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Genomic islands link secondary metabolism to functional adaptation in marine Actinobacteria.

Penn K, Jenkins C, Nett M, Udwary DW, Gontang EA, McGlinchey RP, Foster B, Lapidus A, Podell S, Allen EE, Moore BS, Jensen PR - ISME J (2009)

Bottom Line: These islands are enriched in genes associated with secondary metabolite biosynthesis providing evidence that secondary metabolism is linked to functional adaptation.Genome evolution is dominated by gene duplication and acquisition, which in the case of secondary metabolism provide immediate opportunities for the production of new bioactive products.Evidence that secondary metabolic pathways are exchanged horizontally, coupled with earlier evidence for fixation among globally distributed populations, supports a functional role and suggests that the acquisition of natural product biosynthetic gene clusters represents a previously unrecognized force driving bacterial diversification.

View Article: PubMed Central - PubMed

Affiliation: Center for Marine Biotechnology and Biomedicine, Scripps Institution of Oceanography, University of California San Diego, La Jolla, CA 92093, USA.

ABSTRACT
Genomic islands have been shown to harbor functional traits that differentiate ecologically distinct populations of environmental bacteria. A comparative analysis of the complete genome sequences of the marine Actinobacteria Salinispora tropica and Salinispora arenicola reveals that 75% of the species-specific genes are located in 21 genomic islands. These islands are enriched in genes associated with secondary metabolite biosynthesis providing evidence that secondary metabolism is linked to functional adaptation. Secondary metabolism accounts for 8.8% and 10.9% of the genes in the S. tropica and S. arenicola genomes, respectively, and represents the major functional category of annotated genes that differentiates the two species. Genomic islands harbor all 25 of the species-specific biosynthetic pathways, the majority of which occur in S. arenicola and may contribute to the cosmopolitan distribution of this species. Genome evolution is dominated by gene duplication and acquisition, which in the case of secondary metabolism provide immediate opportunities for the production of new bioactive products. Evidence that secondary metabolic pathways are exchanged horizontally, coupled with earlier evidence for fixation among globally distributed populations, supports a functional role and suggests that the acquisition of natural product biosynthetic gene clusters represents a previously unrecognized force driving bacterial diversification. Species-specific differences observed in clustered regularly interspaced short palindromic repeat sequences suggest that S. arenicola may possess a higher level of phage immunity, whereas a highly duplicated family of polymorphic membrane proteins provides evidence for a new mechanism of marine adaptation in Gram-positive bacteria.

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Composition, evolutionary history, and function of island genes in S. tropica (ST) and S. arenicola (SA). (a) 3040 genes comprising 21 genomic islands were analyzed for positional orthology (ie., the gene is part of the shared “core” genome), re-arranged orthology (ie., the gene is present in the other genome but not in the same position or island), and species-specificity (gene totals presented in wedges). (b) The ST and SA species-specific island genes were analyzed for evidence of parology, xenology, and HGT. Pseudogenes and the number of genes with no evidence for any of these processes were also identified. (c) Functional annotation of the species-specific island genes. (d) Distribution of species-specific island genes that have no evidence for HGT or parology among 27 Actinobacterial genomes.
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Figure 3: Composition, evolutionary history, and function of island genes in S. tropica (ST) and S. arenicola (SA). (a) 3040 genes comprising 21 genomic islands were analyzed for positional orthology (ie., the gene is part of the shared “core” genome), re-arranged orthology (ie., the gene is present in the other genome but not in the same position or island), and species-specificity (gene totals presented in wedges). (b) The ST and SA species-specific island genes were analyzed for evidence of parology, xenology, and HGT. Pseudogenes and the number of genes with no evidence for any of these processes were also identified. (c) Functional annotation of the species-specific island genes. (d) Distribution of species-specific island genes that have no evidence for HGT or parology among 27 Actinobacterial genomes.

Mentions: The 21 genomic islands are not contiguous regions of species-specific DNA but were instead created by a complex process of gene acquisition, loss, duplication, and inactivation (Figure 3). The overall composition, evolutionary history, and function of the island genes are similar in both strains, with duplication and HGT accounting for the majority of genes and secondary metabolism representing the largest functionally annotated category. Remarkably, 42% of the rearranged island orthologs fall within other islands indicating that inter-island movement or “island hopping” is common, thus providing support for the hypothesis that islands undergo continual rearrangement (Coleman et al 2006). There is dramatic, operon-scale evidence of this process in the shared yersiniabactin pathways (ST sid2 and SA sid1), which occur in islands 15 and 10, respectively, and in the unknown dipeptide pathways (ST nrps1 and SA nrps3), which occur in islands 4 and 15, respectively. In both cases, these pathways remain intact yet are located in different islands in the two strains (Figure 1, Table 2, 3). There is also evidence of cluster fragmentation in the 10-membered enediyne gene set SA pks3, which contains the core set of genes associated with calicheamicin biosynthesis (Figure S2) (Ahlert et al 2002), yet is split by the introduction of 145 kb of DNA from three different biosynthetic loci (island 10, Figure 1). The conserved fragments appear to encode the biosynthesis of a calicheamicin anolog, while flanking genes display a high level of gene duplication and rearrangement indicative of active pathway evolution. Cluster fragmentation is also observed in the 9-membered enediyne PKS cluster SA pks1(A-C), which is scattered across the genome in islands 4, 10, and 21 (Figure 1, Table 3).


Genomic islands link secondary metabolism to functional adaptation in marine Actinobacteria.

