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CRISPR-Cas Adaptive Immune Systems of the Sulfolobales: Unravelling Their Complexity and Diversity.

Garrett RA, Shah SA, Erdmann S, Liu G, Mousaei M, León-Sobrino C, Peng W, Gudbergsdottir S, Deng L, Vestergaard G, Peng X, She Q - Life (Basel) (2015)

Bottom Line: Recent work also supports critical roles for non-core Cas proteins, especially during Type III-directed interference, and this is consistent with these proteins tending to coevolve with core Cas proteins.Various novel aspects of CRISPR-Cas systems of the Sulfolobales are considered including an alternative spacer acquisition mechanism, reversible spacer acquisition, the formation and significance of antisense CRISPR RNAs, and a novel mechanism for avoidance of CRISPR-Cas defense.Finally, questions regarding the basis for the complexity, diversity, and apparent redundancy, of the intracellular CRISPR-Cas systems are discussed.

View Article: PubMed Central - PubMed

Affiliation: Archaea Centre, Department of Biology, Copenhagen University, Ole Maaløes Vej 5, DK2200 Copenhagen N, Denmark. garrett@bio.ku.dk.

ABSTRACT
The Sulfolobales have provided good model organisms for studying CRISPR-Cas systems of the crenarchaeal kingdom of the archaea. These organisms are infected by a wide range of exceptional archaea-specific viruses and conjugative plasmids, and their CRISPR-Cas systems generally exhibit extensive structural and functional diversity. They carry large and multiple CRISPR loci and often multiple copies of diverse Type I and Type III interference modules as well as more homogeneous adaptation modules. These acidothermophilic organisms have recently provided seminal insights into both the adaptation process, the diverse modes of interference, and their modes of regulation. The functions of the adaptation and interference modules tend to be loosely coupled and the stringency of the crRNA-DNA sequence matching during DNA interference is relatively low, in contrast to some more streamlined CRISPR-Cas systems of bacteria. Despite this, there is evidence for a complex and differential regulation of expression of the diverse functional modules in response to viral infection. Recent work also supports critical roles for non-core Cas proteins, especially during Type III-directed interference, and this is consistent with these proteins tending to coevolve with core Cas proteins. Various novel aspects of CRISPR-Cas systems of the Sulfolobales are considered including an alternative spacer acquisition mechanism, reversible spacer acquisition, the formation and significance of antisense CRISPR RNAs, and a novel mechanism for avoidance of CRISPR-Cas defense. Finally, questions regarding the basis for the complexity, diversity, and apparent redundancy, of the intracellular CRISPR-Cas systems are discussed.

No MeSH data available.


Related in: MedlinePlus

Dendrograms of archaeal CRISPR-Cas interference gene cassettes. (A) Type I and (B) Type III, where gene identities, sizes and syntenies are shown for representatives of the different subtypes. Total numbers of identified subtypes are indicated on the right for Sulfolobales (S) and all archaea (A). Standard csm/cmr gene names are given for subtypes III-A and III-B. Different subtypes have distinct gene syntenies and branch before the defined threshold indicated by the light blue vertical line defined earlier [36]. Subtypes III-C and III-D correspond to the earlier defined families A and D [42] while variant subtype VIII-1 is only found in some members of the Sulfolobales [36]. All Type III gene cassettes carry cas10, the gene for protein S, cas5, and multiple cas7 paralogues. asp denotes the putative aspartate protease gene. The subtype I-D gene cassette branches at the junction of the Type I and Type III subtypes (based on data in [36]).
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life-05-00783-f001: Dendrograms of archaeal CRISPR-Cas interference gene cassettes. (A) Type I and (B) Type III, where gene identities, sizes and syntenies are shown for representatives of the different subtypes. Total numbers of identified subtypes are indicated on the right for Sulfolobales (S) and all archaea (A). Standard csm/cmr gene names are given for subtypes III-A and III-B. Different subtypes have distinct gene syntenies and branch before the defined threshold indicated by the light blue vertical line defined earlier [36]. Subtypes III-C and III-D correspond to the earlier defined families A and D [42] while variant subtype VIII-1 is only found in some members of the Sulfolobales [36]. All Type III gene cassettes carry cas10, the gene for protein S, cas5, and multiple cas7 paralogues. asp denotes the putative aspartate protease gene. The subtype I-D gene cassette branches at the junction of the Type I and Type III subtypes (based on data in [36]).

Mentions: For Type I systems, reevaluation of archaeal subtype classifications based on interference complexes, led to the proposal to divide subtype I-B into subtypes I-B and I-G, which are similar to the earlier proposed groupings Hmar and Tneap, respectively (Figure 1A) [41]. Moreover, previously, we had proposed dividing archaeal Type III systems into five families A to E [42]. Later family E became Type III-A and families B and C became Type III-B and, to conform with this widely used nomenclature, families A and D became subtypes III-C and III-D, respectively (Figure 1B) [36]. The most common archaeal Type I subtypes are I-A, I-B and I-D and I-G while subtypes I-C and I-E occur rarely and subtype I-F has not been detected [36]. For the archaeal Type III systems, subtypes III-A and III-B dominate and III-C and III-D are less common. In addition, numerous variant subtypes have been identified some of which are phyla specific and their number may increase as more genomes are sequenced. Among the Sulfolobales, subtypes I-A, I-D, III-B and III-D dominate together with a single Type III variant VIII-I that is exclusive to the Sulfolobales [36] (Figure 1).


