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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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Linear alignment of the S. tropica and S. arenicola genomes starting with the origins of replication. (a) Positional orthologs (core) flanked by islands (E, F), heat-mapped HGT genes (D, G), rearranged orthologs (C, H), species-specific genes (B, I), secondary metabolite genes (green), MGEs (pink) with prophage (P) and AICES (E) indicated (A, J). For genomic islands, predicted (lower case) and isolated (uppercase with structures) secondary metabolites are given (not shown are six non-island secondary metabolic gene clusters of unknown function). Shared positional (blue) and rearranged (red) secondary metabolite clusters are indicated. *Previously isolated from other bacteria. (b) Expanded view of SA pks5 revealing gene and modular architecture. (c) Neighbor-joining phylogenetic tree of KS domains from SA pks5 revealing gene and modular duplication events (erythromycin root, % bootstrap values from 1000 re-samplings).
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Figure 1: Linear alignment of the S. tropica and S. arenicola genomes starting with the origins of replication. (a) Positional orthologs (core) flanked by islands (E, F), heat-mapped HGT genes (D, G), rearranged orthologs (C, H), species-specific genes (B, I), secondary metabolite genes (green), MGEs (pink) with prophage (P) and AICES (E) indicated (A, J). For genomic islands, predicted (lower case) and isolated (uppercase with structures) secondary metabolites are given (not shown are six non-island secondary metabolic gene clusters of unknown function). Shared positional (blue) and rearranged (red) secondary metabolite clusters are indicated. *Previously isolated from other bacteria. (b) Expanded view of SA pks5 revealing gene and modular architecture. (c) Neighbor-joining phylogenetic tree of KS domains from SA pks5 revealing gene and modular duplication events (erythromycin root, % bootstrap values from 1000 re-samplings).

Mentions: All genes were assessed for evidence of HGT based on abnormal DNA composition, phylogenetic, taxonomic, and sequence-based relationships, and comparisons to known Mobile Genetic Elements (MGEs). Genes identified by ≥2 different methodologies were counted as positive for HGT. To reflect confidence in the assignments, genes displaying positive evidence of HGT were color coded from yellow to red corresponding to total scores from 2 to 6. The results were mapped onto the genome to reveal HGT clustering patterns and adjacent clusters were merged (Figure 1a). Four DNA compositional analyses included G+C content (obtained from the JGI annotation), codon adaptive index, calculated with the CAI calculator (Wu et al 2005) using a suite of housekeeping genes as reference, dinucleotide frequency differences (δ*), calculated using IslandPath (Hsiao et al 2003), and DNA composition, calculated using Alien_Hunter (Vernikos and Parkhill 2006). G+C content or codon usage values >1.5 standard deviations from the genomic mean and dinucleotide frequency differences >1 standard deviation from the mean were scored positive for HGT. Taxonomic relationships in the form of lineage probability index (LPI) values for all protein coding genes were assigned using the Darkhorse algorithm (Podell and Gaasterland 2007). Genes with an LPI of <0.5, indicating the orthologs are not in closely related genomes, were scored positive for HGT. A reciprocal Darkhorse analysis (Podell et al 2008) was then performed on the orthologs of all positives, and if these genes had an LPI score >0.5, indicating the match sequence is phylogenetically typical within its own lineage, they were assigned an additional positive score.


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)

Linear alignment of the S. tropica and S. arenicola genomes starting with the origins of replication. (a) Positional orthologs (core) flanked by islands (E, F), heat-mapped HGT genes (D, G), rearranged orthologs (C, H), species-specific genes (B, I), secondary metabolite genes (green), MGEs (pink) with prophage (P) and AICES (E) indicated (A, J). For genomic islands, predicted (lower case) and isolated (uppercase with structures) secondary metabolites are given (not shown are six non-island secondary metabolic gene clusters of unknown function). Shared positional (blue) and rearranged (red) secondary metabolite clusters are indicated. *Previously isolated from other bacteria. (b) Expanded view of SA pks5 revealing gene and modular architecture. (c) Neighbor-joining phylogenetic tree of KS domains from SA pks5 revealing gene and modular duplication events (erythromycin root, % bootstrap values from 1000 re-samplings).
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Related In: Results  -  Collection

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getmorefigures.php?uid=PMC2749086&req=5

Figure 1: Linear alignment of the S. tropica and S. arenicola genomes starting with the origins of replication. (a) Positional orthologs (core) flanked by islands (E, F), heat-mapped HGT genes (D, G), rearranged orthologs (C, H), species-specific genes (B, I), secondary metabolite genes (green), MGEs (pink) with prophage (P) and AICES (E) indicated (A, J). For genomic islands, predicted (lower case) and isolated (uppercase with structures) secondary metabolites are given (not shown are six non-island secondary metabolic gene clusters of unknown function). Shared positional (blue) and rearranged (red) secondary metabolite clusters are indicated. *Previously isolated from other bacteria. (b) Expanded view of SA pks5 revealing gene and modular architecture. (c) Neighbor-joining phylogenetic tree of KS domains from SA pks5 revealing gene and modular duplication events (erythromycin root, % bootstrap values from 1000 re-samplings).
Mentions: All genes were assessed for evidence of HGT based on abnormal DNA composition, phylogenetic, taxonomic, and sequence-based relationships, and comparisons to known Mobile Genetic Elements (MGEs). Genes identified by ≥2 different methodologies were counted as positive for HGT. To reflect confidence in the assignments, genes displaying positive evidence of HGT were color coded from yellow to red corresponding to total scores from 2 to 6. The results were mapped onto the genome to reveal HGT clustering patterns and adjacent clusters were merged (Figure 1a). Four DNA compositional analyses included G+C content (obtained from the JGI annotation), codon adaptive index, calculated with the CAI calculator (Wu et al 2005) using a suite of housekeeping genes as reference, dinucleotide frequency differences (δ*), calculated using IslandPath (Hsiao et al 2003), and DNA composition, calculated using Alien_Hunter (Vernikos and Parkhill 2006). G+C content or codon usage values >1.5 standard deviations from the genomic mean and dinucleotide frequency differences >1 standard deviation from the mean were scored positive for HGT. Taxonomic relationships in the form of lineage probability index (LPI) values for all protein coding genes were assigned using the Darkhorse algorithm (Podell and Gaasterland 2007). Genes with an LPI of <0.5, indicating the orthologs are not in closely related genomes, were scored positive for HGT. A reciprocal Darkhorse analysis (Podell et al 2008) was then performed on the orthologs of all positives, and if these genes had an LPI score >0.5, indicating the match sequence is phylogenetically typical within its own lineage, they were assigned an additional positive score.

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