Nucleoid-associated proteins encoded on plasmids: Occurrence and mode of function
Introduction
Plasmids (extrachromosomal replicons) are one of the most important ‘vehicles’ of genes for resistance to antibiotics, metabolism of natural and synthetic compounds, pathogenicity, and host symbiosis. Plasmid transfer is involved in the rapid evolution and adaptation of microbes by transferring specific traits among different host microbes. After a host cell receives a plasmid, integration of the newly acquired genetic elements into the host cell (the successful survival of a plasmid in a host cell) is required to maintain host cell fitness. Several studies have shown that carrying a plasmid is a ‘burden’ on the host because the replication and maintenance of plasmids perturbs host transcriptional networks (Nojiri, 2013, Shintani, 2014). Two mechanisms of plasmid integration into host cells have been described as ‘physical integration’ and ‘regulatory integration’ (Dorman, 2014).
Over the last 10 years, nucleoid-associated proteins (NAPs) have been shown to be involved in folding chromosomal DNA to make it more compact through their DNA-binding ability, which is important for the regulation of transcriptional networks in hosts (Dillon, Dorman, 2010, Nojiri, 2012). One of the best studied NAPs is histone-like nucleoid structuring protein (H-NS) in enterobacteria. Other NAPs have been identified, including factor for inversion stimulation (FIS), histone-like protein from Escherichia coli strain U93 (HU), integration host factor (IHF), and leucine-responsive regulatory protein (Lrp) (Dillon and Dorman, 2010). NdpA (sometimes named YejK in E. coli) is a functionally unknown NAP included in the nucleoid of E. coli and Pseudomonas aeruginosa (Murphy, 1999, Ohniwa, 2011). Some of these NAP genes have been found on plasmids and are thought to play an important role in the integration and adaptation of plasmids into new host cells (Takeda et al., 2011). Recently, Dorman (2014) suggested that NAPs can be used to reduce fitness costs through physical and regulatory integration of plasmids into host cells. In the present study, the distributions of NAP genes on plasmids and their host chromosome(s) were determined as a follow-up to our previous study (Takeda et al., 2011). Recent studies on NAP genes found in plasmids and their (putative) roles in host cells are described.
Section snippets
H-NS family proteins
H-NS, one of the best-characterized NAPs, was shown in the 1970s to be a heat-resistant protein that activates transcription in bacterial cells, and was ‘re-discovered’ as a histone-like protein in bacteria 10 years later (Lammi, 1984, Navarre, 2010). A large number of excellent reviews are available (Dorman, 2004, Dorman, 2014, Fang, Rimsky, 2008, Navarre, 2010, Stoebel, 2008). H-NS is found in the genera Escherichia and Salmonella, whose amino acid sequences show 95% identity. It is one of
Method used to analyze the distribution of NAP genes in genomes
We previously determined the distributions of NAP genes on plasmids and chromosomes (Takeda et al., 2011). Amino acid sequences of H-NS family proteins (H-NS, Ler, MvaT, BpH3, Bv3F, HvrA, Lsr2, XrvA, and Rok) and other NAPs (FIS, HU, IHF, Lrp, and NdpA) were used; their accession numbers in the DDBJ/EMBL/GenBank databases are provided in Table 1. Complete sequences of 4602 plasmids (plasmid database) listed in GenBank (Aug. 2014) and 3279 complete genome sequences of bacteria (genome database,
Functional analyses of NAPs encoded on plasmids
Most reports of NAPs encoded on plasmids have focused on H-NS family proteins, and there are no reports exploring the function of other NAPs encoded on plasmids except for our recent report (Suzuki-Minakuchi et al., 2015). Recent studies that included functional analyses of H-NS family proteins encoded on the plasmids of Enterobacteriaceae and Pseudomonas are described will be discussed later.
Concluding remarks
The present study focused on the roles of NAPs encoded on plasmids and their relationships with those in host chromosomes. H-NS family proteins are thought to be major factors for plasmid integration into host cells. Other NAPs are thought to be important for plasmid replication, maintenance, and transfer. There were many plasmids on which NAP genes were not found, despite their large size and high GC content (Fig. 2). There may be more unidentified NAP genes on plasmids such as H-NSIncA/C, and
Acknowledgments
This work was partially supported by JSPS KAKENHI grant number 24780087 to M.S. and 24380043 to H.N.
References (116)
Indirect recognition in sequence-specific DNA binding by Escherichia coli integration host factor: the role of DNA deformation energy
J. Biol. Chem
(2006)Silencing of foreign DNA in bacteria
Curr. Opin. Microbiol
(2012)Structural insights into the regulation of foreign genes in Salmonella by the Hha/H-NS complex
J. Biol. Chem
(2013)- et al.
Twelve species of the nucleoid-associated protein from Escherichia coli. Sequence recognition specificity and DNA binding affinity
J. Biol. Chem
(1999) Differential functional properties of chromosomal- and plasmid-encoded H-NS proteins
Res. Microbiol
(2011)HU protein of Escherichia coli binds specifically to DNA that contains single-strand breaks or gaps
J. Biol. Chem
(1995)The repABC plasmid family
Plasmid
(2008)- et al.
Variation in HU composition during growth of Escherichia coli: the heterodimer is required for long term survival
J. Mol. Biol
(1997) - et al.