Penn K, Jenkins C, Nett M, Udwary DW, Gontang EA, McGlinchey RP, Foster B, Lapidus A, Podell S, Allen EE, Moore BS, Jensen PR - ISME J (2009)

Composition, evolutionary history, and function of island genes in S. tropica (ST) and S. arenicola (SA). (a) 3040 genes comprising 21 genomic islands were analyzed for positional orthology (ie., the gene is part of the shared “core” genome), re-arranged orthology (ie., the gene is present in the other genome but not in the same position or island), and species-specificity (gene totals presented in wedges). (b) The ST and SA species-specific island genes were analyzed for evidence of parology, xenology, and HGT. Pseudogenes and the number of genes with no evidence for any of these processes were also identified. (c) Functional annotation of the species-specific island genes. (d) Distribution of species-specific island genes that have no evidence for HGT or parology among 27 Actinobacterial genomes.
© Copyright Policy
Related In: Results  -  Collection

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getmorefigures.php?uid=PMC2749086&req=5

Figure 3: Composition, evolutionary history, and function of island genes in S. tropica (ST) and S. arenicola (SA). (a) 3040 genes comprising 21 genomic islands were analyzed for positional orthology (ie., the gene is part of the shared “core” genome), re-arranged orthology (ie., the gene is present in the other genome but not in the same position or island), and species-specificity (gene totals presented in wedges). (b) The ST and SA species-specific island genes were analyzed for evidence of parology, xenology, and HGT. Pseudogenes and the number of genes with no evidence for any of these processes were also identified. (c) Functional annotation of the species-specific island genes. (d) Distribution of species-specific island genes that have no evidence for HGT or parology among 27 Actinobacterial genomes.
Mentions: The 21 genomic islands are not contiguous regions of species-specific DNA but were instead created by a complex process of gene acquisition, loss, duplication, and inactivation (Figure 3). The overall composition, evolutionary history, and function of the island genes are similar in both strains, with duplication and HGT accounting for the majority of genes and secondary metabolism representing the largest functionally annotated category. Remarkably, 42% of the rearranged island orthologs fall within other islands indicating that inter-island movement or “island hopping” is common, thus providing support for the hypothesis that islands undergo continual rearrangement (Coleman et al 2006). There is dramatic, operon-scale evidence of this process in the shared yersiniabactin pathways (ST sid2 and SA sid1), which occur in islands 15 and 10, respectively, and in the unknown dipeptide pathways (ST nrps1 and SA nrps3), which occur in islands 4 and 15, respectively. In both cases, these pathways remain intact yet are located in different islands in the two strains (Figure 1, Table 2, 3). There is also evidence of cluster fragmentation in the 10-membered enediyne gene set SA pks3, which contains the core set of genes associated with calicheamicin biosynthesis (Figure S2) (Ahlert et al 2002), yet is split by the introduction of 145 kb of DNA from three different biosynthetic loci (island 10, Figure 1). The conserved fragments appear to encode the biosynthesis of a calicheamicin anolog, while flanking genes display a high level of gene duplication and rearrangement indicative of active pathway evolution. Cluster fragmentation is also observed in the 9-membered enediyne PKS cluster SA pks1(A-C), which is scattered across the genome in islands 4, 10, and 21 (Figure 1, Table 3).

Bottom Line: These islands are enriched in genes associated with secondary metabolite biosynthesis providing evidence that secondary metabolism is linked to functional adaptation.Genome evolution is dominated by gene duplication and acquisition, which in the case of secondary metabolism provide immediate opportunities for the production of new bioactive products.Evidence that secondary metabolic pathways are exchanged horizontally, coupled with earlier evidence for fixation among globally distributed populations, supports a functional role and suggests that the acquisition of natural product biosynthetic gene clusters represents a previously unrecognized force driving bacterial diversification.

View Article: PubMed Central - PubMed

Affiliation: Center for Marine Biotechnology and Biomedicine, Scripps Institution of Oceanography, University of California San Diego, La Jolla, CA 92093, USA.

ABSTRACT
Genomic islands have been shown to harbor functional traits that differentiate ecologically distinct populations of environmental bacteria. A comparative analysis of the complete genome sequences of the marine Actinobacteria Salinispora tropica and Salinispora arenicola reveals that 75% of the species-specific genes are located in 21 genomic islands. These islands are enriched in genes associated with secondary metabolite biosynthesis providing evidence that secondary metabolism is linked to functional adaptation. Secondary metabolism accounts for 8.8% and 10.9% of the genes in the S. tropica and S. arenicola genomes, respectively, and represents the major functional category of annotated genes that differentiates the two species. Genomic islands harbor all 25 of the species-specific biosynthetic pathways, the majority of which occur in S. arenicola and may contribute to the cosmopolitan distribution of this species. Genome evolution is dominated by gene duplication and acquisition, which in the case of secondary metabolism provide immediate opportunities for the production of new bioactive products. Evidence that secondary metabolic pathways are exchanged horizontally, coupled with earlier evidence for fixation among globally distributed populations, supports a functional role and suggests that the acquisition of natural product biosynthetic gene clusters represents a previously unrecognized force driving bacterial diversification. Species-specific differences observed in clustered regularly interspaced short palindromic repeat sequences suggest that S. arenicola may possess a higher level of phage immunity, whereas a highly duplicated family of polymorphic membrane proteins provides evidence for a new mechanism of marine adaptation in Gram-positive bacteria.

Show MeSH