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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

Type II CRISPR regions.Homologous regions from Syn OS-A and Syn OS-B′ where one or both genomes has a Type II CRISPR locus are displayed. The CRISPR displayed is indicated by the panel letter (e.g. panel ‘A’ shows CRISPR-IIA, panel ‘B’ shows CRISPR-IIB, etc.) Figure conventions are as described in Figure 2. FS indicates a frameshift in the CDS. Additional details can be found in Table S3.
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pone-0004169-g003: Type II CRISPR regions.Homologous regions from Syn OS-A and Syn OS-B′ where one or both genomes has a Type II CRISPR locus are displayed. The CRISPR displayed is indicated by the panel letter (e.g. panel ‘A’ shows CRISPR-IIA, panel ‘B’ shows CRISPR-IIB, etc.) Figure conventions are as described in Figure 2. FS indicates a frameshift in the CDS. Additional details can be found in Table S3.

Mentions: The Type II CRISPR repeat is 36 bp (Table 1 and S1). Type II CRISPR arrays are found at five locations on the Syn OS-A genome (IIA-E) and at four locations on the Syn OS-B′ genome (IIA, IID, IIF and IIG) (Figure 1). One CRISPR array on each genome (IIA) is associated with the cas genes while the others are not. The Syn OS-A CRISPR-IIA has 12 repeats associated with the cas genes (2,557,478–2,559,455 bp). The other locations of the Type II CRISPRs on the Syn OS-A genome include 7 repeats at 1,260,139–1,260,640 (IIB), two repeats at 1,860,020–1,860,135 (IIC), two repeats at 1,960,214–1,960,325 (IID), and 17 repeats at 2,327,972–2,329,201 (IIE). Syn OS-B′ CRISPR-IIA has 16 repeats associated with the cas genes (866,037–867,185 bp). The other locations of the CRISPR-II on Syn OS-B′ include 35 repeats spanning 156,596–159,176 bp (IID), 18 repeats spanning 515,271–516,592 (IIF), and 31 repeats spanning 2,016,367–2,018,657 (IIG) (Table 1 and Figure 3).


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)

Type II CRISPR regions.Homologous regions from Syn OS-A and Syn OS-B′ where one or both genomes has a Type II CRISPR locus are displayed. The CRISPR displayed is indicated by the panel letter (e.g. panel ‘A’ shows CRISPR-IIA, panel ‘B’ shows CRISPR-IIB, etc.) Figure conventions are as described in Figure 2. FS indicates a frameshift in the CDS. Additional details can be found in Table S3.
© Copyright Policy
Related In: Results  -  Collection

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

pone-0004169-g003: Type II CRISPR regions.Homologous regions from Syn OS-A and Syn OS-B′ where one or both genomes has a Type II CRISPR locus are displayed. The CRISPR displayed is indicated by the panel letter (e.g. panel ‘A’ shows CRISPR-IIA, panel ‘B’ shows CRISPR-IIB, etc.) Figure conventions are as described in Figure 2. FS indicates a frameshift in the CDS. Additional details can be found in Table S3.
Mentions: The Type II CRISPR repeat is 36 bp (Table 1 and S1). Type II CRISPR arrays are found at five locations on the Syn OS-A genome (IIA-E) and at four locations on the Syn OS-B′ genome (IIA, IID, IIF and IIG) (Figure 1). One CRISPR array on each genome (IIA) is associated with the cas genes while the others are not. The Syn OS-A CRISPR-IIA has 12 repeats associated with the cas genes (2,557,478–2,559,455 bp). The other locations of the Type II CRISPRs on the Syn OS-A genome include 7 repeats at 1,260,139–1,260,640 (IIB), two repeats at 1,860,020–1,860,135 (IIC), two repeats at 1,960,214–1,960,325 (IID), and 17 repeats at 2,327,972–2,329,201 (IIE). Syn OS-B′ CRISPR-IIA has 16 repeats associated with the cas genes (866,037–867,185 bp). The other locations of the CRISPR-II on Syn OS-B′ include 35 repeats spanning 156,596–159,176 bp (IID), 18 repeats spanning 515,271–516,592 (IIF), and 31 repeats spanning 2,016,367–2,018,657 (IIG) (Table 1 and Figure 3).

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