Structure of the Escherichia coli leucine-responsive regulatory protein Lrp reveals a novel octameric assembly
J. Mol. Biol
(2007) Structural basis for H-NS-mediated trapping of RNA polymerase in the open initiation complex at the rrnB P1
J. Biol. Chem
(2002)
H-NS-like nucleoid-associated proteins, mobile genetic elements and horizontal gene transfer in bacteria
Plasmid
New insights into transcriptional regulation by H-NS
Curr. Opin. Microbiol
On the origin of the selectivity of plasmidic H-NS towards horizontally acquired DNA: linking H-NS oligomerization and cooperative DNA binding
J. Mol. Biol
Global gene expression profiling in Escherichia coli K12. The effects of leucine-responsive regulatory protein
J. Biol. Chem
Diversity, biology and evolution of IncQ-family plasmids
Plasmid
The architectural role of nucleoid-associated proteins in the organization of bacterial chromatin: a molecular perspective
J. Struct. Biol
Complete nucleotide sequence of carbazole/dioxin-degrading plasmid pCAR1 in Pseudomonas resinovorans strain CA10 indicates its mosaicity and the presence of large catabolic transposon Tn4676
J. Mol. Biol
Impact of catabolic plasmids on host cell physiology
Curr. Opin. Biotechnol
Differential binding of the Escherichia coli HU, homodimeric forms and heterodimeric form to linear, gapped and cruciform DNA
J. Mol. Biol
Structure of the histone-like protein H-NS and its role in regulation and genome superstructure
Curr. Opin. Microbiol
Mechanism of chromosome compaction and looping by the Escherichia coli nucleoid protein Fis
J. Mol. Biol
IHF and HU: flexible architects of bent DNA
Curr. Opin. Struct. Biol
Spread and survival of promiscuous IncP-1 plasmids
Acta Biochim. Pol
Growth phase-dependent variation in protein composition of the Escherichia coli nucleoid
J. Bacteriol
The Hha protein facilitates incorporation of horizontally acquired DNA in enteric bacteria
Microbiology
Differential regulation of horizontally acquired and core genome genes by the bacterial modulator H-NS
PLoS Genet
Shigella flexneri 2a strain 2457T expresses three members of the H-NS-like protein family: characterization of the Sfh protein
Mol. Genet. Genomics
The structural and functional organization of H-NS-like proteins is evolutionarily conserved in gram-negative bacteria
Mol. Microbiol
H-NS cooperative binding to high-affinity sites in a regulatory element results in transcriptional silencing
Nat. Struct. Mol. Biol
Effects of Fis on Escherichia coli gene expression during different growth stages
Microbiology
A fundamental regulatory mechanism operating through OmpR and DNA topology controls expression of Salmonella pathogenicity islands SPI-1 and SPI-2
PLoS Genet
Resistance plasmid families in Enterobacteriaceae
Antimicrob. Agents Chemother
H-NS family members function coordinately in an opportunistic pathogen
Proc. Natl. Acad. Sci. U.S.A.
Genome-scale reconstruction of the Lrp regulatory network in Escherichia coli
Proc. Natl. Acad. Sci. U.S.A.
Genome-wide analysis of Fis binding in Escherichia coli indicates a causative role for A-/AT-tracts
Genome Res
Escherichia coli DnaA interacts with HU in initiation at the E. coli replication origin
Mol. Microbiol
A consensus sequence for binding of Lrp to DNA
J. Bacteriol
DNA bridging: a property shared among H-NS-like proteins
J. Bacteriol
Three-way interactions among the Sfh, StpA and H-NS nucleoid-structuring proteins of Shigella flexneri 2a strain 2457T
Mol. Microbiol
Advancing the qorum in Pseudomonas aeruginosa: MvaT and the rgulation of N-acylhomoserine lactone production and virulence gene expression
J. Bacteriol
Bacterial nucleoid-associated proteins, nucleoid structure and gene expression
Nat. Rev. Microbiol
Genome-wide analysis of the H-NS and Sfh regulatory networks in Salmonella Typhimurium identifies a plasmid-encoded transcription silencing mechanism
Mol. Microbiol
Growth phase variation of integration host factor level in Escherichia coli
J. Bacteriol
H-NS: a universal regulator for a dynamic genome
Nat. Rev. Microbiol
Regulation of transcription by DNA supercoiling in Mycoplasma genitalium: global control in the smallest known self-replicating genome
Mol. Microbiol
Reciprocal transcriptional and posttranscriptional growth-phase-dependent expression of sfh, a gene that encodes a paralogue of the nucleoid-associated protein H-NS
J. Bacteriol
An H-NS-like stealth protein aids horizontal DNA transmission in bacteria
Science
The locus of enterocyte effacement (LEE)-encoded regulator controls expression of both LEE- and non-LEE-encoded virulence factors in enteropathogenic and enterohemorrhagic Escherichia coli
Infect. Immun
Proteins from the prokaryotic nucleoid: primary and quaternary structure of the 15-kD Escherichia coli DNA binding protein H-NS
Mol. Microbiol
The xrvA gene of Xanthomonas oryzae pv. oryzae, encoding an H-NS-like protein, regulates virulence in rice
Microbiology
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Contributed equally to this work.