The AraC Negative Regulator family modulates the activity of histone-like proteins in pathogenic bacteria

Santiago, Araceli E.; Yan, Michael; Hazen, Tracy H.; Sauder, Brooke; Meza-Segura, Mario; Rasko, David A.; Kendall, Melissa M.; Ruı́z-Pérez, Fernando; Nataro, James P.

doi:10.1371/journal.ppat.1006545

Cited by 19 publications

(31 citation statements)

References 54 publications

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“…In addition to the already reported Aar-dependent modulation of H-NS2 ( 31 ), we show here that, unlike H-NS, H-NS2 shows temperature- and nutrient-dependent regulation. With respect to temperature, H-NS2 expression is higher at 37°C than at 25°C.…”

Section: Discussionsupporting

confidence: 83%

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Evolution of Bacterial Global Modulators: Role of a Novel H-NS Paralogue in the Enteroaggregative Escherichia coli Strain 042

et al. 2018

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Global regulators such as H-NS play key relevant roles enabling bacterial cells to adapt to a changing environment. H-NS modulates both core and horizontally transferred (HGT) genes, but the mechanism by which H-NS can differentially regulate these genes remains to be elucidated. There are several instances of bacterial cells carrying genes that encode homologues of the global regulators. The question is what the roles of these proteins are. We noticed that the enteroaggregative E. coli strain 042 carries a new hitherto uncharacterized copy of the hns gene. We decided to investigate why this pathogenic E. coli strain requires an extra H-NS paralogue, termed H-NS2. In our work, we show that H-NS2 displays specific expression and regulatory properties. H-NS2 targets a subset of H-NS-specific genes and may help to differentially modulate core and HGT genes by the H-NS cellular pool.

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Section: Discussionsupporting

confidence: 83%

“…It has been recently shown that the plasmid-encoded AraC negative regulator Aar modulates expression of both H-NS and H-NS2 in E. coli strain 042 ( 31 ). We decided to investigate whether, in addition to Aar, environmental or physiological factors influence H-NS2 expression.…”

Section: Resultsmentioning

confidence: 99%

Evolution of Bacterial Global Modulators: Role of a Novel H-NS Paralogue in the Enteroaggregative Escherichia coli Strain 042

et al. 2018

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“…In EAEC, regulation of virulence is mediated by AggR and its negative regulator Aar. Aar controls the expression of at least 210 genes; one-third of these genes are related to metabolism and transport [ 24 ]. We sought to determine the relevance of AggR/Aar-mediated regulation of metabolic pathways in EAEC by performing untargeted metabolomic analysis of EAEC042 and EAEC042 aar .…”

Section: Resultsmentioning

confidence: 99%

“…Since PE and LysoPE species serve as the donor of fatty acids in the N-acylation of apolipoproteins generating lysophospholipids as products of degradation by action of N-acyltransferases, we sought to identify AggR/Aar-regulated proteins with N-acyltransferase activity. With this purpose, we took advantage of previously reported microarray and RNAseq data from EAEC 042 aggR and EAEC 042 aar strains [ 8 , 24 ], which identified one potential hypothetical N-acyltransferase; AatD (CBG27765.1, EC042_pAA011) [ 8 , 25 ]. AatD is encoded in the aat operon and its function remains obscure [ 25 ].…”

Section: Resultsmentioning

confidence: 99%

Characterization of a novel AraC/XylS-regulated family of N-acyltransferases in pathogens of the order Enterobacterales

