Processing-Independent CRISPR RNAs Limit Natural Transformation in Neisseria meningitidis

Yan Zhang; Nadja Heidrich; Biju Joseph Ampattu; Carl W. Gunderson; H. Steven Seifert; Christoph Schoen; Jörg Vogel; Erik J. Sontheimer

doi:10.1016/j.molcel.2013.05.001

Processing-Independent CRISPR RNAs Limit Natural Transformation in Neisseria meningitidis

Yan Zhang, Nadja Heidrich, Biju Joseph Ampattu, Carl W. Gunderson, H. Steven Seifert, Christoph Schoen, Jörg Vogel^*, Erik J. Sontheimer

^*Corresponding author for this work

Microbiology-Immunology

Research output: Contribution to journal › Article › peer-review

148 Scopus citations

Abstract

CRISPR interference confers adaptive, sequence-based immunity against viruses and plasmids and is specified by CRISPR RNAs (crRNAs) that are transcribed and processed from spacer-repeat units. Pre-crRNA processing is essential for CRISPR interference in all systems studied thus far. Here, our studies of crRNA biogenesis and CRISPR interference in naturally competent Neisseria spp. reveal a unique crRNA maturation pathway in which crRNAs are transcribed from promoters that are embedded within each repeat, yielding crRNA 5' ends formed by transcription and not by processing. Although crRNA 3' end formation involves RNase III and trans-encoded tracrRNA, as in other type II CRISPR systems, this processing is dispensable for interference. The meningococcal pathway is the most streamlined CRISPR/Cas system characterized to date. Endogenous CRISPR spacers limit natural transformation, which is the primary source of genetic variation that contributes to immune evasion, antibiotic resistance, and virulence in the human pathogen N.meningitidis.

Original language	English (US)
Pages (from-to)	488-503
Number of pages	16
Journal	Molecular cell
Volume	50
Issue number	4
DOIs	https://doi.org/10.1016/j.molcel.2013.05.001
State	Published - May 23 2013

ASJC Scopus subject areas

Molecular Biology
Cell Biology

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10.1016/j.molcel.2013.05.001

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title = "Processing-Independent CRISPR RNAs Limit Natural Transformation in Neisseria meningitidis",

abstract = "CRISPR interference confers adaptive, sequence-based immunity against viruses and plasmids and is specified by CRISPR RNAs (crRNAs) that are transcribed and processed from spacer-repeat units. Pre-crRNA processing is essential for CRISPR interference in all systems studied thus far. Here, our studies of crRNA biogenesis and CRISPR interference in naturally competent Neisseria spp. reveal a unique crRNA maturation pathway in which crRNAs are transcribed from promoters that are embedded within each repeat, yielding crRNA 5' ends formed by transcription and not by processing. Although crRNA 3' end formation involves RNase III and trans-encoded tracrRNA, as in other type II CRISPR systems, this processing is dispensable for interference. The meningococcal pathway is the most streamlined CRISPR/Cas system characterized to date. Endogenous CRISPR spacers limit natural transformation, which is the primary source of genetic variation that contributes to immune evasion, antibiotic resistance, and virulence in the human pathogen N.meningitidis.",

author = "Yan Zhang and Nadja Heidrich and Ampattu, {Biju Joseph} and Gunderson, {Carl W.} and Seifert, {H. Steven} and Christoph Schoen and J{\"o}rg Vogel and Sontheimer, {Erik J.}",

note = "Funding Information: We thank V. Pelicic for genomic DNAs from meningococcal transposon insertion strains; Y. Chao, G. Dugar, and C.M. Sharma for discussions; and R. Reinhardt and K. F{\"o}rstner for dRNA-seq and data mapping, respectively. This work was supported by DFG grants (875/4-2 and 875/7-1) to J.V., and by National Institutes of Health grants R37 AI033493 and R01 AI044239 to H.S.S. and R01 GM093769 to E.J.S. ",

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AU - Schoen, Christoph

AU - Vogel, Jörg

AU - Sontheimer, Erik J.

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PY - 2013/5/23

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N2 - CRISPR interference confers adaptive, sequence-based immunity against viruses and plasmids and is specified by CRISPR RNAs (crRNAs) that are transcribed and processed from spacer-repeat units. Pre-crRNA processing is essential for CRISPR interference in all systems studied thus far. Here, our studies of crRNA biogenesis and CRISPR interference in naturally competent Neisseria spp. reveal a unique crRNA maturation pathway in which crRNAs are transcribed from promoters that are embedded within each repeat, yielding crRNA 5' ends formed by transcription and not by processing. Although crRNA 3' end formation involves RNase III and trans-encoded tracrRNA, as in other type II CRISPR systems, this processing is dispensable for interference. The meningococcal pathway is the most streamlined CRISPR/Cas system characterized to date. Endogenous CRISPR spacers limit natural transformation, which is the primary source of genetic variation that contributes to immune evasion, antibiotic resistance, and virulence in the human pathogen N.meningitidis.

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Processing-Independent CRISPR RNAs Limit Natural Transformation in Neisseria meningitidis

Abstract

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