the terminus of replication fell between two intervals.

Citation: Lawrence J. 2005. The Dynamic Bacterial Genome, p 19-37. In Higgins N (ed), The Bacterial Chromosome. ASM Press, Washington, DC. doi: 10.1128/9781555817640.ch2
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Figure 6.

Relationship between the amount of recently acquired DNA and information content in bacterial genomes. Genomes used for analysis are shown in Fig. 3 ; information content is measured as corrected, length-normalized average χ of codon usage as described elsewhere ( ).

10.1128/9781555817640/fig2-6_thmb.gif
10.1128/9781555817640/fig2-6.gif
Image of Figure 6.
Figure 6.

Relationship between the amount of recently acquired DNA and information content in bacterial genomes. Genomes used for analysis are shown in Fig. 3 ; information content is measured as corrected, length-normalized average χ of codon usage as described elsewhere ( ).

Citation: Lawrence J. 2005. The Dynamic Bacterial Genome, p 19-37. In Higgins N (ed), The Bacterial Chromosome. ASM Press, Washington, DC. doi: 10.1128/9781555817640.ch2
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