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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 SUPERFAMILY-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 higher proportions of genes in islands (red bars) versus outside islands (non-islands; purple bars) do not have a SUPERFAMILY prediction (potential novel genes; p = 4.43E-14).
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pgen-0010062-g002: Proportion of Novel Genes in Genomic Islands (Red Bars) versus the Rest of the Genome (Blue Bars) according to a SUPERFAMILY-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 higher proportions of genes in islands (red bars) versus outside islands (non-islands; purple bars) do not have a SUPERFAMILY prediction (potential novel genes; p = 4.43E-14).

Mentions: COG analysis is suitable for detecting orthologous genes but may fail to identify more “distant” homologs that have complex evolution histories (e.g., multiple duplications and deletions among lineages). To complement the COG-based analysis of novel genes in GIs, we adapted another independent method to detect novel hypothetical proteins called SUPERFAMILY analysis [39]. We chose this method because of its reported accuracy and its ability to detect more remote homologs based on structurally conserved similarities [40]. Genes that cannot be assigned to a SUPERFAMILY do not have detectable structural domain homologs in the SCOP database, and therefore are more likely to be novel genes. In both the DINUC and DIMOB datasets, we observed that the proportion of such novel genes is significantly higher in islands compared with outside of islands (see Table 3 for a list of p-values from paired t tests). Pair-wise comparison for the DIMOB dataset is illustrated in Figure 2 and tabulated in Table S6 together with the other datasets. This SUPERFAMILY analysis, like the COG-based analysis, indicates that the vast majority of microbes examined have more novel genes in GIs. The SUPERFAMILY analysis, however, may be considered to be more rigorous and subject to less sampling bias in the Tree of Life than the COG-based analysis, because it can detect more distantly related homologs. Notably, the proportion of novel genes outside of islands according to the SUPERFAMILY analysis is remarkably consistent regardless of the lineages of the organisms. Any variability in novel gene content between organisms does appear to primarily occur in GI regions.


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 SUPERFAMILY-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 higher proportions of genes in islands (red bars) versus outside islands (non-islands; purple bars) do not have a SUPERFAMILY prediction (potential novel genes; p = 4.43E-14).
© Copyright Policy
Related In: Results  -  Collection

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

pgen-0010062-g002: Proportion of Novel Genes in Genomic Islands (Red Bars) versus the Rest of the Genome (Blue Bars) according to a SUPERFAMILY-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 higher proportions of genes in islands (red bars) versus outside islands (non-islands; purple bars) do not have a SUPERFAMILY prediction (potential novel genes; p = 4.43E-14).
Mentions: COG analysis is suitable for detecting orthologous genes but may fail to identify more “distant” homologs that have complex evolution histories (e.g., multiple duplications and deletions among lineages). To complement the COG-based analysis of novel genes in GIs, we adapted another independent method to detect novel hypothetical proteins called SUPERFAMILY analysis [39]. We chose this method because of its reported accuracy and its ability to detect more remote homologs based on structurally conserved similarities [40]. Genes that cannot be assigned to a SUPERFAMILY do not have detectable structural domain homologs in the SCOP database, and therefore are more likely to be novel genes. In both the DINUC and DIMOB datasets, we observed that the proportion of such novel genes is significantly higher in islands compared with outside of islands (see Table 3 for a list of p-values from paired t tests). Pair-wise comparison for the DIMOB dataset is illustrated in Figure 2 and tabulated in Table S6 together with the other datasets. This SUPERFAMILY analysis, like the COG-based analysis, indicates that the vast majority of microbes examined have more novel genes in GIs. The SUPERFAMILY analysis, however, may be considered to be more rigorous and subject to less sampling bias in the Tree of Life than the COG-based analysis, because it can detect more distantly related homologs. Notably, the proportion of novel genes outside of islands according to the SUPERFAMILY analysis is remarkably consistent regardless of the lineages of the organisms. Any variability in novel gene content between organisms does appear to primarily occur in GI regions.

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