The CRISPR/Cas Immune System Is an Operon Regulated by LeuO, H-NS, and Leucine-Responsive Regulatory Protein in Salmonella enterica Serovar Typhi

Medina-Aparicio, Liliana; Rebollar-Flores, Javier E; Gallego-Hernández, Ana L.; Vázquez, Arturo Pérez; Olvera, Leticia; Gutiérrez-Rı́os, Rosa Marı́a; Calva, Edmundo; Hernández-Lucas, Ismael

doi:10.1128/jb.01480-10

Cited by 101 publications

(106 citation statements)

References 66 publications

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“…As the genome does not carry PAM sequences, it is not regarded as a threat and therefore is not targeted. Remarkably, the expression of CRISPR-Cas systems can be regulated by some cellular transcription factors, such as the heat-stable nucleoid structuring protein (H-NS) and its antagonist LeuO in E. coli and Salmonella enterica (276,(298)(299)(300). Moreover, certain cellular factors and pathways can control the activation of some CRISPR-Cas systems.…”

Section: Genetic Elements Controlling the Stability Of Mobile Elementsmentioning

confidence: 99%

Bacterial Genome Instability

Darmon

Leach

2014

Microbiol Mol Biol Rev

345

289

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SUMMARY Bacterial genomes are remarkably stable from one generation to the next but are plastic on an evolutionary time scale, substantially shaped by horizontal gene transfer, genome rearrangement, and the activities of mobile DNA elements. This implies the existence of a delicate balance between the maintenance of genome stability and the tolerance of genome instability. In this review, we describe the specialized genetic elements and the endogenous processes that contribute to genome instability. We then discuss the consequences of genome instability at the physiological level, where cells have harnessed instability to mediate phase and antigenic variation, and at the evolutionary level, where horizontal gene transfer has played an important role. Indeed, this ability to share DNA sequences has played a major part in the evolution of life on Earth. The evolutionary plasticity of bacterial genomes, coupled with the vast numbers of bacteria on the planet, substantially limits our ability to control disease.

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Section: Genetic Elements Controlling the Stability Of Mobile Elementsmentioning

confidence: 99%

Bacterial Genome Instability

Darmon

Leach

2014

Microbiol Mol Biol Rev

345

289

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“…This enzyme is important for processing crRNA transcripts with the aid of an RNA molecule and the Cas protein, Cas9. H-NS and LeuO have been shown to regulate the CRISPR system in both Escherichia coli and Salmonella typhi, whereas LRP regulates the S. typhi CRISPR system (13)(14)(15). Other non-cas genes participating in the activity of the CRISPR system have not yet been identified in other bacteria.…”

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confidence: 99%

High-temperature protein G is essential for activity of the Escherichia coli clustered regularly interspaced short palindromic repeats (CRISPR)/Cas system

Yosef

Goren

Kiro

et al. 2011

Proc. Natl. Acad. Sci. U.S.A.

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Prokaryotic DNA arrays arranged as clustered regularly interspaced short palindromic repeats (CRISPR), along with their associated proteins, provide prokaryotes with adaptive immunity by RNAmediated targeting of alien DNA or RNA matching the sequences between the repeats. Here, we present a thorough screening system for the identification of bacterial proteins participating in immunity conferred by the Escherichia coli CRISPR system. We describe the identification of one such protein, high-temperature protein G (HtpG), a homolog of the eukaryotic chaperone heat-shock protein 90. We demonstrate that in the absence of htpG, the E. coli CRISPR system loses its suicidal activity against λ prophage and its ability to provide immunity from lysogenization. Transcomplementation of htpG restores CRISPR activity. We further show that inactivity of the CRISPR system attributable to htpG deficiency can be suppressed by expression of Cas3, a protein that is essential for its activity. Accordingly, we also find that the steady-state level of overexpressed Cas3 is significantly enhanced following HtpG expression. We conclude that HtpG is a newly identified positive modulator of the CRISPR system that is essential for maintaining functional levels of Cas3.defense mechanism | phage-host interactions | positive selection T he clustered regularly interspaced short palindromic repeats (CRISPR) system is a significant defense mechanism of prokaryotes against viruses and horizontally transferred DNA (1-3) and RNA (4). It is found in ∼90% of archaeal genomes and ∼40% of bacterial genomes, and consists of a CRISPR array, usually preceded by a leader DNA sequence, located near a cluster of CRISPR-associated (cas) genes (5-7). RNA transcribed from the CRISPR array (crRNA) is processed by Cas proteins and directs interfering proteins to target DNA/RNA matching the sequences between the repeats. These sequences, called spacers, often originate from plasmids and phages; thus, the system adaptively targets these invaders. High variability is found among bacterial species in the number, sequence, and length of the CRISPR arrays; the sequence and length of the leader DNA; and the number and sequence of the associated proteins. The CRISPR arrays are composed of 2 to ∼250

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“…However, in many cases, the architecture and regulation of bacterial operons are rather more complex, involving many regulatory elements and multiple internal promoters that may be distinctly regulated. Sophisticated regulatory mechanisms have evolved to ensure that the relative expression level of each individual gene meets the necessities of the cell, which may vary under different conditions (4)(5)(6).…”

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confidence: 99%

Regulation of Internal Promoters in a Zinc-Responsive Operon Is Influenced by Transcription from Upstream Promoters

Napolitano

Rubio

Camargo

et al. 2013

Journal of Bacteriology

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In the cyanobacterium Anabaena sp. strain PCC 7120 (also known as Nostoc sp. strain PCC 7120), a zinc-responsive operon (all4725-all4721) has been described, which contains 4 distinct promoters. The two most upstream ones bind Zur with high affinity, whereas the other two do not or do so with a very low affinity. In this paper, a detailed characterization of the four promoters is presented, showing that all four were induced by metal depletion, and they were constitutively derepressed in a zur mutant, despite the two downstream promoters not being direct targets for this regulator. Crucially, induction by metal depletion of the two downstream promoters was abrogated when transcription initiated at the upstream promoters was interrupted by a polar insertion midway in the operon. In contrast, insertion of a nitrogen-responsive promoter at a roughly similar position provoked the two downstream promoters to adopt a regulatory pattern mimicking that of the inserted promoter. Thus, regulation of the two downstream promoters is apparently influenced by transcription from promoters upstream. Evidence is presented indicating that the activity of the two downstream promoters is kept basal in Anabaena by repression. A regulatory model compatible with these results is proposed, where promoters controlled by repression in bacterial operons may be subjected to a hierarchical regulation depending on their position in the operon. According to this model, internal promoters may respond to stimuli governing the activity of promoters upstream by an indirect regulation and to specific stimuli by a direct regulation.

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The CRISPR/Cas Immune System Is an Operon Regulated by LeuO, H-NS, and Leucine-Responsive Regulatory Protein in Salmonella enterica Serovar Typhi

Cited by 101 publications

References 66 publications

Bacterial Genome Instability

Bacterial Genome Instability

High-temperature protein G is essential for activity of the Escherichia coli clustered regularly interspaced short palindromic repeats (CRISPR)/Cas system

Regulation of Internal Promoters in a Zinc-Responsive Operon Is Influenced by Transcription from Upstream Promoters

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