et al. 2020

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Enteroaggregative Escherichia coli (EAEC) is a diarrheagenic pathotype associated with traveler's diarrhea, foodborne outbreaks and sporadic diarrhea in industrialized and developing countries. Regulation of virulence in EAEC is mediated by AggR and its negative regulator Aar. Together, they control the expression of at least 210 genes. On the other hand, we observed that about one third of Aar-regulated genes are related to metabolism and transport. In this study we show the AggR/Aar duo controls the metabolism of lipids. Accordingly, we show that AatD, encoded in the AggR-regulated aat operon (aatPABCD) is an N-acyltransferase structurally similar to the essential Apolipoprotein N-acyltransferase Lnt and is required for the acylation of Aap (anti-aggregation protein). Deletion of aatD impairs posttranslational modification of Aap and causes its accumulation in the bacterial periplasm. trans-complementation of 042aatD mutant with the AatD homolog of ETEC or with the Nacyltransferase Lnt reestablished translocation of Aap. Site-directed mutagenesis of the E207 residue in the putative acyltransferase catalytic triad disrupted the activity of AatD and caused accumulation of Aap in the periplasm due to reduced translocation of Aap at the bacterial surface. Furthermore, Mass spectroscopy revealed that Aap is acylated in a putative lipobox at the N-terminal of the mature protein, implying that Aap is a lipoprotein. Lastly, deletion of aatD impairs bacterial colonization of the streptomycin-treated mouse model. Our findings unveiled a novel N-acyltransferase family associated with bacterial virulence, and that is tightly regulated by AraC/XylS regulators in the order Enterobacterales.

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“…Illnesses caused by the foodborne enteropathogen and Shiga toxin-producing Escherichia coli O157 (STEC) can be lifethreatening (Nataro and Kaper, 1998;Law, 2001;Santiago et al, 2017). Most of the STEC strains identified by USDA carry toxin genes stx1a and stx2a (González-Escalona and Kase, 2019).…”

Section: Introductionmentioning

confidence: 99%

Xenobiotic Effects of Chlorine Dioxide to Escherichia coli O157:H7 on Non-host Tomato Environment Revealed by Transcriptional Network Modeling: Implications to Adaptation and Selection

et al. 2020

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Escherichia coli serotype O157:H7 is one of the major agents of pathogen outbreaks associated with fresh fruits and vegetables. Gaseous chlorine dioxide (ClO 2) has been reported to be an effective intervention to eliminate bacterial contamination on fresh produce. Although remarkable positive effects of low doses of ClO 2 have been reported, the genetic regulatory machinery coordinating the mechanisms of xenobiotic effects and the potential bacterial adaptation remained unclear. This study examined the temporal transcriptome profiles of E. coli O157:H7 during exposure to different doses of ClO 2 in order to elucidate the genetic mechanisms underlying bacterial survival under such harsh conditions. Dosages of 1 µg, 5 µg, and 10 µg ClO 2 per gram of tomato fruits cause different effects with dose-by-time dynamics. The first hour of exposure to 1 µg and 5 µg ClO 2 caused only partial killing with significant growth reduction starting at the second hour, and without further significant reduction at the third hour. However, 10 µg ClO 2 exposure led to massive bacterial cell death at 1 h with further increase in cell death at 2 and 3 h. The first hour exposure to 1 µg ClO 2 caused activation of primary defense and survival mechanisms. However, the defense response was attenuated during the second and third hours. Upon treatment with 5 µg ClO 2 , the transcriptional networks showed massive downregulation of pathogenesis and stress response genes at the first hour of exposure, with decreasing number of differentially expressed genes at the second and third hours. In contrast, more genes were further downregulated with exposure to 10 µg ClO 2 at the first hour, with the number of both upregulated and downregulated genes significantly decreasing at the second hour.

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The AraC Negative Regulator family modulates the activity of histone-like proteins in pathogenic bacteria

Cited by 19 publications

References 54 publications

Evolution of Bacterial Global Modulators: Role of a Novel H-NS Paralogue in the Enteroaggregative Escherichia coli Strain 042

Evolution of Bacterial Global Modulators: Role of a Novel H-NS Paralogue in the Enteroaggregative Escherichia coli Strain 042

Characterization of a novel AraC/XylS-regulated family of N-acyltransferases in pathogens of the order Enterobacterales

Xenobiotic Effects of Chlorine Dioxide to Escherichia coli O157:H7 on Non-host Tomato Environment Revealed by Transcriptional Network Modeling: Implications to Adaptation and Selection

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