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Germ warfare in a microbial mat community: CRISPRs provide insights into the co-evolution of host and viral genomes.

Heidelberg JF, Nelson WC, Schoenfeld T, Bhaya D - PLoS ONE (2009)

Bottom Line: Two distinct CRISPR types, distinguished by the repeat sequence, are found in both the Syn OS-A and Syn OS-B' genomes.The genome of Syn OS-A contains a third CRISPR type with a distinct repeat sequence, which is not found in Syn OS-B', but appears to be shared with other microorganisms that inhabit the mat.The ability of metagenomics to track population-level variation in viritope sequences allows for a culture-independent method for evaluating the fast co-evolution of host and viral genomes and its consequence on the structuring of complex microbial communities.

View Article: PubMed Central - PubMed

Affiliation: Department of Biological Sciences, Marine Environmental Biology Division, Wrigley Institute for Environmental Studies, University of Southern California, Avalon, California, United States of America.

ABSTRACT
CRISPR arrays and associated cas genes are widespread in bacteria and archaea and confer acquired resistance to viruses. To examine viral immunity in the context of naturally evolving microbial populations we analyzed genomic data from two thermophilic Synechococcus isolates (Syn OS-A and Syn OS-B') as well as a prokaryotic metagenome and viral metagenome derived from microbial mats in hotsprings at Yellowstone National Park. Two distinct CRISPR types, distinguished by the repeat sequence, are found in both the Syn OS-A and Syn OS-B' genomes. The genome of Syn OS-A contains a third CRISPR type with a distinct repeat sequence, which is not found in Syn OS-B', but appears to be shared with other microorganisms that inhabit the mat. The CRISPR repeats identified in the microbial metagenome are highly conserved, while the spacer sequences (hereafter referred to as "viritopes" to emphasize their critical role in viral immunity) were mostly unique and had no high identity matches when searched against GenBank. Searching the viritopes against the viral metagenome, however, yielded several matches with high similarity some of which were within a gene identified as a likely viral lysozyme/lysin protein. Analysis of viral metagenome sequences corresponding to this lysozyme/lysin protein revealed several mutations all of which translate into silent or conservative mutations which are unlikely to affect protein function, but may help the virus evade the host CRISPR resistance mechanism. These results demonstrate the varied challenges presented by a natural virus population, and support the notion that the CRISPR/viritope system must be able to adapt quickly to provide host immunity. The ability of metagenomics to track population-level variation in viritope sequences allows for a culture-independent method for evaluating the fast co-evolution of host and viral genomes and its consequence on the structuring of complex microbial communities.

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Related in: MedlinePlus

Comparison of Type III CRISPR locus to Roseiflexus RS-1 and Symbiobacterium.Homologous regions from Syn OS-A, Syn-OS-B′, Roseiflexus RS-1 and Symbiobacterium are displayed. Gene identifiers are shown above or below each gene, excluding the GenBank locus tag prefix ‘CYA_’ (for Syn OS-A), ‘CYB_’ (for Syn OS-B′), RoseRS_ (for Roseiflexus RS-1) or STH (for Symbiobacterium thermophilum). Additional figure conventions are as described in Figure 2. Details about the genes can be found in Table S3.
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pone-0004169-g004: Comparison of Type III CRISPR locus to Roseiflexus RS-1 and Symbiobacterium.Homologous regions from Syn OS-A, Syn-OS-B′, Roseiflexus RS-1 and Symbiobacterium are displayed. Gene identifiers are shown above or below each gene, excluding the GenBank locus tag prefix ‘CYA_’ (for Syn OS-A), ‘CYB_’ (for Syn OS-B′), RoseRS_ (for Roseiflexus RS-1) or STH (for Symbiobacterium thermophilum). Additional figure conventions are as described in Figure 2. Details about the genes can be found in Table S3.

Mentions: A) CRISPR-IA region from Syn OS-A (top) and Syn OS-B′ (bottom). The cas gene cluster is indicated by a grey bracket. B) CRISPR-IB region. Gene identifiers are shown above or below each gene, excluding the GenBank locus tag prefix ‘CYA_’ (for Syn OS-A) or ‘CYB_’ (for Syn OS-B′). Genes are color-coded following the COG-based IMG convention (http://img.jgi.doe.gov), (described in Figure 4), except that genes annotated as “hypothetical protein” are in grey, genes with no putative ortholog in the other genome are in red, and genes annotated as transposases are in black. Orthologous genes are indicated by yellow blocks. Detailed information on each gene is available in Table S3.


