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Evidence of a large novel gene pool associated with prokaryotic genomic islands.

Hsiao WW, Ung K, Aeschliman D, Bryan J, Finlay BB, Brinkman FS - PLoS Genet. (2005)

Bottom Line: This represents the first comprehensive analysis of novel genes in prokaryotic genomic islands and provides clues regarding the origin of novel genes.Moreover, there are more novel genes within the gene pool associated with genomic islands.Since genomic islands are frequently associated with a particular microbial adaptation, such as antibiotic resistance, pathogen virulence, or metal resistance, this suggests that microbes may have access to a larger "arsenal" of novel genes for adaptation than previously thought.

View Article: PubMed Central - PubMed

Affiliation: Department of Molecular Biology and Biochemistry, Simon Fraser University, Burnaby, British Columbia, Canada.

ABSTRACT
Microbial genes that are "novel" (no detectable homologs in other species) have become of increasing interest as environmental sampling suggests that there are many more such novel genes in yet-to-be-cultured microorganisms. By analyzing known microbial genomic islands and prophages, we developed criteria for systematic identification of putative genomic islands (clusters of genes of probable horizontal origin in a prokaryotic genome) in 63 prokaryotic genomes, and then characterized the distribution of novel genes and other features. All but a few of the genomes examined contained significantly higher proportions of novel genes in their predicted genomic islands compared with the rest of their genome (Paired t test = 4.43E-14 to 1.27E-18, depending on method). Moreover, the reverse observation (i.e., higher proportions of novel genes outside of islands) never reached statistical significance in any organism examined. We show that this higher proportion of novel genes in predicted genomic islands is not due to less accurate gene prediction in genomic island regions, but likely reflects a genuine increase in novel genes in these regions for both bacteria and archaea. This represents the first comprehensive analysis of novel genes in prokaryotic genomic islands and provides clues regarding the origin of novel genes. Our collective results imply that there are different gene pools associated with recently horizontally transmitted genomic regions versus regions that are primarily vertically inherited. Moreover, there are more novel genes within the gene pool associated with genomic islands. Since genomic islands are frequently associated with a particular microbial adaptation, such as antibiotic resistance, pathogen virulence, or metal resistance, this suggests that microbes may have access to a larger "arsenal" of novel genes for adaptation than previously thought.

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Proportion of Novel Genes in Genomic Islands (Red Bars) versus the Rest of the Genome (Blue Bars) according to a COG-Based AnalysisProportions of novel genes are calculated as a percentage of all genes within islands or outside of islands, respectively, for each genome (listed on the x axis). A paired t test indicates that significantly more genes in islands versus non-islands do not have a COG classification (p = 1.20E-18). This phenomenon is uniform across prokaryotic lineages and domains. Similar results are also observed if different datasets are analyzed, or different methods for identifying novel genes are used (Table 3).
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pgen-0010062-g001: Proportion of Novel Genes in Genomic Islands (Red Bars) versus the Rest of the Genome (Blue Bars) according to a COG-Based AnalysisProportions of novel genes are calculated as a percentage of all genes within islands or outside of islands, respectively, for each genome (listed on the x axis). A paired t test indicates that significantly more genes in islands versus non-islands do not have a COG classification (p = 1.20E-18). This phenomenon is uniform across prokaryotic lineages and domains. Similar results are also observed if different datasets are analyzed, or different methods for identifying novel genes are used (Table 3).

Mentions: The most striking observation was that the proportion of genes in the “none” category, which, for readability, we refer to as “proportion of novel genes,” was higher in islands than outside for almost all organisms. On average, 42% of the genes in islands are novel compared to 26% of the genes outside of islands for an organism using the DINUC criteria. The result for the DIMOB dataset is also consistent (53% for islands genes and 28% for outside genes). The actual proportions do vary widely between organisms (though the general trend is consistent) so caution is required when interpreting the means. Figure 1 shows the pair-wise comparison for each organism in the DIMOB dataset and Table S6 tabulates the results for all criteria examined. This observation of a higher proportion of novel genes in islands was statistically significant regardless of whether the DINUC (Paired t test, p-value = 1.27E-18) or the DIMOB (p-value = 1.20E-18; Figure 1) criterion was used to define putative GIs. Since this observation has not been rigorously validated in the past, we decided to characterize and validate this observation further. The other category of genes that is over-represented within islands in both sets of predicted islands (DINUC and DIMOB) is the genes involved in DNA replication, recombination, and repair. Conversely, genes involved in macromolecule biosynthesis (transport and metabolism genes for lipid, amino acid, nucleotide, carbohydrate, and co-enzymes) are present in significantly lower proportions in the predicted islands versus outside of islands. We also found that there is no difference in the proportion of transcriptional genes in islands versus outside of islands. This result may appear to contradict observations made by Jain et al. [38]; however, the differences are likely due more to differences in the type of HGT being detected. Their dataset from six organisms consisted of a rather small set of homologous genes which were more likely to be subject to orthologous displacement than to de novo acquisition. Since sequence compositional approaches are less able to detect orthologous displacement from organisms with similar compositions, our results suggest that if these genes have indeed undergone HGT, the mode of transfer is likely to be homologous recombination between closely related species or ancient HGT that has been subject to amelioration. See Protocol S1 for details regarding this analysis and Table S7 for the tabulated results.


