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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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S. tropica prophage and S. arenicola CRISPRs. Four of 8 SA CRISPRs (1, 5, 7, 8) have spacers (color coded) that share 100% sequence identity with genes (Stro numbers and annotation given) in ST prophage 1 (Table S2, inverted for visual purposes). Other CRISPRs are colored purple. SA CRISPRs 2-3 and 5-6 share the same direct repeats and may have at one time been a single allele. CRISPR associated (CAS) genes (red) and genes interrupting CRISPRs (black) are indicated. None of the spacer sequences possessed 100% identity to prophage in the NCBI non-redundant sequence database, the SDSU Center for Universal Microbial Sequencing database, or the CAMERA metagenomic database.
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Figure 2: S. tropica prophage and S. arenicola CRISPRs. Four of 8 SA CRISPRs (1, 5, 7, 8) have spacers (color coded) that share 100% sequence identity with genes (Stro numbers and annotation given) in ST prophage 1 (Table S2, inverted for visual purposes). Other CRISPRs are colored purple. SA CRISPRs 2-3 and 5-6 share the same direct repeats and may have at one time been a single allele. CRISPR associated (CAS) genes (red) and genes interrupting CRISPRs (black) are indicated. None of the spacer sequences possessed 100% identity to prophage in the NCBI non-redundant sequence database, the SDSU Center for Universal Microbial Sequencing database, or the CAMERA metagenomic database.

Mentions: Differences between the two species also occur in CRISPR sequences, which are non-continuous direct repeats separated by variable (spacer) sequences that have been shown to confer immunity to phage (Barrangou et al 2007). The ST genome carries three intact prophage and three CRISPRs (35 spacers), while only one prophage has been identified in the genome of SA, which possesses eight different CRISPRs (140 spacers). The SA prophage is unprecedented among bacterial genomes in that it occurs in two adjacent copies that share 100% sequence identity. These copies are flanked by tRNA att sites and separated by an identical 45 bp att site, suggesting double integration as opposed to duplication (te Poele et al 2008). Remarkably, four of the SA CRISPRs possess a spacer that shares 100% identity with portions of three different genes found in ST prophage 1 (Figure 2). These spacer sequences have no similar matches to genes in the SA prophage or in any prophage sequences deposited in the NCBI, CAMERA, or the SDSU Center for Universal Microbial Sequencing databases. The detection of these spacer sequences provides evidence that SA has been exposed to a phage related to one that currently infects ST and that SA now maintains acquired immunity to this phage genotype as has been previously reported in other bacteria (Barrangou et al 2007). This is a rare example in which evidence has been obtained for CRISPR-mediated acquired immunity to a prophage that resides in the genome of a closely related environmental bacterium. Given that SA strain CNS-205 was isolated from Palau while ST strain CNB-440 was recovered 15 years earlier from the Bahamas, it appears that actinophage have broad temporal-spatial distributions or that resistance is maintained on temporal scales sufficient for the global distribution of a bacterial species.


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)

S. tropica prophage and S. arenicola CRISPRs. Four of 8 SA CRISPRs (1, 5, 7, 8) have spacers (color coded) that share 100% sequence identity with genes (Stro numbers and annotation given) in ST prophage 1 (Table S2, inverted for visual purposes). Other CRISPRs are colored purple. SA CRISPRs 2-3 and 5-6 share the same direct repeats and may have at one time been a single allele. CRISPR associated (CAS) genes (red) and genes interrupting CRISPRs (black) are indicated. None of the spacer sequences possessed 100% identity to prophage in the NCBI non-redundant sequence database, the SDSU Center for Universal Microbial Sequencing database, or the CAMERA metagenomic database.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2749086&req=5

Figure 2: S. tropica prophage and S. arenicola CRISPRs. Four of 8 SA CRISPRs (1, 5, 7, 8) have spacers (color coded) that share 100% sequence identity with genes (Stro numbers and annotation given) in ST prophage 1 (Table S2, inverted for visual purposes). Other CRISPRs are colored purple. SA CRISPRs 2-3 and 5-6 share the same direct repeats and may have at one time been a single allele. CRISPR associated (CAS) genes (red) and genes interrupting CRISPRs (black) are indicated. None of the spacer sequences possessed 100% identity to prophage in the NCBI non-redundant sequence database, the SDSU Center for Universal Microbial Sequencing database, or the CAMERA metagenomic database.
Mentions: Differences between the two species also occur in CRISPR sequences, which are non-continuous direct repeats separated by variable (spacer) sequences that have been shown to confer immunity to phage (Barrangou et al 2007). The ST genome carries three intact prophage and three CRISPRs (35 spacers), while only one prophage has been identified in the genome of SA, which possesses eight different CRISPRs (140 spacers). The SA prophage is unprecedented among bacterial genomes in that it occurs in two adjacent copies that share 100% sequence identity. These copies are flanked by tRNA att sites and separated by an identical 45 bp att site, suggesting double integration as opposed to duplication (te Poele et al 2008). Remarkably, four of the SA CRISPRs possess a spacer that shares 100% identity with portions of three different genes found in ST prophage 1 (Figure 2). These spacer sequences have no similar matches to genes in the SA prophage or in any prophage sequences deposited in the NCBI, CAMERA, or the SDSU Center for Universal Microbial Sequencing databases. The detection of these spacer sequences provides evidence that SA has been exposed to a phage related to one that currently infects ST and that SA now maintains acquired immunity to this phage genotype as has been previously reported in other bacteria (Barrangou et al 2007). This is a rare example in which evidence has been obtained for CRISPR-mediated acquired immunity to a prophage that resides in the genome of a closely related environmental bacterium. Given that SA strain CNS-205 was isolated from Palau while ST strain CNB-440 was recovered 15 years earlier from the Bahamas, it appears that actinophage have broad temporal-spatial distributions or that resistance is maintained on temporal scales sufficient for the global distribution of a bacterial species.

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
Related in: MedlinePlus