CRISPR-Cas Adaptive Immune Systems of the Sulfolobales: Unravelling Their Complexity and Diversity.

Garrett RA, Shah SA, Erdmann S, Liu G, Mousaei M, León-Sobrino C, Peng W, Gudbergsdottir S, Deng L, Vestergaard G, Peng X, She Q - Life (Basel) (2015)

Dendrograms of archaeal CRISPR-Cas interference gene cassettes. (A) Type I and (B) Type III, where gene identities, sizes and syntenies are shown for representatives of the different subtypes. Total numbers of identified subtypes are indicated on the right for Sulfolobales (S) and all archaea (A). Standard csm/cmr gene names are given for subtypes III-A and III-B. Different subtypes have distinct gene syntenies and branch before the defined threshold indicated by the light blue vertical line defined earlier [36]. Subtypes III-C and III-D correspond to the earlier defined families A and D [42] while variant subtype VIII-1 is only found in some members of the Sulfolobales [36]. All Type III gene cassettes carry cas10, the gene for protein S, cas5, and multiple cas7 paralogues. asp denotes the putative aspartate protease gene. The subtype I-D gene cassette branches at the junction of the Type I and Type III subtypes (based on data in [36]).
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4390879&req=5

life-05-00783-f001: Dendrograms of archaeal CRISPR-Cas interference gene cassettes. (A) Type I and (B) Type III, where gene identities, sizes and syntenies are shown for representatives of the different subtypes. Total numbers of identified subtypes are indicated on the right for Sulfolobales (S) and all archaea (A). Standard csm/cmr gene names are given for subtypes III-A and III-B. Different subtypes have distinct gene syntenies and branch before the defined threshold indicated by the light blue vertical line defined earlier [36]. Subtypes III-C and III-D correspond to the earlier defined families A and D [42] while variant subtype VIII-1 is only found in some members of the Sulfolobales [36]. All Type III gene cassettes carry cas10, the gene for protein S, cas5, and multiple cas7 paralogues. asp denotes the putative aspartate protease gene. The subtype I-D gene cassette branches at the junction of the Type I and Type III subtypes (based on data in [36]).
Mentions: For Type I systems, reevaluation of archaeal subtype classifications based on interference complexes, led to the proposal to divide subtype I-B into subtypes I-B and I-G, which are similar to the earlier proposed groupings Hmar and Tneap, respectively (Figure 1A) [41]. Moreover, previously, we had proposed dividing archaeal Type III systems into five families A to E [42]. Later family E became Type III-A and families B and C became Type III-B and, to conform with this widely used nomenclature, families A and D became subtypes III-C and III-D, respectively (Figure 1B) [36]. The most common archaeal Type I subtypes are I-A, I-B and I-D and I-G while subtypes I-C and I-E occur rarely and subtype I-F has not been detected [36]. For the archaeal Type III systems, subtypes III-A and III-B dominate and III-C and III-D are less common. In addition, numerous variant subtypes have been identified some of which are phyla specific and their number may increase as more genomes are sequenced. Among the Sulfolobales, subtypes I-A, I-D, III-B and III-D dominate together with a single Type III variant VIII-I that is exclusive to the Sulfolobales [36] (Figure 1).

Bottom Line: Recent work also supports critical roles for non-core Cas proteins, especially during Type III-directed interference, and this is consistent with these proteins tending to coevolve with core Cas proteins.Various novel aspects of CRISPR-Cas systems of the Sulfolobales are considered including an alternative spacer acquisition mechanism, reversible spacer acquisition, the formation and significance of antisense CRISPR RNAs, and a novel mechanism for avoidance of CRISPR-Cas defense.Finally, questions regarding the basis for the complexity, diversity, and apparent redundancy, of the intracellular CRISPR-Cas systems are discussed.

View Article: PubMed Central - PubMed

Affiliation: Archaea Centre, Department of Biology, Copenhagen University, Ole Maaløes Vej 5, DK2200 Copenhagen N, Denmark. garrett@bio.ku.dk.

ABSTRACT
The Sulfolobales have provided good model organisms for studying CRISPR-Cas systems of the crenarchaeal kingdom of the archaea. These organisms are infected by a wide range of exceptional archaea-specific viruses and conjugative plasmids, and their CRISPR-Cas systems generally exhibit extensive structural and functional diversity. They carry large and multiple CRISPR loci and often multiple copies of diverse Type I and Type III interference modules as well as more homogeneous adaptation modules. These acidothermophilic organisms have recently provided seminal insights into both the adaptation process, the diverse modes of interference, and their modes of regulation. The functions of the adaptation and interference modules tend to be loosely coupled and the stringency of the crRNA-DNA sequence matching during DNA interference is relatively low, in contrast to some more streamlined CRISPR-Cas systems of bacteria. Despite this, there is evidence for a complex and differential regulation of expression of the diverse functional modules in response to viral infection. Recent work also supports critical roles for non-core Cas proteins, especially during Type III-directed interference, and this is consistent with these proteins tending to coevolve with core Cas proteins. Various novel aspects of CRISPR-Cas systems of the Sulfolobales are considered including an alternative spacer acquisition mechanism, reversible spacer acquisition, the formation and significance of antisense CRISPR RNAs, and a novel mechanism for avoidance of CRISPR-Cas defense. Finally, questions regarding the basis for the complexity, diversity, and apparent redundancy, of the intracellular CRISPR-Cas systems are discussed.

No MeSH data available.


Related in: MedlinePlus