Evidence of a large novel gene pool associated with prokaryotic genomic islands.

Hsiao WW, Ung K, Aeschliman D, Bryan J, Finlay BB, Brinkman FS - PLoS Genet. (2005)

Proportion of Novel Genes in Genomic Islands (Red Bars) versus the Rest of the Genome (Blue Bars) according to a COG-Based AnalysisProportions of novel genes are calculated as a percentage of all genes within islands or outside of islands, respectively, for each genome (listed on the x axis). A paired t test indicates that significantly more genes in islands versus non-islands do not have a COG classification (p = 1.20E-18). This phenomenon is uniform across prokaryotic lineages and domains. Similar results are also observed if different datasets are analyzed, or different methods for identifying novel genes are used (Table 3).
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC1285063&req=5

pgen-0010062-g001: Proportion of Novel Genes in Genomic Islands (Red Bars) versus the Rest of the Genome (Blue Bars) according to a COG-Based AnalysisProportions of novel genes are calculated as a percentage of all genes within islands or outside of islands, respectively, for each genome (listed on the x axis). A paired t test indicates that significantly more genes in islands versus non-islands do not have a COG classification (p = 1.20E-18). This phenomenon is uniform across prokaryotic lineages and domains. Similar results are also observed if different datasets are analyzed, or different methods for identifying novel genes are used (Table 3).
Mentions: The most striking observation was that the proportion of genes in the “none” category, which, for readability, we refer to as “proportion of novel genes,” was higher in islands than outside for almost all organisms. On average, 42% of the genes in islands are novel compared to 26% of the genes outside of islands for an organism using the DINUC criteria. The result for the DIMOB dataset is also consistent (53% for islands genes and 28% for outside genes). The actual proportions do vary widely between organisms (though the general trend is consistent) so caution is required when interpreting the means. Figure 1 shows the pair-wise comparison for each organism in the DIMOB dataset and Table S6 tabulates the results for all criteria examined. This observation of a higher proportion of novel genes in islands was statistically significant regardless of whether the DINUC (Paired t test, p-value = 1.27E-18) or the DIMOB (p-value = 1.20E-18; Figure 1) criterion was used to define putative GIs. Since this observation has not been rigorously validated in the past, we decided to characterize and validate this observation further. The other category of genes that is over-represented within islands in both sets of predicted islands (DINUC and DIMOB) is the genes involved in DNA replication, recombination, and repair. Conversely, genes involved in macromolecule biosynthesis (transport and metabolism genes for lipid, amino acid, nucleotide, carbohydrate, and co-enzymes) are present in significantly lower proportions in the predicted islands versus outside of islands. We also found that there is no difference in the proportion of transcriptional genes in islands versus outside of islands. This result may appear to contradict observations made by Jain et al. [38]; however, the differences are likely due more to differences in the type of HGT being detected. Their dataset from six organisms consisted of a rather small set of homologous genes which were more likely to be subject to orthologous displacement than to de novo acquisition. Since sequence compositional approaches are less able to detect orthologous displacement from organisms with similar compositions, our results suggest that if these genes have indeed undergone HGT, the mode of transfer is likely to be homologous recombination between closely related species or ancient HGT that has been subject to amelioration. See Protocol S1 for details regarding this analysis and Table S7 for the tabulated results.

Bottom Line: This represents the first comprehensive analysis of novel genes in prokaryotic genomic islands and provides clues regarding the origin of novel genes.Moreover, there are more novel genes within the gene pool associated with genomic islands.Since genomic islands are frequently associated with a particular microbial adaptation, such as antibiotic resistance, pathogen virulence, or metal resistance, this suggests that microbes may have access to a larger "arsenal" of novel genes for adaptation than previously thought.

View Article: PubMed Central - PubMed

Affiliation: Department of Molecular Biology and Biochemistry, Simon Fraser University, Burnaby, British Columbia, Canada.

ABSTRACT
Microbial genes that are "novel" (no detectable homologs in other species) have become of increasing interest as environmental sampling suggests that there are many more such novel genes in yet-to-be-cultured microorganisms. By analyzing known microbial genomic islands and prophages, we developed criteria for systematic identification of putative genomic islands (clusters of genes of probable horizontal origin in a prokaryotic genome) in 63 prokaryotic genomes, and then characterized the distribution of novel genes and other features. All but a few of the genomes examined contained significantly higher proportions of novel genes in their predicted genomic islands compared with the rest of their genome (Paired t test = 4.43E-14 to 1.27E-18, depending on method). Moreover, the reverse observation (i.e., higher proportions of novel genes outside of islands) never reached statistical significance in any organism examined. We show that this higher proportion of novel genes in predicted genomic islands is not due to less accurate gene prediction in genomic island regions, but likely reflects a genuine increase in novel genes in these regions for both bacteria and archaea. This represents the first comprehensive analysis of novel genes in prokaryotic genomic islands and provides clues regarding the origin of novel genes. Our collective results imply that there are different gene pools associated with recently horizontally transmitted genomic regions versus regions that are primarily vertically inherited. Moreover, there are more novel genes within the gene pool associated with genomic islands. Since genomic islands are frequently associated with a particular microbial adaptation, such as antibiotic resistance, pathogen virulence, or metal resistance, this suggests that microbes may have access to a larger "arsenal" of novel genes for adaptation than previously thought.

Show MeSH
Related in: MedlinePlus