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Chapter 15 : Genomic Flux: Genome Evolution by Gene Loss and Acquisition

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Abstract:

This chapter describes methods for assessing the frequency of successful gene acquisition and the fraction of modern genomes that has been acquired by horizontal transfer of useful phenotypic information. Although both loss and acquisition strongly influence genome evolution, the authors suggest that the two processes are synergistic due to the limits on genome expansion. To assess the contribution of genomic flux to genome evolution and speciation, one must measure rates of gene loss and acquisition. All novel phenotypes were conferred by horizontally transferred genes. Therefore, genes for the diverse metabolic pathways have formed slowly at earlier times and not during the course of competitive invasion of novel ecological niches. Regardless of the relative rates of these two processes, it is clear that gene loss and acquisition have facilitated exploration of novel environments and allowed more rapid divergence of bacterial types in competitive situations. The authors propose that the prevalence of gene clusters stands as evidence that genomic flux has historically been a primary contributor to genome evolution. They have outlined a model for the evolution of bacterial genomes through the synergistic processes of gene acquisition and gene loss. The organization of genes into operons reflects the important role in bacterial evolution and speciation played by genomic flux—the development of bacterial genomes by gene loss and gene acquisition.

Citation: Lawrence J, Roth J. 1999. Genomic Flux: Genome Evolution by Gene Loss and Acquisition, p 263-289. In Charlebois R (ed), Organization of the Prokaryotic Genome. ASM Press, Washington, DC. doi: 10.1128/9781555818180.ch15

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Image of FIGURE 1
FIGURE 1

Genome evolution by genomic flux. A genome is depicted as a set of genes (lines and boxes) ranked by average selection coefficient; classes of genes discussed in Table 1 are noted on the left. Genes inherited vertically are represented by solid lines; foreign genes are indicated by open boxes. Genes below the threshold for maintenance cannot be maintained by natural selection and will be lost by mutation and deletion. Acquired genes introduced by horizontal transfer will ultimately be lost if they fail to confer sufficient fitness.

Citation: Lawrence J, Roth J. 1999. Genomic Flux: Genome Evolution by Gene Loss and Acquisition, p 263-289. In Charlebois R (ed), Organization of the Prokaryotic Genome. ASM Press, Washington, DC. doi: 10.1128/9781555818180.ch15
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Image of FIGURE 2
FIGURE 2

(A) Relationships between overall nucleotide composition of a bacterial genome and nucleotide compositions of the three codon positions (first to third); after Muto and Osawa ( ) and Lawrence and Ochman ( ). The organisms providing the data are shown at the top. The data for and were calculated from 100 and 25% of the genome sequences, respectively, after known horizontally transferred sequences were removed. (B) Process of amelioration used to infer the time of introduction of acquired genes ( ). The acquired genes (shaded symbols) are atypical for the genome (solid symbols) in which they are found. The codon position-specific nucleotide compositions of acquired genes are back-ameliorated ( equation 4 ) until the minimum deviation (by least-squares analysis) from the Muto and Osawa relationships (open symbols) are obtained. The heavy lines indicate the codon position-specific nucleotide compositions during back-amelioration. The arrows indicate the calculated back-amelioration process used to estimate the elapsed time since the sequence showed the pattern of the donor. The inset graph shows the deviation of the curves from the Muto and Osawa relationships as a function of time rather than overall percent G+C.

Citation: Lawrence J, Roth J. 1999. Genomic Flux: Genome Evolution by Gene Loss and Acquisition, p 263-289. In Charlebois R (ed), Organization of the Prokaryotic Genome. ASM Press, Washington, DC. doi: 10.1128/9781555818180.ch15
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Image of FIGURE 3
FIGURE 3

The distribution of times of introduction for horizontally acquired genes in ; after Lawrence and Ochman ( ). All foreign genes that could be ameliorated successively are included. Roughly one-third of the foreign genes are not included because their positional percent G+C contents did not converge to fit the Muto and Osawa relationships (see the text).

Citation: Lawrence J, Roth J. 1999. Genomic Flux: Genome Evolution by Gene Loss and Acquisition, p 263-289. In Charlebois R (ed), Organization of the Prokaryotic Genome. ASM Press, Washington, DC. doi: 10.1128/9781555818180.ch15
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Image of FIGURE 4
FIGURE 4

Schematic representation of the effects of genomic flux on the genome. The events depicted occurred since divergence of and from the common ancestor. The useful gene flux (ABD) depicted above the major arrow describes genes that are kept in the genome long enough to show measurable amelioration. Although large numbers of potentially useful genes enter the chromosome (A) and may be maintained for some time, most of these are ultimately lost (B); however, about 250 remain (D). The number of selectively maintained foreign genes (D) is matched by a loss of ancestral genes (C). The flux below the major arrow (EFGH) represents sequences that provide no selective advantage. Large amounts of DNA with no value are likely introduced into the chromosome (G), but the vast majority are removed by deletion (H). About 500 of these genes are still in the genome but will eventually be removed by mutation and drift; these include those known to be useless (F), like mobile genetic elements, and those merely too recently arrived to have been subject to deletion (E). The newly arrived genes have not been tested by selection, but very few are likely to remain. As shown by the black bars, the ancestral chromosome also contained a portion of selectively useless genes that would have been deleted.

Citation: Lawrence J, Roth J. 1999. Genomic Flux: Genome Evolution by Gene Loss and Acquisition, p 263-289. In Charlebois R (ed), Organization of the Prokaryotic Genome. ASM Press, Washington, DC. doi: 10.1128/9781555818180.ch15
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Image of FIGURE 5
FIGURE 5

Divergence of and genomes. Based on the model presented in the text, the likely events and final genomic consequences of this act of speciation are portrayed. On genomes, triangles indicate acquired foreign material. Open boxes indicate lost ancestral material.

Citation: Lawrence J, Roth J. 1999. Genomic Flux: Genome Evolution by Gene Loss and Acquisition, p 263-289. In Charlebois R (ed), Organization of the Prokaryotic Genome. ASM Press, Washington, DC. doi: 10.1128/9781555818180.ch15
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Image of FIGURE 6
FIGURE 6

Mechanism for clustering of genes by horizontal transfer. The diagram compares the fates of identical alleles of two genes, that together confer a weakly selectable function. In one organism these genes are clustered (C), and in the other they are separated (S). Both sets are equally subject to loss by mutation and drift. However, clustered genes can spread horizontally to new genomes. Following transfer, genes that were essential in the donor become nonessential in the new species. While the selected genes are selectively maintained, the genes are deleted. This tightens the cluster and enhances the likelihood of its further transfer.

Citation: Lawrence J, Roth J. 1999. Genomic Flux: Genome Evolution by Gene Loss and Acquisition, p 263-289. In Charlebois R (ed), Organization of the Prokaryotic Genome. ASM Press, Washington, DC. doi: 10.1128/9781555818180.ch15
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Tables

Generic image for table
TABLE 1

Fitness contributions of bacterial genes

Citation: Lawrence J, Roth J. 1999. Genomic Flux: Genome Evolution by Gene Loss and Acquisition, p 263-289. In Charlebois R (ed), Organization of the Prokaryotic Genome. ASM Press, Washington, DC. doi: 10.1128/9781555818180.ch15

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