The architectural role of nucleoid-associated proteins in the organization of bacterial chromatin: A molecular perspective

Luijsterburg, Martijn S.; Noom, Maarten C.; Wuite, Gijs J. L.; Dame, Remus T.

doi:10.1016/j.jsb.2006.05.006

Cited by 247 publications

(262 citation statements)

References 79 publications

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“…T he bacterial chromosome is organized into a compact structure composed of topologically independent loops in part as a consequence of interactions with nucleoid-associated proteins (NAPs) (1). H-NS, one of the most abundant NAPs in the Enterobacteriaceae (2), is thought to stabilize the loops by forming long patches that bridge distant DNA to form loop structures of variable size (3).…”

Section: H-ns | Virulencementioning

confidence: 99%

Lsr2 is a nucleoid-associated protein that targets AT-rich sequences and virulence genes inMycobacterium tuberculosis

Gordon

Li²,

Wang

et al. 2010

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

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Bacterial nucleoid-associated proteins play important roles in chromosome organization and global gene regulation. We find that Lsr2 of Mycobacterium tuberculosis is a unique nucleoid-associated protein that binds AT-rich regions of the genome, including genomic islands acquired by horizontal gene transfer and regions encoding major virulence factors, such as the ESX secretion systems, the lipid virulence factors PDIM and PGL, and the PE/PPE families of antigenic proteins. Comparison of genome-wide binding data with expression data indicates that Lsr2 binding results in transcriptional repression. Domain-swapping experiments demonstrate that Lsr2 has an N-terminal dimerization domain and a C-terminal DNA-binding domain. Nuclear magnetic resonance analysis of the DNA-binding domain of Lsr2 and its interaction with DNA reveals a unique structure and a unique mechanism that enables Lsr2 to discriminately target AT-rich sequences through interactions with the minor groove of DNA. Taken together, we provide evidence that mycobacteria have employed a structurally distinct molecule with an apparently different DNA recognition mechanism to achieve a function similar to the Enterobacteriaceae H-NS, likely coordinating global gene regulation and virulence in this group of medically important bacteria.

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Section: H-ns | Virulencementioning

confidence: 99%

Lsr2 is a nucleoid-associated protein that targets AT-rich sequences and virulence genes inMycobacterium tuberculosis

Gordon

Li²,

Wang

et al. 2010

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

198

250

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“…Bacterial NAPs (e.g., the 9-kD HU, 11-kD Fis [for factor for inversion stimulation] and 15 kD H-NS proteins) have in common a low molecular mass, a high Lys content, and nonspecific binding to DNA (Luijsterburg et al, 2006;Dillon and Dorman, 2010) and to other nucleic acids (Balandina et al, 2002;Brescia et al, 2004;Kamashev et al, 2008). SWIB-4 has a histonelike domain that is likely to be involved in binding to DNA as well as RNA and single-stranded DNA as also shown for histones (Spelsberg et al, 1970).…”

Section: Discussionmentioning

confidence: 99%

The Core of Chloroplast Nucleoids Contains Architectural SWIB Domain Proteins

et al. 2012

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A highly enriched fraction of the transcriptionally active chromosome from chloroplasts of spinach (Spinacia oleracea) was analyzed by two-dimensional gel electrophoresis and mass spectrometry to identify proteins involved in structuring of the nucleoid core. Among such plastid nucleoid-associated candidate proteins a 12-kD SWIB (SWI/SNF complex B) domaincontaining protein was identified. It belongs to a subgroup of low molecular mass SWIB domain proteins, which in Arabidopsis thaliana has six members (SWIB-1 to SWIB-6) with predictions for localization in the two DNA-containing organelles. Green/red fluorescent protein fusions of four of them were shown to be targeted to chloroplasts, where they colocalize with each other as well as with the plastid envelope DNA binding protein in structures corresponding to plastid nucleoids. For SWIB-6 and SWIB-4, a second localization in mitochondria and nucleus, respectively, could be observed. SWIB-4 has a histone H1 motif next to the SWIB domain and was shown to bind to DNA. Moreover, the recombinant SWIB-4 protein was shown to induce compaction and condensation of nucleoids and to functionally complement a mutant of Escherichia coli lacking the histone-like nucleoid structuring protein H-NS.

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“…Two nonstructural components with ancillary roles in translation were also up-regulated in the gonad: polypeptide deformylase (Mazel et al 1994) and a predicted S-adenosyl-L-methionine-dependent methyltransferase (Pleshe et al 2005;Savic et al 2009). Additionally, evidence for a higher rate of DNA replication in this tissue relative to the soma was apparent in the increased expression of uracil-DNA glycosylase, a key enzyme of the base excision system (Holmquist 1998), and a nucleoid DNA-binding protein of the HU family, which exhibits peak expression during the exponential phase of growth in Escherichia coli (Luijsterburg et al 2006). Moreover, the up-regulated gene annotated as a ''cardiolipin synthase'' has a conserved domain with closer homology with Nuc, an EDTA-resistant nuclease that digests nucleic acids without sequence specificity (Pohlman et al 1993).…”

Section: Differential Expression Analysis Supports Limited Regulationmentioning

confidence: 99%

Analysis of gene expression from theWolbachiagenome of a filarial nematode supports both metabolic and defensive roles within the symbiosis

et al. 2012

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The a-proteobacterium Wolbachia is probably the most prevalent, vertically transmitted symbiont on Earth. In contrast with its wide distribution in arthropods, Wolbachia is restricted to one family of animal-parasitic nematodes, the Onchocercidae. This includes filarial pathogens such as Onchocerca volvulus, the cause of human onchocerciasis, or river blindness. The symbiosis between filariae and Wolbachia is obligate, although the basis of this dependency is not fully understood. Previous studies suggested that Wolbachia may provision metabolites (e.g., haem, riboflavin, and nucleotides) and/or contribute to immune defense. Importantly, Wolbachia is restricted to somatic tissues in adult male worms, whereas females also harbor bacteria in the germline. We sought to characterize the nature of the symbiosis between Wolbachia and O. ochengi, a bovine parasite representing the closest relative of O. volvulus. First, we sequenced the complete genome of Wolbachia strain wOo, which revealed an inability to synthesize riboflavin de novo. Using RNA-seq, we also generated endobacterial transcriptomes from male soma and female germline. In the soma, transcripts for membrane transport and respiration were up-regulated, while the gonad exhibited enrichment for DNA replication and translation. The most abundant Wolbachia proteins, as determined by geLC-MS, included ligands for mammalian Toll-like receptors. Enzymes involved in nucleotide synthesis were dominant among metabolism-related proteins, whereas the haem biosynthetic pathway was poorly represented. We conclude that Wolbachia may have a mitochondrion-like function in the soma, generating ATP for its host. Moreover, the abundance of immunogenic proteins in wOo suggests a role in diverting the immune system toward an ineffective antibacterial response.

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The architectural role of nucleoid-associated proteins in the organization of bacterial chromatin: A molecular perspective

Cited by 247 publications

References 79 publications

Lsr2 is a nucleoid-associated protein that targets AT-rich sequences and virulence genes inMycobacterium tuberculosis

Lsr2 is a nucleoid-associated protein that targets AT-rich sequences and virulence genes inMycobacterium tuberculosis

The Core of Chloroplast Nucleoids Contains Architectural SWIB Domain Proteins

Analysis of gene expression from theWolbachiagenome of a filarial nematode supports both metabolic and defensive roles within the symbiosis

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