Germ warfare in a microbial mat community: CRISPRs provide insights into the co-evolution of host and viral genomes.

Heidelberg JF, Nelson WC, Schoenfeld T, Bhaya D - PLoS ONE (2009)

Comparison of Type III CRISPR locus to Roseiflexus RS-1 and Symbiobacterium.Homologous regions from Syn OS-A, Syn-OS-B′, Roseiflexus RS-1 and Symbiobacterium are displayed. Gene identifiers are shown above or below each gene, excluding the GenBank locus tag prefix ‘CYA_’ (for Syn OS-A), ‘CYB_’ (for Syn OS-B′), RoseRS_ (for Roseiflexus RS-1) or STH (for Symbiobacterium thermophilum). Additional figure conventions are as described in Figure 2. Details about the genes can be found in Table S3.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2612747&req=5

pone-0004169-g004: Comparison of Type III CRISPR locus to Roseiflexus RS-1 and Symbiobacterium.Homologous regions from Syn OS-A, Syn-OS-B′, Roseiflexus RS-1 and Symbiobacterium are displayed. Gene identifiers are shown above or below each gene, excluding the GenBank locus tag prefix ‘CYA_’ (for Syn OS-A), ‘CYB_’ (for Syn OS-B′), RoseRS_ (for Roseiflexus RS-1) or STH (for Symbiobacterium thermophilum). Additional figure conventions are as described in Figure 2. Details about the genes can be found in Table S3.
Mentions: A) CRISPR-IA region from Syn OS-A (top) and Syn OS-B′ (bottom). The cas gene cluster is indicated by a grey bracket. B) CRISPR-IB region. Gene identifiers are shown above or below each gene, excluding the GenBank locus tag prefix ‘CYA_’ (for Syn OS-A) or ‘CYB_’ (for Syn OS-B′). Genes are color-coded following the COG-based IMG convention (http://img.jgi.doe.gov), (described in Figure 4), except that genes annotated as “hypothetical protein” are in grey, genes with no putative ortholog in the other genome are in red, and genes annotated as transposases are in black. Orthologous genes are indicated by yellow blocks. Detailed information on each gene is available in Table S3.

Bottom Line: Two distinct CRISPR types, distinguished by the repeat sequence, are found in both the Syn OS-A and Syn OS-B' genomes.The genome of Syn OS-A contains a third CRISPR type with a distinct repeat sequence, which is not found in Syn OS-B', but appears to be shared with other microorganisms that inhabit the mat.The ability of metagenomics to track population-level variation in viritope sequences allows for a culture-independent method for evaluating the fast co-evolution of host and viral genomes and its consequence on the structuring of complex microbial communities.

View Article: PubMed Central - PubMed

Affiliation: Department of Biological Sciences, Marine Environmental Biology Division, Wrigley Institute for Environmental Studies, University of Southern California, Avalon, California, United States of America.

ABSTRACT
CRISPR arrays and associated cas genes are widespread in bacteria and archaea and confer acquired resistance to viruses. To examine viral immunity in the context of naturally evolving microbial populations we analyzed genomic data from two thermophilic Synechococcus isolates (Syn OS-A and Syn OS-B') as well as a prokaryotic metagenome and viral metagenome derived from microbial mats in hotsprings at Yellowstone National Park. Two distinct CRISPR types, distinguished by the repeat sequence, are found in both the Syn OS-A and Syn OS-B' genomes. The genome of Syn OS-A contains a third CRISPR type with a distinct repeat sequence, which is not found in Syn OS-B', but appears to be shared with other microorganisms that inhabit the mat. The CRISPR repeats identified in the microbial metagenome are highly conserved, while the spacer sequences (hereafter referred to as "viritopes" to emphasize their critical role in viral immunity) were mostly unique and had no high identity matches when searched against GenBank. Searching the viritopes against the viral metagenome, however, yielded several matches with high similarity some of which were within a gene identified as a likely viral lysozyme/lysin protein. Analysis of viral metagenome sequences corresponding to this lysozyme/lysin protein revealed several mutations all of which translate into silent or conservative mutations which are unlikely to affect protein function, but may help the virus evade the host CRISPR resistance mechanism. These results demonstrate the varied challenges presented by a natural virus population, and support the notion that the CRISPR/viritope system must be able to adapt quickly to provide host immunity. The ability of metagenomics to track population-level variation in viritope sequences allows for a culture-independent method for evaluating the fast co-evolution of host and viral genomes and its consequence on the structuring of complex microbial communities.

Show MeSH
Related in: MedlinePlus